Vertebrate Embryology - Randel PDF

Introduction to
VERTEBRATE-
EMBRYOLOGY
Introduction to
VERTEBRATE
EMBRYOLOOi
FIFTH EDITION
WALDO SHUMWAY
Dean, Stevens Institute
F. B. ADAMSTONE
Professor of Zoology
University ot Illinois
*Nb<^
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New Yor^c • JOHN W I L E y & .S

London • CHAPMAN Si HAL
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TODAYS TOrjORROWS tÔu AC"
U^BASn HARPHUHstlGfl "'
CoETEiGHT, 1027, 1B30, 1935, 1642
BY
WALDO S H U M W A T
COPYKIGHT, 1954
BY
J O H N WILEY & SON&, I N C .
All Rights Reserved

This look er any pari thereof iriusl not
he reproduced in dtty for-m loithoi^t the
•written permisson of the •jmllisher.
To
E. S. S.
and
F. S. S.
Preface
The preparation of a fifth edition of this book is long overdue, but
the events of the past ten years have interrupted the normal course •
of events in many situations. Dr. Shumway was in service with the
Army during World War II and since then has gone into another field
of work. Thus the task of carrying out a revision of this book for a
new edition fell largely to my lot.
In a general sort of way every effort has been made to retain those
features of the original book which have been so successful. The book is
again organized on a comparative basis, and the,general account of the
developmental process is supplemented by detailed material relating
to the amphioxus, the frog, the chick, and man. Sufficient material is
provided on each of them so that considerable stress may be laid
on one or more at the wish of the instructor. The subject matter is
also treated again both from the morphological and physiological
viewpoints—a procedure which undoubtedly makes the subject much
more interesting to the student. Basic material from the field of
experimental embryology is incorporated in the body of the text, for
this material has assumed such -fundamental importance that it can
no longe^ be omitted from consideration even in the most elementary
treatment of the subject. The subject matter of this chapter, however,
has been largely restricted to a discussion of the processes underlying
the early stages of development. Other material from experimental
studies is incorporated at various points in the body of the book
\Yithout special emphasis. It is recognized, nfloreover, that the subject
matter of experimental embryology is now so extensive that it con-
stitutes a separate (field of study in itself.
An attempt has been made to bring the different topics up to date,
and modification of the account of early development in the chick
has been particularly necessary. Above all, however, an effort has
been made to preserve the objective of presenting a broad factual out-
line of the information that is necessary for the acquisition of a sound,
basic knowledge of the subject, on which the interested student will
be able to build.
The illustrations have been extensively revised to insure uniformity
^"i Preface
t Z ^ ^ J , f'''''^' * ' '•'^"'•'^^^ '^^'^'^'' of this material.

Much of this work has been done by Mr. Charles McLaughlin, artist
of the Zoo ogy Department of the University of Illinois, but many of
the beautiful ongmal figures by Mrs. Katharine Hill Paul have been'
reTaiTiArl
retained
It IS a pleasure at this time, also, to extend my thanks to many of
my colleagues in the Zoology Department at the University of Illinois,
in particular to Dr. S. Meryl Rose and Dr. Francis Kruidenier, who
have read various sections of the text, as well as to Dr. AV. M. Luce
and Dr. J. B. Kitzmiller for criticism of the portions relating to genetics.
r, , ,„, . F- B. ADAMSTONE
Urbana, Illmots
March, 195^
Contents
CHAPTER PAGE
1. The study of Embryology 1
2. Reproductive Habits and Vertebrate Life Histories . . 10
3. The Germ Cells—^Their Structure, Origin, and Development . 24
4. Fertilization . . . . . . . . . 47
5. The Mechanism of Heredity 58
6. Cleavage and Formation of the Blastula . . . . 79
7. Gastrulation and Neurulation . . . . . . 93
8. Embryonic Form and E.xtraembryonic JMembranes . . 115-
9. The Reproductive Cycle and Placenta of the Mammal . . 135
10. Experimental Embryology . . . . . . 146
11. Digestive System and Related Structures . . . . 171
12. Respiratory Organs . . . . . . . . 188
13. Coelom and Mesenteries . . . . . . . 194
14. The Urinogeniial System . . . . . . 201
15. Blood Vascular System 222
16. The Skeleton 242
17. Muscles . , 253
18. Integument 258
19. Nervous System 263
20. Nerve Terminations . . . . . . . 283

X Contents
21. Atlas of Vertebrate Embryos . 295
22. Embryological Technique 334
Glossary . . . . 351
Bibliography . . . . 369
Index . . . . . . 373
T
The Study of Embryology

Embryology may be defined as that division of biological science
which deals with the development of the individual organjsm.. It is
concerned primarily with the orderly series of changes in form and func-
tion by which the initial germ of the new individual is transformed into
a sexually mature adult. In addition, modern experimental embry-
ology seeks to determine the causes of these changes and the nature of
the processes underlying them. Among vertebrate animals, at least, the
germ with which development begins is normally an egg cell that has
been fertilized by a sperm. These cells are the germ cells produced by
the parental organisms when they reach sexual maturity, the male de-
veloping sperm cells, and the female, eggs or ova. Sometimes the word
ontogeny is also employed to designate the period of embryonic devel-
opment, but, more often, the term is used to define the entire life
history of an individual from its origin to its death.
Early Embryologists
• Speculation regarding the^process of development particularly as it
relates to man himself undoubtedly goes back far beyond the written
record. I t is desirable, therefore, at the outset, to review the history
of this science in order to become acquainted with the contributions of
some of the earlier^ workers and also to learn something of the evolution
of scientific thougJit in this field.
(<S[ristotlg^384-322 B.C.) . The earliest treatise on embryology which
has been preserved is Aristotle's work entitled De Generatione Ani-
mqlium, which describes the reproduction and development of many
kinds of animals. Another treatise, De Historia Animaliuin, gives the •
first account of the development of the hen's egg. These works show
great powers of (Observation, skill in comparison, and imagination in
interpretation. From our standpoint, however, Aristotle's most sig-
nificant contribution was his conclusion, based on his observations on
the hen's egg, that devejopment always proceeds from simple, formless
beginnings to the complex organization of the adult. He pointed out
1
2 The Study of Embryology
that, in the early embryo, he could see certain structures such as the
heart, blood vessels, etc., but no trace of other organs such as the lungs
appeared until later. He concluded, therefore, that all structures
are not present from the beginning, but that they develop in suc-
cession until the adult condition is attained. This explanation of
the process of development is the basic concept of the theory of
"epigenesis."
William Harvey (1578-1657). This is another famous name in em-
bryology. His book, Emrcitationes de Generatione Animalium, is
based largely on the development of the chick, which he described in
great detail, although lie too was limited bj' the fact that the micro-
scope had not yet come into general use. One of his contributions was
a careful study of the development of the deer, which he compared with
the chick. From purely theoretical considerations he came to the con-
clusion that mammals also formed eggs. The dictum "Ex ovo omnia"—
all animals arise from eggs—is found on the frontispiece of the first
editions of his book.
Marcello Malpighi (1628-1694). By thi« time the microscope in-
vented by the Jensen brothers (1592) had come into fairly wide use, and
with it Malpighi restudied the development of the hen's egg. He pub-
lished an account of this work in the Proceedings of the Royal Society of
London in an article entitled "De Ovo Incubato." This was illustrated
with excellent figures of the developing chick beginning with the unin-
cubated egg and showing the gradual increase in complexity of such
structures as the heart, blood vessels, and brain. Then, in spite of
these precise and accurate observations, he stated his conclusion that
the-various parts of the embryo were already contained in the egg,
fully formed, just as a miniature plant is present in the seed and
beconies visible as it increases in size. This concept of the process of
development is known as the "preformation theory" as opposed to
' Aristotle's theory of epigenesis.
• After Malpighi's time, the microscope came into much wider use and
many remarkable discoveries were made with the newly invented
instrument. Anthony van Leeuwenhoek (1632-L723) made many
microscopes of his own and did much to improve the instrument. He
made numerous studies of natural objects, and, among other things,
discovered spermatozoa in human seminal fluid. lb was not until
many years later, however, that the real significance of these structures
in the process of fertilization was thoroughly understood.
The enthusiasm resulting from such discoveries led to many wholly
imaginative accounts of miniature adults in eggs and sperm. Thus,
•Hartsoeker (1694) illustrated a miniature human being in the sperm.
T h e Study of Embryology 3
These speculations led ultimately to the theory of emboitement first
sponsored by Bonnett. This idea in its final form held.that each germ
cell of the'female parent contained a miniature individual. Moreover,
each of these, in turn, must also contain a miniature offspring; and so
on, for all future generations of the race. It is highly improbable that
Bonnett himself would have subscribed to the elaborate theory which
was finally evolved.
Caspar Friedrich Wolff (1733-1794). Although the preformation
theory was widely accepted, some investigators found reason to doubt
its vahdity. Among these, Wolff made a very careful study of the
development of the intestine of the chick and demonstrated that the
tubuJar gut arose from the folding and remolding of a flat layer of
tissue in the embryo at an early stage of incubation. This was a direct
refutation of the preformationist idea, which held that the intestine
was present as a tubular structure from the start. Thus, Wolff in his
Theoria Generationis not only attacked the theory of pi-eformation on
purely logical grounds but also presented strong scientific evidence to
support his views. In spite of this, it was not until sometime later that
the theory of epigenesis was reestablished as the accepted explanation
of the developmental process.
Toward the end of the 19th century the larger divisions of the field
of embryology were mapped out, and the foundations were laid for the
great progress of the 20th century. A brief review of these develop-
ments is given below.
Comparative Embryology
Karl Ernst von Baer (1792-1876) is often spoken of as the father
of modern embryology. He discovered the egg of the dog (1827) and
other mammals, thus substantiating the ideas of William Harvey. He
made exhaustive studies on the embryo of the chick and various other
animals and further elaborated the "germ-layer" concept of Wolff so
that it was raised to the status of a general law. It is often called the
theory of the "specificity of the germ layers," implying that the various
structures of the body arise from the same germ layers in different
species of animals. Von Baer also published a book on animal devel-
opment (1828-1837), in which he compared in detail the development
of different animal's. From these he drew four important conclusions,
known as von Baer's laws:
" 1 . The more general characteristics of any large group of animals
appear in the embryo earlier than the more special characteristics.
"2. After the more general characteristics, those that are less general
arise, and so on until the most special characteristics appear.
4 T h e Study of Embryology
"3. The embiyo of any particular kind of animal grows more unlike
the forms of other species instead of passing through them.
"4. The embryo of a higher species may resemble the embryo of
a lower species but never resenables the adult form -of that species."
From the time of von Baer to the present, the history of embryology
has been maiked by increasing specialization. Thus the field of com-
parative embryology falls readily into two subdivisions, viz., vertebrate
and invertebrate. Nevertheless, the two are very intimately con-
nected and the study of comparative invertebrate embryology has
thrown much light on vertebrate embryology because many marine
invertebrates lend themselves readily to experimental procedures
Cellular Embryology
Soon after the first volume of von Baer's treatise appeared, Schleiden
and Schwann (1838, 1839) announced the cell theory, stating that all
living things are composed of, and arise from, living units known as
cells. This resulted in an intensive study of the part played by indi-
vidual cells in the development, of the new organism commencing, in
the latter part of the 19th century, with the germ cells, their origin and
fertilization. In 1878, Charles Otis Whitman (1842-1910) traced for
the first time a detailed history of cells formed by the dividing egg in
the leech (Clepsine), thereby initiating the study of cell lineage. Be-
ginning about 1925 this phase of embryology has been greatly broad-
ened by the adoption of modern experimental techniques, which make
it possible to mark the tissues of the developing embryo so that they
may be recognized in their final position in the embryo. Cellular
erhbryology is, therefore, a subject which unites embryology with
cytology, for it has come to be realized that the structure and activi-
ties of the cells of the embryo are of tundamenCal impoetance in the
process of development.
Genetics and Embryology

I n 1866, Gregor Mendel (1822-1884) first carried on successful ex-
periments in breeding plants to discover the laws by which individual
characteristics are inherited by one generation from another. . His
contributions were long unrecognized, but, iir WOO, they were redis-
covered independently both in Europe and in the United States. In
addition, certain other discoveries had been made regarding the be-
havior of the chromosomes in the developing germ cells, which led
Sutton to suggest that the behavior 'of the chromosomes afforded a
mechanical explanation of Mendel's laM'S) and to formulate the chromo-
somal'theory of inheritance. This theory was further elaborated by
Johannsen (1911), who developed the theory of the gene, a name pro-
posed for the ultimate unit of heredity. This theory in the hands of
T. H. Morgan and others has assumed a great importance to embryolo-
gists, for, to quote Brachet, "Embryology is fundamentally the study
of heredity in action." Hence, the aim of embryologists from the stand-
point of genetics is to determine how the gene produces its effect in
•the developing organism. Much fundamental work has been done in
this field beginning with the work of Ephrussi and other investigators.
Phylogeny and Embryology

In 1859 Charles Darwin published his book, Origin oj Species. This
led not only to a great deal of controversy but also to a great deal
of scientific work, as a result of which embryology profited greatly.
In 1866, Ernst Haeckel (1834-1919) published a theory which he be-
lieved supported Darwin-'s theory of evolution. He called it the "funda-
mental biogenetic law." I t is more often known as the recapitulation
theory. This theory states that ontogeny,is a brief and incomplete
recapitulation of phylogeny; that is to say, an animal passes through
stages in its development comparable to those through which its ances-
tors passed in their evolution. So far as the vertebrates are concerned,
this would mean that a mammalian embryo must pass through stages
which are definitely fish-like and later through stages which are essen-
tially reptilian. The fact is that, although there are individual char-
acteristics which may be reminiscent of fish-like or reptilian ancestors,
there is never a time in the development of a mammal when it could
be mistaken for a fish or a reptile. There are evidences that the verte-
brates do retain in embryonic development certain features which also
appeared in the development of their ancestors. For example, clefts
appear in the pharynx of the embryos of birds and mammals, opening
to the exterior just as they do in the embryos of fish. In the adult
fish these clefts contain the gills, but this is not true of adult reptiles,
birds, or mammals. It has been found very difficult, if not impossible, •
to draw up a genealogical tree of the vertebrates based solely on
embryological data. Hence the recapitulation theory is not accepted
and applied so unreservedly as formerly.
Experimental Embryology
Among Haeckel's contemporary opponents was Wilhelm His (1831-
1904), who directed attention to the physiology of the embryo. Deny-
ing the theory of recapitulation, he called attention to the mechanical
processes by which the various structures of the embryo arise from
particular regions of the germ. Later, Wilhelm Roux (1850-1924) put
the study of experimental embryology on a firm basis when he pub-
lished a program for the new science, which he called the "mechanics
of development." This has led to an intensive attack upon the prob-.
lems of development from the physicochemical side, which is carried
on actively at the present time. Weismann (1834-1913), a leader in
theoretical embryology, suggested a theory of chromosomal inheritance
which came very close to the mark. Jacques Loeb (1859-1924) dis-
covered a method of inducing development in unicrtilized eggs (artifi-'
cial parthenogenesis), which has led to extensive research on the nature
of fertilization.
More recently the basic studies of Vogt (1929) and others on the
segregation of the potential organ-forming regions of the early embryo '
and the demonstration by Spemann of the role of the organizer in
development have led to important discoveries relating to the me-
chanics of development. As more refined techniques have been devel-
oped and applied, more detailed analysis of the process of development
has become possible and much progress has been made in relation to
the differentiation of specific organ fields, the phenomena of induction,
competence, etc. Even the part played by the gene has begun to come
under investigation.
Another branch of the science of embryology which has become a
field of major importance is chemical embryology. The basic work in
this field has been summarized in the monumental works of Joseph
Needham and Brachet. Much progress has also been made in regard
to the metabolic aspects of development, including such phases as the
role of food substances, enzyme activity, hormonal control, and various
other, conditions affecting development.
Some of the chief developments of the first half of the 20th century
are outlined briefly in the table appended to this chapter, but the field
of experimental embryology is so vast that in a book of this scope no
attempt can be made to mention the names and contributions of other
men still alive who are-actively engaged in this work. To do so the
roll of distinguished embryologists here and abroad would have to be
called!
T h e Value of Ertibryology
To the student who specializes- in zoology, embryology has a par-
ticular importance because it deals with the origin and development
of the adult body. There is a fascination in tracing out the history of
the different anatomical structures as they take form, grow, and gradu-
ally assume the appearance familiar to-us in the mafciare animal. In
the history of the different organs are found elues to their relationship
and functions. Everyone knows, for example, that the adrenal gland
secretes a hormone, epinephrin, which, circulating in the blood, rouses
the sympathetic nervous system to greater activity. But in embryol-
ogy the student learns that the part of the adrenal gland which, secretes
epinephrin is derJT'ed from those same ganglia which give rise to the
sympathetic nerves.
• He also finds clues to ancestral relationships. Even though the
recapitulation theoQ- has been abandoned as an explanation of devel-
opment, embryologists recognize that there are structures in the body
which correspond to similar parts used for the same or different pur-
poses in the bodies of some distant ancestor. The "retention theory"
has been proposed by de Beer as an explanation. Thus the vestigial
tail of the human embryo arises in the same place and manner as the
tails of other vertebrates, and it may be that some remote prehuinan
ancestor sported and made use of a tail. The embryo retains this tail
not as a recapitulation of ancestral history but because it inherits the
genes which initiate the development of a tail. So the student of com-
parative anatomy often turns to embryology hoping to find homologies
in the mode of origin and manner of development of the adult organs
in which he is interested.
The modern student of embryology is concerned mainly with the
dynamics of development. He examines the protoplasmic organization
of the egg and the sperm, their genetic constitution, and the nature
of the process by which the sperm initiates development in the egg.
He traces the history of the different cells into which the egg divides
and tries to learn the way in which differentiation takes place. He is
interested in the mechanics of the processes by which these cells arrange
themselves into the different germ layers, and how the different organs
arise.
To these problems he brings the methods of descriptive embryology:
the delicate technique of preparing embryological material, the skilled
use of the microscope and its accessories, the interpretation and recon-
struction of his prepared material. He also uses the methods of ex-
perimental embryology: the alteration of the normal conditions of
development, new genetic complexes, altered enviranmental conditions
at different stages of development, the development of individual cells
or parts of the emlpryo in isolation or transplanted into new positions
or different hosts.
Embryology is not an easy subject. It requires a high type of visual
imagination. The student must bear in mind that he is dealing with
living objects, three-dimensional and continually changing in volume,
shape, and constitution. Much of his attention must be given to the
cells of the embryo, as they multiply, migrate, take on different appear-
ances, and carry on different functions. But he must always remember,
that the embryo has a life of its own to lead and that all the different
cells and cell groups in the embryonic body must work in harmony if
the development of the embryo is normal. He must not lose sight of
the embryo-as-a-whole.
The -student preparing for medicine has a professional interest in
embryology. Teachers of human anatomy have long since agreed that
a knowledge of embryological relationships is the best possible prep-
aration for the study of human anatomy. A good working acquaintance
with the outlines of human embryology is prerequisite to the study of
obstetrics. The practitioner of medicine must be prepared to answer'
all sorts of questions about human development.
Any approach to the subject of vertebrate embryology whether
morphological or experimental must be preceded by the acquisition of
a sound knowledge of the basic pattern of development. Two different
methods of approach are available. By the first method the different
types of development are taken up one after another, e.g., amphioxus,
frog, chick, man. The second method consists of discussing the differ-
ent topics of embryology in turn '(e.g., development of the digestive sys-
tem) and comparing the conditions found in each of the types. In thiff
book, the second, or comparative rhethod is employed. It is helpful
also to examine briefly the life histories of each of the types to be used
in later discussion. This will serve to introduce the main stages of
embryology and also to point out the different conditions under which
development takes place.
^ The Study of Embryology 9
IMPORTANT EVENTS IN THE HISTORY OF EMBRYOLOGY
Embryology in the Classic Period
4th century B.C. Aristotle
Embryology in the Renaissance Period
(Before the general use of the microscope)
. 1651 Harvey Epigenesis
(After the general use of the microscope)
1672 Malpighi Preformation
1768 Wolff Epigenesis
Embryology in the Nineteenth Century
1828 von Baer Comparative embryology
1839 Schleiden and Schwann Announced cell theory
1859 Darwin Announced theory of natural
selection
1866 Haeckel Biogenetic law
1866 Mendel Announced laws of inheritance
(Microscopic technique being developed)
1874 His Experimental embryology
1878 Whitman Cell lineage
1883 Roux Mechanics of development
1891 Weismann Theory of the germplasm
1899 Loeb ArtifiQial parthenogenesis
Embryology in the Twentieth Century
1900 ^,--'''Suttogj.< Chromosomal theory of in-
^-——^^^^^^^^-^"'^ heritance
1900 Driesch Theory of pluripotency
1905 Conklin Determinate vs. indeterminate
cleavage
1911 Johannsen Theory of the gene
1929 Vogt Theory of presumptive organ
regions
1929 Holtfreter Chemical aspects of induction
1933 Child Axial-gradient theory
1934 Spemann, Mangold Organizer concept
1932 et seq. lileedham, Brachet Chemical embryology
1937 et seq. Dalcq, Pasteels, Weiss Field concept of development
1938 et seq. Waddington, Ephrussi Genie control of development
(.Specialized Phases of Embryology
1924 et seq. Weiss Regeneration
1924 et seq. Detwiler Neuroembryology
Reproductive Habits
and Vertebrate Life Histories
When the vertebrate organism becomes a sexually mature adult, it
has reached the time when reproduction normally takes place. In many
species characteristic changes in behavior pattern accompanying repro-
ductive activity develop, and in some animals the whole plan of exist-
ence may be profoundly modified. Typical examples of such changes
in behavior patterns are the long journey of the Pacific salmon from
the ocean to the spawning grounds far inland at the headwaters of
such rivers as the Columbia and Fraser; and the long migratory flights
of many species of birds, such as the journey of the Canada goose to
the Arctic tundra.
These responses are often direct reactions, to changes in environ-
mental conditions. They may have a seasonal aspect and may be asso-
ciated with various physiological and morphological responses in the
organism. Many species of fish, such as the suckers and sturgeon,
spawn early in the springtime; others, such as the whitefish, spawn in
the fall. In birds the mating season usually occurs in spring or early
summer. Among 'maimmals many species have recurring periods of
reproductive activity throughout >the year, e.g., rat, rabbit, monkey,
arid man ;• others, such as the deer, have a single breeding season in
autumn,
J (Underlying the seasonal aspect of reproductive activity are other,
;' more .basic, factors, some of which vary with the season of the year.
"'"'Viit'h'as sometimes been found possible to change certain environmental
conditions experimentally and thus bring about modification in the
reproductive cycle. Light intensity is a ,very important factor in this
respect in many animals—particularly in birds. Rowan and Bisson-
nette have shown that it is possible to accelerate the seasonal develop-
ment of the-gonads of birds by the use of artificial light, thus, in a
sense, prolonging the length of daylight. In this way, Rowan caused
juncoes to mate in the middle of winter. Temperature is another factor
of importance, and. certain species of fish will not spawn until the
temperature of the water is at or very near some particular level.
10
General Plan of Vertebrate Development 11
Various physiological factors also influence the reproductive activity
of animals. At the time of sexual maturity, the animal is usually at
the height of physical vigor but any disturbing factor such as sickness
or physical abnormality may completely destroy its ability to repro-
duce. Dietary deficiencies often injure the germ cells of the animal
and result in reproductive failure. This is true of deficiencies of various
vitamins, e.g., vitamin E, as shown by Evans and Mason in the rat,
and by Adamstone in the chick. Even the lack of an essential amino
acid, such as tryptophan, may have similar results. In many animals
there exists a very complicated interrelationship between various en-
docrine glands and the gonads so that it is often possible to modify
reproductive activity by experimental production of hormone imbal-
ance. It is probable, for example, that the winter mating of juncoes,
mentioned above, is in reality a secondary reaction due to the effect
of light on the pituitary body and indirectly on the gonads.
With the onset of reproductive activity there may be striking
changes in certain morphological structures of the animal, particu-
larly the secondary sexual characteristics. As a rule, it is the male
in which these changes are most pronounced. The development of
brilliant coloration in some fishes, showy plumage in many species of
birds, and the antlers of the deer are typical examples. The develop-
ment of these characteristics may be accompanied by changes in the
behavior of the^nimal. Among birds, for exaiiiple, the prairie chicken
and the bird of paradise stage elaborate mating dances. Among mam-
mals, the rivalry of the males for domination of the herd may be
expressed in violent physical combat, as in the deer 'family, the winner
driving oS his weaker opponents and mating with 'the females of the
band.
GENERAL PLAN OF VERTEBRATE DEVELOPMENT

The general plan of development is essentially the same in all verte-
brate animals. In the different classes of vertebrates, however, there
are many individual departures from this general plan. Hence a more
accurate picture of vertebrate embryology can be obtained from a
study of the details of development of several well-known forms rather
than only one. Of all the vertebrates, the frog, the chick, and man
have been studied most intensively, but the protochordate amphioxus
is almost equally interesting from a comparative point of view. In
order to compare the details of development of these forms it is help-
ful not only to have a general picture of embryonic development but
also to review the life history of each.
12 Reproduction and Life Histories
Before continuing with brief accounts of the life histories of the
vertebrates which will be studied, it is advisable that the student
review the list of terms which will be used in the descriptions to follow.
SOME EXPRESSIONS COMMON IN DESCRIBING EMBRYOS

' (Synonyms in parentheses)
Anterior (cephalic, cranial, rostral)—^head end.
Posterior (caudal)—tail end.
Dorsal—back surface.
Ventral—^belly surface.
Lateral—either right (dextral) side, or left (sinistral) side.
Mesial (median, medial)—middle.
Proximal—nearer the point of reference.
Distal—farther from the point of reference.
Transverse—a plane intersecting the anteroposterior axis at right angles,
"dividing anterior portion from posterior.
Sagittal—^the mesial plane of the body or any plane parallel to it, dividing
right portion from left.
Frontal (coronal)—any plane at right angles to both transverse and mesial
planes dividing dorsal portion from ventral.
Primordium {anlage, Ger.; ebauche, F;'.)—the first recognizable stage in the
development of any new part of the embryo.
Invagination—the growth of a, surface in (toward the point of reference).
Evagination—the growth of a surface out (away from the point of reference).
Vertebrates are characterized in the first place by the bisexual

method of reproduction involving the production of germ cell^ by the
male and female parents. Among the protochordates (tunicates) we
find groups in which the same individual' produces botii eggs and
sperm. Such individuals are called hermaphrodites. This phenomenon
does not. occur widely among the vertebrates and is not typical of many
species. Occasionally, also, a condition of false hermaphroditism
occurs in which an individual of'one sex may_have external genitalia
resembling to some extent those of the other. .
The prodiiction and liberation of germ cells is, therefore, the first
real step in reproduction. These cells, however, cannot develop inde-
pendently but must first unite during the process of fertilization to
produce a fertilized egg cell or zygote. Thereafter the fertilized egg
cell begins to develop almost immediately, and, by a .succession of cell
divisions or cleavages, a large number of daughter cells or blastomeres
are produced. -These become arranged in a typical ^manner so as to
form a -single-layered embryo or blastula. In addition to the produc-
tion of a jarge number of cells the process of cleavage also brings about
a distribution or- segregation of the materials of the fertilized egg cell
among the individual blastomeres. .The formation of the blastula is
Vertebrate Life Histories 13
followed immediately by the development of the gastrula, the process
being known as gastrulation. This is accompanied by the reallocation
of the cells of the blastula so that the materials of the presumptive
germ layers are arranged in their proper definitive positions within the
embryo. Thus the three primary germ layers are separated out. When
the germ layers have once been segregated, further remodeling and
recombination of these tissues result in the development of the various
organs and organ systems of the embryo. At this stage the animal,
though small, is ready to begin its own independent existence
VERTEBRATE LIFE HISTORIES

Amphioxus
The amphioxus [Branchiostoma lanceolatum) is not a vertebrate,
for it, lacks a skull and vertebral column, but because it has a notochord
and other chordate structures it is classified as a relative of the verte-
brates, namely, a protochordate. Some workers believe that the struc-
tures peculiar to the amphioxus are more primitive than those seen in
the vertebrates; others hold that they are degenerate and due to the
mode of life adopted by this curious animal.
SPAWNING. Amphioxus is found in brackish water along the sea-
shore in many localities from Europe to the coast of China. In the
Bay of Naples where its development has been carefully studied its
breeding season occurs in late spring and summer. During the. late
afternoon the males and females emerge from the sands in which they
normally burrow, and swim about in the shallow waters, shedding
sperm and eggs, respectively.
FERTILIZATION. The sperm swim to the eggs, one sperm normally
entering each egg, after which a membrane—the fertilization membrane
—appears (Fig. 1^). ' •
CLEAVAGE. About an hour after fertilization the fertilized egg divides
into two equal parts. This is the first cleavage or 2-cell stage, and each
of the cells is called a i^-blastomere (Fig. IB, C). The second cleav-
age follows in about % hour to bring about,the 4-cell stage with its
^-blastomeres. Later cleavages occur more rapidly, and the cells at
one pole are slightly larger than those at the opposite pole (Fig. ID, E).
BLASTULA. Four to six hours after fertilization the blastomeres have
become arranged in the form ot a hollow sphere called a blastula
(Fig. \F). The enclosed cavity formed by the rounding of the inner
surfaces of the blastomeres and the formation of a jelly between them
is called the blastocoel (Fig. IG).
GASTRULA. Six to seven hours after fertilization the larger blasto-
Fig. 1. Development of the amphioxus. A, Fertilized egg, from posterior side.
B, Beginning first cleavage, from posterior side. C, First cleavage complete, from
vegetal side (note extruded jelly). D, Third cleavage, from right side. ' E, Fifth
cleavage (32-cell stage), from side. F, Blastula (256-cell stage), from right side.
G, Blastula, sagittal section. H, Gastrula, sagittal section. /, Late gastrula,
sagittal section. J, Early embryo of 7 somites, optical section from left side.
K, Embryo of 10 or 11 somites, optical section from left side. L, Embryo of 48
hours, optical section from left aide. All X 166. (Ajter Qonklin, 1932.) M, Larva
with 3 gill slits, from left side, X60. {Ajter Lankaster and Willey.) N, Adult,
from left side, ><2. (After Lankaster.)
15
meres begin to move into the blastocoel just as if that side of the
blastula were collapsing inward. This process is called invagination,
and, when it is complete, the hollow, spherical blastula has been trans-
formed into a two-layered cup, the gastrula (Fig. IH). The newly
formed cavity of the gastrula is the gastrocoel or archenteron, and its
exterior opening is the blastopore (Fig. 17).
T H E GERM LAYERS. The outer layer of the gastrula is known as
the ectoderm; the inner one is frequently called the endoderm. In
reality this last layer includes not only the endoderm proper but also
material of the presumptive middle germ layer or chorda-mesoderm.
This will be separated out about 11 or 12 hours after fertilization.
As the germ layers are segregated further differentiation proceeds
immediately. The ectoderm on the dorsal side forms the primordium
of the neural tube, the endoderm becomes the lining of the primitive
gut, and the chorda-wesoderm forms the notochord and mesodermal
pouches (Fig. 1J,K).
HATCHING. The embryo escapes from its egg envelopes at about
this time, or a little earlier. It is now cylindrical in form, and flattened
on the dorsal surface, its length about twice its diameter. It appears
to be about twice the volume of the original egg, owing to the large
digestive cavity arising from the gastrocoel.
T H E LARVA. After hatching, and until the mouth opens, about the
fourth day after fertilization, the embryo subsists on the remainder of
the yolk originally stored in the egg cell. It is then about 1 mm. in
length, very slender, and probably of no greater volume than the origi-
nal egg (Fig. IL). Xs soon as the mouth opens and the embryo is able
to ingest food from external sources it is called a larva. By now all
the organ systems except those connected with reproduction are func-
tioning. For about 3 months the larva (Fig. IM) leads a free-swim-
ming existence, gradually making its way to deeper waters.
METAMORPHOSIS. At the end of 3 months, approximately, the larva
has increased in length to an average of 3.5 mm. I t now gives up its
free-swimming life to burrow in the sand, and it slowly assumes its
adult characteristics (Fig. LV). The ability to produce mature germ
cells is first manifested when the'animal is about 20 mm. long.
Tlie Frog
The frog (Rana pipiens) is one of the anuran amphibia. It is se-
lected as a representative of the ichthyopsid type of vertebrate, in-
cluding the fish and amphibia, and is classified as an anamniote because
it develops without an amnion. It has long been a favorite object of
embryological observation and experiment, and its development is
better known than that of any other vertebrate except the chick.
Fig. 2. Development of the frog, Rana pipiens. A, Fertilized egg, frorn left side.
B, First cleavage, from posterior side. C, Second cleavage, from left side. D,
Third cleavage, from side. E, Fifth cleavage, from side. F, Early gastrula
(dorsal lipstage), from posterior side. G, Mid-gastrula (lateral lips), posterior
side. H, Late gastrula (yolk-plug stage), posterior side. /, Neurula, dorsal side.
/, Neural folds open, dorsal side. K, Neural folds closed, dorsal side. L, Tail-bud
stage, dorsal side. All X 10. M, Stage of muscular response. A'^, Hatching stage.
O, Opercular-fold stage. P, Tadpole after closing of operculum. {M-P, X7V2.)
{From Shumway, Anat. Rec. 78:139-147, rearranged.)
SPAWNING. The breeding season of the frog is in the early spring,
soon after the ice is off the ponds. The males, emerging first from
hibernation, make their way to the breeding grounds, where they con-
gregate and sing in chorus while awaiting the coming of the females.
When the females arrive, mating occurs, and both individuals discharge
their germ cells in the early morning. The eggs (Fig. 2A) are sur-
rounded with a layer of albumen which swells rapidly, causing the
eggs, in masses of 3500 to 4500 (Wright), to adhere to vegetation or to
rest on the bottom in shallow water. Considerable yolk is present in
the egg, giving one pole a creamy color; the opposite hemisphere is
darkly pigmented.
FERTILIZATION. Fertilization is external, but the close contact of the
individuals during mating insures the entrance of the sperm into the
egg before the swelling of the egg jelly prevents such entrance.
CLEAVAGE. The rate of cleavage depends upon the temperature, but
the first division (Fig. 2B) may occur 1 to 2 hours after fertilization,
earlier at high temperatures, later at low ones. The first two cleavages
divide the egg completely, but the third cleavage is unequal, so that the
four darkly pigmented %-blastomeres of the animal hemisphere are
markedly smaller than the four of the vegetal hemisphere where the
yolk is concentrated (Fig. 2D). After the third cleavage, the pattern
becomes more irregular.
BLASTULA. The blastula is again a hollow sphere, but the presence
of the large yolk-laden blastomeres in the vegetal hemisphere results
in an eccentrically placed blastula cavity. Furthermore, cleavage
planes tangential to the surface of the blastula produce a layer of
blastomeres several cells in thickness.
GASTRULA. The presence of large amounts of yolk causes great
modification in the process of gastrulation. In the end a characteristic
gastrula is formed in which the small pigmented cells have almost
completely overgrown the large yolk-laden cells of the vegetal pole
(Fig. 2H) while segregation of the germ layers is under way.
T H E GERM LAYERS. The cells which are left on the exterior of the
gastrula make up the ectoderm; the inturned cells forming the roof of
the gastrocoel make up the chorda-mesoderm. The yolk-laden cells
which are overgrown in the process become the endoderm.
T H E NEURULAI The neural plate lies over the dorsal side of the
embryo and from it the neural tube will be formed. The frog embryo
at this stage is called a neuru-la (50 hours after fertilization, when kept
at 18°C.). While the neural tube is being formed the embryo increases
in length to about 2.5 mm. This length is attained, ordinarily, 72 hours
after fertilization (Fig. 2K],
HATCHING. The embryo continuesto increase rapidly in length and
in the development of its organ systems. It attains a length of 6 mm.
(Fig. 2N) 140 hours after fertilization at 18°C. and wriggles out of
its jelly. The embryo as yet has no mouth or external gills, but while
these organs are forming it attaches itself to the egg jelly by means
of the oral sucker with which it is provided.
T H E LAEVA. External gills (Fig. 2N, 0) develop on the embryo
soon after hatching (6-7 mm.), but, by the time the mouth has formed,
these gills are covered over by a fold of skin, the operculum. This
remains open on the left side by means of an aperture called the spiracle.
Meantime, clefts have opened between the endoderm of the pharynx
and the ectoderm just back of the head, and in these clefts the internal
gills are formed. By now, the«embryo may be called a larva. It is
11 mm. in length (Fig. 2P), at the age of 284 hours after fertilization
(if it has been kept at 18°C.). The tadpole is about 84 mm. long when
fully developed.
About a month after hatching, the legs develop: first the fore-legs,
concealed by the operculum; later the hind-legs. The lungs are also
developing, and the tadpole frequently comes to the surface of the water
to breathe.
METAMORPHOSIS. About 3 months (90 to 100 days) after the egg is
laid, the larva undergoes a rapid change into the adult condition
(Fig. 2N). If food is scanty, or prolonged cool weather prevails, this
change or rhetamorphosis may be held over until the following spring.
The animals become sexually mature in the second spring following
metamorphosis.
The Chick
' ' The domestic fowl {Gallus doniesticus) develops under conditions
widely removed from the two preceding types, for the egg is laid on
land. This type of development is characteristic of the sauropsids
(reptiles and bii'ds) and of the egg-laying mammals or monotremes.
We have observed that most of the early embryologists worked with
the hen's egg, for it may be procured in abui\dance at all seasons of the
year and is easily incubated. The development of the hen's, egg is
studied in almost every embryological laboratory and is bettej known
than that of any other vertebrate.
FERTILIZATION. The egg is fertilized within the oviduct of the female
after she has copulated with a male.
The egg cell itself is extremely large, at the time of fertilization con-
sisting of an enormous mass of yolk about 40 mm. in diameter on which
rests a tiny disc of protoplasm, the blastodisc. The whole structure is
enclosed by a vitelline membrane (Fig. dA).
Fig. 3. Development of the hen's egg. A, Fertihzed egg, with shell partly broken
away to show interior, X%. B, Second cleavage, shell and albumen removed,
from above, X%. C, Later cleavage stage, germinal disc only, from above, X4.
D, Blastoderm at! 15 hours of incubation, X7. E, Blastoderm at 20 hours of
incubation, X7. F, Blastoderm at 25 hours of incubation, X6. G, Blastoderm at
38 hours of incubation, X5%. H, Blastoderm at 48 hours of incubation, X2%.
I, Blastoderm at 68 hours of incubation, X2%. /, Embryo with yolk sac, amnion,
and allantois at sixth day of incubation, X%. K, Embryo at nineteenth day of
incubation, X%. (All after Duval; K modified.)
19
20 ' Reproduction and Life Histories
CLEAVAGE. This process takes pl^ce as the egg is traversing the ovi-
duct. In the hen's egg, cleavage affects only the blastodisc and the
yolk is entirely undivided (Fig. 3JS, C). Furthermore^ the blastomeres
are not at first separated completely from each other but remain con-
nected below and at the margin of the disc.
BLASTULA. Tangential cleavage planes, at about the 64-cell stage,
cut off the central cells from the undivided protoplasm beneath them,
thus forming a blastocoel. Central and marginal cells together make
up the blastoderm, which expands rapidly as new cells are added at its
periphery. The undivided protoplasm beneath the blastoderm is soon
consumed, and the central portion of the blastoderm lies directly above
the yolk. The original blastocoel is thus enlarged by the addition of
space resulting from the liquefaction of the yolk.
GASTRULA. The blastoderm, grows out over the yolk all around its
peripliery, but in one area cells separated beneath the surface convert
the blastoderm into a two-layered structure which may be called the
gastrula. It is during gastrulation that the eggs are usually laid
(Fig. 3A). After the eggs are laid, the hen broods them for about
3 weeks. This process keeps the eggs at a temperature of about
38°-39°C.
GERM LAYERS. The two layers of the gastrula are usually called the
ectoderm and the endoderm. Strictly speaking, however, the outer
layer is composed of ectoderm and potential mesoderm and is more
properly called mesectoderrn. Early in the first day of incubation an
axial thickening, which is known as the primitive streak (Fig. 3D),
appears ifi the center of the blastoderm. Here it will be svifScient to
note that the notochord grows forward from the anterior end of the
primitive streak, and the mesoderm grows out from its sides and
posterior end (Fig. 3^^) between the ectodermal and endodermal layers.
FORMATION OF THE BODY. The embryo is still a flat disc, so the neural
folds, somites, etc., take their.origin during the first day in a manner
which differs from that of the frog much as a flat map differs from a
globe (Fig. 3F). Later a series of folds marks off the embryo (Fig. 3G,
H, I) while the margin of the blastoderm continues to grow down
around the yolk to form a yolk sac. To this the embryo'is attached by
a yolk stalk. In the wall of the yolk sac there develops an extensive
vascular network which conveys food digested, by the wall of the yolk
sac to the rapidly growing embryo.
AMNION AND ALLANTOIS. Other folds grow up from the blastoderm
to fprm a second sac, the amnion, which encloses the embryo. In this
a fluid is formed so that the chick really develops in a watery medium,
or "private pond," as it has been called (Fig. 3J). In connection with
the development of the amnion a third envelope, the chorion, is formed.
Still another sac-like structure, the allantois, grows out from the body
of the chick to serve as an organ for metabolic exchange and storage
of waste products.
HATCHING. On the twentieth day (Fig. 3K) the chick punctures the
shell, the remains of the yolk sac are drawn back into the body, and
the lungs begins to function. The following day the baby chick breaks
out of the shell, leaving amnion, chorion, and allantois behind. Growth
is rapid, and sexual maturity is attained at the age of 4 or 5 months in
the male, and 4 to 10 months in the female.
Man
The development of man {Homo sapiens) has been the subject of
much study and speculation since long before the time of Aristotle,
particularly among students of medicine. But although a great deal
is known concerning the later stages of development, the earliest stages
remain obscure, and our account must be supplemented with observa-
tions on other placental mammals.
FERTILIZATION. Fertilization is internal and probably takes place in
the upper part of the oviduct (Fig. iA).
CLEAVAGE. The human egg has not been observed in any of the early
cleavage stages until quite recently (Hertig-Rock, 1948, 1949), biit in
the monkey (Fig. 45, C, D) it is known thait cleavage is complete and
the first blastomeres are approximately equal in size. There is so little
yolk in the egg that the blastomeres round up and slip about on each
other, giving rise to a solid mass of blastomeres called a morula.
BLASTULA. The human blastula has also never been observed, and
there is some difficulty about homologizing the early embryos of man
and other mammals with such forms as the frog and the chick. Some
authorities consider the morula a solid blastula. Others, and these are
in the majority, believe that the blastula stage of other vertebrates is
represented in man by a stage known as the blastocyst. This is derived
from the morula by the formation of a cavity, filled with a liquid, which
gradually separates an outer layer of cells, the trophoblast, from an
inner mass of cells, the embryonic knob (Fig. 4B).
GASTRULA. The embryonic knob consists of an upper group of cells
attached to the itrophoblast, which is usually called ectoderm, and a
lower layer of cêlls which separates from the upper layer (Fig. 4 f ) .
The lower layer organizes itself into a very small hollow '5rolk sac,
which is considered to be.endoderm (Fig. 4G).
IMPLANTATION. The embryo reaches the uterus after about 3 % days
in the oviduct and about the tenth day implants itself in the uterine
wall, which has been prepared to receive it. The age of the youngest
human embryo so far recorded (Hertig-Rock 8020) is estimated at
Fig. 4. Development of man. A, Mature egg, unfertilized, from uterine tube,

section, X250 {after Allen). B, C, D, Cleavage in the monkey egg,-first, second,
and third cleavages, X112 {after Lewis and Hartman, in Arey). E, Section of
monkey egg before implantation, X250 {after Streeter). F, Section of human
ovum, after implantation, X150 (after Hertig). G, Section of human embryo,
15 days old, XlOO {after Brewer). H, Primitive groove stage, X20 {Heuser).
I, Three somites and neural folds, X18 {Ingalls). J, Seven somites, X15 {Payne).
K, Ten somites, X15 {Corner). (I-K, Redrawn from Streeter.) L, Diagram of
uterus and embryo at about 1 month, X ^ {after Arey). M, Embryo of 11 mm.
(about 6 weeks) with its membranes, chorion opened, X1 {after Arey). N, Fetus,
near term, {dingrnmrnntic, after Ahlfeld).
7 days after conception. A 12-day embryo (Hertig-Rock 7700) is
illustrated in Fig. 4^.
GERM LAYERS. The upper portion of the embryonic knob has mean-
while developed a cavity, the amniotic cavity, and so forms a hollow
vesiciV rrr cvrrritiiiyit with the Ao/ibw yofk sac. Thus, where the two
vesicles are in contact, there is formed a circular disc called the embry-
onic shield. The upper layer, continuous with the wall of the amnion,
consists of ectoderm and chorda-mesoderm; the lower layer, continuous
with the wall of the yolk sac, is endoderm. A primitive streak is formed
much as in the chick and appears to be related in a similar manner to
the segregation of the mesoderm (Fig. 4H).
FORMATION OF THE ^QDY. The body is elevated above the embryonic
disc by the formation of head and tail folds and the lateral sulci.
Neural folds make their appearance (Fig. 47) and unite to form a
neural tube (Fig. 4J, fC). Somites are formed from the mesoderm next
to the notochord (Fig, 4/^ K) .(J
EMBRYONIC MEMBRANES AND PLACENTA. AS the embryo grows, its
membranes, the amnion and chorion, as well as the overlying uterine
tissue increase in size until they fill the entire cavity of the uterus, which
enlarges to accommodate the developing embryo. A small yolk sac and
rudimentary allantois are also developed. In the meantime, the embryo
establishes a placental connection with the uterus (Fig. 4L, M). I t is
this area which is supplied by the allantois or'umbilical blood vessels.
Here the maternal and embryonic blood streams are brought close
together and substances diffuse from one to the other. This is the
region where oxygen and carbon dioxide are interchanged, and here the
embryo receives its food, predigested by the mother.
FETUS. By the ei^d of the second month the embryo has quite
definitely taken on the characteristics of the human species and is
known thereafter as the fetus. From this time on, its developmental
history is mainly, one of growth while further development proceeds
(Fig. 4:N). At the tenth lunar month (280 days) the intrauterine devel-
opment is completed and the fetus is delivered from the body of the
mother by the process of parturition or birth.
EXTRAUTERINE DEVELOPMENT. Like all mammals, the human infant
is still dependent upon the mother for nourishment after birth and is
then fed by milk produced by her mammary glands. In the human
species, moreover, pa^-ental care is carried to the greatest extremes.
Development continues long after birth, e.g., the replacement of the
teeth and the "knitting" of the bones. Sexual maturity (puberty) is
not attained until the age of 12-15 years in females, and 13-16 years in
males. Growth continues into the third decade.
The Germ Cells—Their Structure,
Origin, and Development
The germ with which development commences in the vertebrate is the
fertilized egg or zygote. This is produced by the union of the male
germ cell or sperm with the female germ cell or ovum at the time of
fertilization. The two kinds of gametes or germ cells are highly
specialized cells and differ from each other in appearance, size, and
structure. These differences will be mor,e apparent after a review of
cell structure in general.
Structure of the Cell

A. Nucleus (composed of karyoplasm).
1. Reticulum (composed of chromatin).
2. Karyolymph (nuclear sap).
3. Nucleolus (plasmasome).
4. Nuclear membrane.
B. Cytosome (composed of cytoplasm).
1. Hyaloplasm (ground protoplasm).
2. Centrosomes (centrioles).
3.. Mitochondria (chondriosomes).
4. Golgi bodies (diotyosomes). . >
5. Plastids {not found in animal cells).
6.'Metaplasm (relatively lifeless accumulations). j
7. Plasma membrane.
C. Envelopes or matrix (cell wall).
THE CELL ^
The familiar definition of a cell (Fig. 5) is "a mass of protoplasm,
containing a nucleus, both of which have arisen by the division of the
corresponding elements of a preexisting cell." Protoplasm in this sense
refers to the living substance of the cell, including'the material both
inside the nucleus and in the cell body or cytosome. It is customary
to use the term karyoplasm (nucleoplasm) for the nuclear protoplasm
and the word cytoplasm for the protoplasm of the cell body. Some
24
The Cell 25
writers employ only the words nucleus and cytoplasm to distinguish
Ijetween nucleus and cell body.
The Nucleus
The cell nucleus is generally a rounded body separated from the
cytosome by a delicate nuclear membrane. Within this is a transparent
ground substance known as the karyolymph or nuclear sap. But the
characteristic substance of the nucleus is its chromatin, a material stain-
Golgi 1)0(1168
Plastid
Centrosomes
Mitochondria Nucleolus
Nuclear
membrane
Chromatin knot
Vacuoles
Plasma
membrane
Cell wall
Metaplasia
Fig. 5. Diagram of a composite cell {ajter Wilson).
ing sharply with basic dyes, and, in fixed material, arranged usually in
a network of threads called the reticulum (Sharp). Sometimes swell-
ings, or chromonleres, are apparent at the nodes of the network. The
nucleus usually contains a smaller body known as the nucleolus, which
differs chemically from the rest of the nucleus and stains with acid
dyes. It undergoes characteristic changes during cell division, dis-
appearing as thei chromosomes become prominent and reappearing after
division is complfete.
Most cells have a single nucleus, although the red blood cells of
mammals extrude their nuclei during development, becoming enucleate
cells. In some cases the nucleus may divide so that a multinucleate
cell is formed, e.g., the osteoclasts of developing bone. In other cases,
26 T h e Germ Cells
it may divide many times while the cell body remains undivided, thus
producing a syncytium. In still other cases, the nucleus may fragment
and be distributed throughout the cytoplasm in the form of small
granules called chromidia. The form of the nucleus also varies con-
siderably. In most cells it is somewhat bladder-like and hence is de-
scribed as vesicular, in contrast to the compact type found in the head
of the sperm. It may be lobulafed or polymorphous in some instances,
as in the granular white blood cells..
The nucleus is extremely important in the cell in controlling its gen-
eral metabolic activities. It is also the bearer of the chromatin mate-
rial from which the chromosomes are elaborated during cell division.
The Cytosome
The cytoplasm of the cell body includes an outer delicate semi-
permeable membrane known as the plasma membrane. This is the
surface at which the protoplasm of.the cell is in contact with its environ-
ment and thus is of very great importance in controlling the entrance
and exit ol cellular metabolites. Contained within the cell membrane
is the liquid ground substance or hyaloplasin in which are distributed a
number of differentiated bodies or cell organelles. The more important
of these cytoplasmic inclusions are the centrosomes, the mitochondria,
and the Golgi bodies—each of which appears to have a special role in
. the functional activities of the cell.
T H E CENTROSOMES (CENTRIOLES) . These are small spherical bodies,
one or two in number', situated near the nucleus. They are most prom-
inent and active during the process of cell division. In cells with loco-
motor organs like the tail of the, sperm, the centrosomes are connected
with the contractile element of the locomotor organ.
T H E MITOCHONDRIA (CHONDRIOSOMES) . These are ^numerous small
bodies, filamentous, rod-like, or granular in, shape, and scattered ihrough-
the cytoplasm. They are dissolved by many common reagents used in
preparing cells for microscopic study, but can be demonstrated in the
living cell by the stain Janus green B, which is considered to be specific
for these structures. They are preserved by special chemi'cals, e.g.,
osmium tetroxide, after which they may be stained by special jnethods.
These structures are apparently of very great importance in the cell
although as yet their exact function is not understood. Nevertheless,'
since about 1925, a great body of evidence has been accumulated which
indicates that they are related to the elaboration or activity of enzymes
concerned with such functions as cellular oxidatioii and reduction and
the handling of cellular metabolites such as fats and carbohydrates.
T H E GOLGI BODIES (DICTYOSOMES) . These are found scattered
T h e Germ Cells 27
through the cytoplasm of the cell in the form of rods or granules and are
often aggregated into the form of a network, the so-called Golgi appa-
ratus. Much confusion surrounds this cell organelle because of the great
difficulty in demonstrating it. Ordinarily, it is revealed by the use of
such classical methods as the silver impregnation method of Golgi or by
the use of osmic acid. These methods are often capricious and unrelia-
ble and, hence, some investigators deny the existence of the Golgi bodies
as a physical entity. There is little doubt, however, that the dicty-
osomes found in developing sperm cells are true cell organelles. Some
authors speak of the Golgi material or the Golgi zone of the cell,
whereas others have sought to identify the Golgi bodies with other
cytoplasmic elements such as the mitochondria or the plastids of plant
cells. There is still some uncertainty whether or not they can be
demonstrated in the living cell. Their function is also doubtful, but
some investigators have ascribed to them a secretory role in the elabora-
tion of various cell products such as mucous and zymogen granules.
METAPLASM. This is the name given to all those bodies in the cyto-
plasm which generally do not possess the properties of independent
growth and division. They may be distributed as tiny droplets,
granules, etc., or they may be aggregated in the form of vacuoles.
Among these are such bodies as secretory granules, which represent
intermediate stages in the production of cell secretions, e.g., zymogen
granules. Storage granules, representing the end stages in the accumu-
lation of such reserve food materials as yolk, oil, and starch, may also
be present. Pigment granules are also to be included among these
bodies. Embryologists sometimes use the term deutoplasm for reserve
food materials stored in the cell.
The Cell Membrane

In general, anirnal cells do not produce a definite cell wall but instead
form a very delicate semipermeable membrane such as the vitelline
membrane of the egg cell. In some tissues, the individual cells produce
a common matrix in which they are embedded, such as the intercellular
substance of cartilage or bone.
THE GERM CELLS

'' The Sjperm
The male germ cell of vertebrates is a very minute flagellate cell
ranging in size from 0.020 mm. (crocodile) to more than 2 mm. in
Discoglossus, an amphibian. The general shape is that of a tadpole
with an excessively long tail, but there are sufficient differences among
28 T h e Germ Cells
these tiny cells that sperm cells from different species of animals may
be readily identifidci by specialists.'
The sperm (spermatozoon) consists of a head and a tail (Fig. 6).
Some sperm, e.g., human, have a short neck between the head and tail.
The head contains the nucleus, which is compact and stains very
deeply with basic dyes. Here also is the acrosome, usually at the apical
end, originating from the Golgi bodies of the spermatid, and possibly
Acrosome
Head vacuole
Nucleus
Postnuclear cap
Neck bodies
Proximal centrosome
Mitochondria
Distal centrosome •
Axial filament
Plasma membrane
Fig. 6. Diagram of a human sperm (after Gatenby).
concerned with the production of some secretion involved in fertiliza-

tion. The head is surrounded by a delicate plasma membrane.
The tail consists of three divisions: middle piece, main piece, and end
piece. The middle piece contains two centrosomes; the'one nearer the
head is called the proximal centrosome, the one farther from the head,
the distal centrosome. These bodies are so minute that some difference
of opinion has been expressed as to their number and position in the
various types of sperm. They have also been confused with other "small
bodies such as the "neck bodies" of the human sperm. The axial fila-
ment arises in the middle piece of the sperm apparently from the
proximal centrosome and passes through the ring-shaped distal centro-
some. This structure is the contractile filament which gives the sperm
its power of locomotion. Around the axial filament in the middle piece
T h e Germ «€ells 29
re granules of mitochondrial origin. Surrounding all these structures
•« a delicate plasma membrane. The main piece, as the name implies,
• j.jjg longest part of the tail and consists of the axial filament and
nlasma membrane. The end piece is the terminal region in which the
naked axial filament projects beyond the limits of its sheath. Abnor-
mal sperm occur in some individuals. There may be giant or dwarf
sperm; some may have double heads or tails or other abnormality.
Later we shall see that there are always (except in birds and some fish)
two classes of sperm, which are, respectively, male-producing and
female-producing. These are not visibly different as a rule.
LONGEVITY OF SPERMATOZOA. There is considerable variation in the
length of life of the sperm cell. In the fowl, it has been demonstrated
by removing all males of the flock after copulation that the sperm retain
their fertilizing power in the oviduct of the hen for about 2 weeks on the
average and with a maximum recorded life of a month.
In some animals, such as the bat, sperm may remain alive in the
genital tract of the female for prolonged periods. It has been claimed
that sperm received by the female during copulation in the fall may be
still alive and capable of fertilization the following spring. It has been
suggested, however, that the ova are fertilized immediately and that
this phenomenon really represents delayed implantation of the ova
fertilized in the fall. In man, it is probable that the life of a sperm in
the oviduct does not exceed a week, and Hartman has shown that in
the monkey {Macaccvs) the sperm survived but a few days.
DURATION OF FERTILIZING POWER. Although the sperm may remain
alive for a considerable period, they apparently lose their fertilizing
power rather quickly. I t has been shown in the hen that eggs fertilized
by sperm received at a'single copulation may begin to develop but after
about 2 weeks become markedly less hatchable with the increasing age
of the sperm.
ACTIVITY OF SPERMATOZOA. The spermatozoa, when set free in the
tubules of the testis, are non-motile. They are, however, gradually
transported down the seminiferous tubules and eventually reach the
epididymis. Her;:e they acquire slight motility and at the time of liber-
ation take on their greatest activity. In the lower vertebrates, the
sperm are mixed, with mucoid cellular debris, the mixture forming the
milt liberated by,the male. In the mammals, the sperm are mixed with
the secretions of the prostate gland and seminal vesicles, thus forming
the seminal iiuid. I t has been shown that the secretions of these glands
are rich in fructose, which may possibly be a nutrient material for the
sperm cells. The seminal fluid is a gelatinous, sticky substance which
becomes more liquid in the vagina of the female. When the sperm
30 T h e Germ Cells
have been transported to the upper reaches of the female genital tract,
they are thought to swim actively against the current produced by the
downward-stroking cilia. The rate of progress of human sperm swim-
ming in an aqueous medium is about 2.5 mm. per minute.
NUMBER OF SPERM LIBERATED. There is great variation in the number
of sperm cells liberated among vertebrate animals. In fish, the sperm,
are set free in a watery medium and the numbers produced may reach
almost astronomical figures. Thus, in the codfish, where half a million
eggs are produced, there may literally be billions of spermatozoa. In
man, about 2 to 3 cc. of seminal fluid are liberated at a single emission
and this contains probably between 200 and 300 million sperm cells.
LIMITATIONS ON VIABILITY OF SPERM. Spermatozoa are subject to
many harmful environmental conditions. I t is well known that nutri-
tional factors affecting the male animal may seriously weaken the sperm
cells. Thus various vitamin deficiencies such as vitamin E deficiency
may completely destroy the fertilizing power of the sperm long before
any abnormality can be demonstrated in them. Other factors, such as
extremes of heat and cold, may be injurious to the developing germ cells.
In mammals, the scrotal temperature is considerably below that of the
body of-the animal, and, if the testes are retained in the body, whether
through abnormal conditions or as a result of experimental interference,
the sperm will degenerate and lose their fertilizing power. Sperm are
also particularly sensitive to the pH of the medium in which they are
liberated. They can withstand a considerable degree of alkalinity, but
a slightly acid condition is fatal, In the mammal, the acidity of the
vagina of the female is a common caHise of sterility.
Sperm of the Amphioxus

The sperm of the amphioxus (Fig. 7A) is the smallest recorded among
chordate animals. Its total length varies from 0.016 to 0.021 mm.
(Sabotta). The spherical head is not more than 0.001 mm. ip length,
the size of a yolk granule. There is a^ minute, bead-like acrosonie.
What appears to be a rounded middle piece pressed against the head
is followed by a very slender main piece. The end piece is not dis-
tinguishable. The length of life of the sperm has not been recorded.
Sperm of the Frog

The sperm of Rana pipiens (Fig. 7B) averages about 0.03 mm. in
length after fixation. The head is long and cylindrical, surmounted by
a bead-like acrosome. The tail originates in a short middle piece, and
has a long main piece indistinguishable from the end piece. The length
of life for sperm of this species has not been reported.
T h e Germ Cells 31
Fig. 7. Typical sperm. A, Amphioxus (after Ballowitz). B, Frog. C, Fowl.

D, D', Man. All X 4000,
Sperm of the Fowl

The sperm of the domestic fowl (Fig. 7C) averages approximately
0.05 mm. in length after fixation. The head is long and cylindrical and
is surmounted by a sharp, recurved acrosome. Adamstone has de-
scribed the presence of lipoidal, bead-like structures in the head of the
sperm, which he considers to be in the nature of reserve food supply.
The middle piece is long and merges into the main piece, which is rela-
tively stout and terminates in a short end piece.
(.
Human Sperm
The human sperm (Figs. 6, ID, ID') has been studied by many
investigators including Gatenby and Aykroyd (1940): I t averages
0.055 mm. in length. The acrosome fits over the nucleus like a cap and
is flatten&d to a shovel shape at the anterior end. The nucleus is oval
32 The Germ Cells
and contains a small vacuole. 4 t its posterior end it is covered by a
postnuclear cap, which joins the acrosome to surround the nucleus com-
pletely. The short, constricted neck contains 2 or more neck bodies.
The middle piece is well developed, with a centrosome at either end,
and contains mitochondrial granules. A long main piece and short end
piece are present. -"
/
The Egg
The female germ cell or ovum is quite similar to a generalized cell in
many ways. Prior to its maturation, the egg contains a large vesicular
nucleus, and the cytoplasm is relatively abundant owing to the great
amount of metaplasm present.
Centrosomes are present in
the immature egg, but disap-
pear during maturation. Mi-
Membrane
tochondria and Golgi bodies
have also been identified.
Nucleui
The color of the egg is caused
Nucleolus by the presence of pigment
in, the cytoplasm. In general,
the female germ cell (Fig. 8)
is extremely large, is protected
by envelopes of various kinds,
contains reserve food materi-
al, and is without power of
Fig. 8. Egg of the cat (after Dahlgren and locomotion. The size range
Kepner).
in vertebfates lies between
0.06 mm. (mouse) and 85 mm. (ostrich). The latter figure is the
diameter of the egg cell without shell or albumen, that'is, what we
ordinarily cd\l the "yolk" of the egg. The albumen and shell are really
egg envelopes, and these added to the yolk make the egg very large.
Even larger eggs existed in past geologic ages, e.g., in an extinct species
of bird (Aepyornis). The fossil egg shells of this speeies ajre 13 X 9
/inches and have a capacity of approximately a gallon. The shape of
V / tlê egg varies from spherical to oval.*^
>y / YojLK. frhe yolk forms the bulk of the egg and contains the principal
food materials stored for the developing embryo"\ The yolk of the hen'sy
egg has been carefully analyzed and is found to contain water (50 pejf
cent), proteins, fats, carbohydrates, inorganic salts, vitamins, enzym^,
and pigments (Needham).
The yolk or metaplasm is present in the form of spheres, ovoids, or
discs, which usually stain with basic dyes. The yolk tends to accumu-
late in one hemisphere of the egg, forcing the nucleus and much of the
T h e Germ Cells 33
fjx^wplasm into the other. Since th^ôlk is heavier than the other con-
stituents of the egg, the yolk-j]^Sn hemisphere is the lower one when
the egg is suspended in water. \Qn large-yolked (macrolecithal, mega-
lecithal) eggs, such as those of tne irog and cKicI
the volkm one region is so marked lEatl-.hev are kno-yyp as telolecithal
-gggs] liTimaJl-yoked (mjcrolechhal, oligolecithal) eggs, like those of
the amghioxus and ol man, the yolk is distributed more uniformly:
hence they are classed as isolecithal or honioiecithalft^
pOLABiTY. Eyen in isolecithal eggs, there is aîstmction, which is
sometimes visible, between the two hemispheres of the egg. This is
much more prominent, however, in a telolecithal egg such as the frog's
egg with its darkly pigmented cytoplasm concentrated in the upper
portion or animal hemisphere. The apex of the animal hemisphere is
known as the animal pole or apical pole. The yolky material is con-
centrated in the lower portion or vegetal hemisphere, the apex of which
is the vegetal or abapical pole. The Jine running between these two
poles constitutes the polar axis. This is the axis of symmetry of the
egg around which it is organized. The nucleus always lies in the polar
axis, more or less toward the animal pole. The yolk shows a gradation
from the animal toward the vegetal pole. We shall observe in later
chapters that the animal pole often marks the anterior end of the
developing embryo, and in these cases the vegetal pole marks the
posterior end. There is also reason to believe'that the polar axis, in
addition to being the first expression ofsvmmetrv in the egg, marks a
gradient of metabolism (Child). This means that metabolic processes
are higKesiTat the animal pole and progressively diminish toward the
vegetal pole.
A considerable body of evidence shows that the animal pole of the egg
is the one which is most active in physiological exchange with its en-
vironment while the egg is still in the ovary. I-t is the pole of the egg
\^hich is attached to the ovary in the amphioxus and the chick
(Conklin) and is most richly supplied with blood vessels.
EGG ENVEEOPE^., .The egg usually possesses, in addition to the plasma
membrane, 'd--. variety of protective envelopes which are divided into
three classes according to the mode of their formation. Primary
envelopes -are those formed by the egg itself, such as the delicate
vitelline membrajie.A The secondary envelopes are those formed by
the follicle cells wîch immediately surround the egg in the ovary.
A good exan^ple is the so-called chorion of one of the cyclostomes,
Myxine (Fi^. 9).* It is usually quite difficult to distinguish primary
from secondary envelopes, and it is probable that many vitelline
membranes are compound in origin. In those vertebrates in which
fertilization is external, such as the cyclostomes and bony fish, the
34 T h e Germ Cells
primary and secondary envelopes' are often perforated by openings
called micropyles, through which the sperm may have access to the
egg. The tertiary envelopes include all those formed by the walls
of the oviduct during the passage of the egg. Examples are the egg
albumen, shell membranes, and shells' of such groups as the reptiles,
birds, and the egg-laying mammals/the egg capsules of the elasmo-
branchs; and the egg jelly of the amphibia and many bony fish.
These envelopes are not formed until after fertilization, except in the
Anchor
filaments
"Chorion'
Fig. 9. Egg of Myxine, showing "chorion" and mioropyle {after Dean)
case of the egg jelly, which does not attain its final thickness until after
t]ie entrance of the sperm, when it swells by the absorption of water.
GGS AND THEIR ENVIRONMENT. Needham has pointed'out that e^gs
iffer from one another in respect to the physicochemical constitution
of the unfertilized egg and the possibility of obtaining necessary mate-
ri^l-feom the environment. The marine egg, exemplified by that of
mphioxys, develops in a medium containing oxygen andinorgaiiic salts.
le egg is organized in such a manner as to, facilitate the exchange of
materials with the environment. The yolk is small in amount and (to
judge from analyses made on marine fish eggs) relatively poor in fats
and inorganic salts. Development is rapid up to the hatching stage,
but thereafter the larva takes a long time to attain its full size and to '
reach sexual maturity. , ^ ^.^
The egg whkh__jde:Kaloi)s_in_iresh_w.ater, like that of the n-og, does
© have a mediunl^so rich in salts as the marine e g ^ It is there-
fore originally equipped with a larger store of thisniaterial- But the
T h e Germ Cells 35
oueous mekium still affords facilities for the exchange of carbon
Hioxide and/oxygen and for the disposal.jaf_ nitrogenous wastes. The
ielly with which the frog's egg is provided consists almost entirely
nf protein /and water. Diffusion takes place through it readily, and
it affords protection against mechanical injury and bacterial infection,
and may also furnish a source of nourishment immediately after hatch-
ing There is, however, some question as to its nutritive value.
The terrestrial (cleidoic2_egg^_such as the hen's, stands easily first in
respect to the amount of yolk present. The ratio of fat to protein in
the yolk is also the highest. I t is obvious that the egg must contain
all the material necessary for growth except free oxygen and water, for
these are the only substances passing from the atmosphere through the
protective envelopes of the egg. Hence, except in the earliest stages, the
chick develops more rapidly than the amphioxus and attains its adult
form in a much shorter time. The egg albumen, also a source of food,
is a watery solution of protein with some carbohydrates. As we shall
see in later chapters, the relative isolation of the embryo in the cleidoic
egg is correlated with the development of its extraembryonic mem-
branes,, i.e., the amnion, or water bath, and the allantois which serves
primarily to store nitrogenous wastes.
(The eggs of the mammals, which typically develop in the uterus, are
characterized by little yolk, for, from a very early period, their nourish-
ment is derived exclusively from the body of thfe motheji Accordingly
there is a precocious separation of a special layer, the trophoblast, con-
cerned with implantation, and later the development of a special organ
of interchange, the placenta. - • , ^ o/. - \
The Egg of the Ampkioxus (^

The eggs (Fig. 104) are 0.1 mm. in diameter. Before maturation the
large nucleus is roughly 0.05 mm. in diameter and displaced well toward
the animal poler'xhe cytoplasm consists of a thin outer layer relatively
free from yolk and probably containing mitochondria. The rest of the
cytoplasm contains yollTTairly uniformly distributed./• The egg is,
therefore, classed as isolecithal. There are no egg envelopes except a
vitelline membrane. ^ ^
The Egg of the ^rog C rOoJ)e'ê.tdU^ t ^ hL<L^^HA^)

The diameter of the egg (Fig. 105) is 1.7 mm. (R. pipiens, Wright),
and contains a large'nucleus before maturation. There is a thin outer
layer of cytoplasm, containing granules of pigment in the animal hemi-
sphere. Pigment is also found around the nucleus. The yolk is most
highly concentrated and forms large platelets in the vegetal hemisphere
36 T h e Germ Cells
grading into finer and smaller, platelets in the animal hemisphere.
These eggs are classed as moderately telolecithal.
n Polar body
Vitelline
(fertilization) Egg jelly
membrane
n Polar body Eg-gjeUy
Vitelline
membrane
Corona radiata
(follicle cells)
I Polat body
Nucleus
Vitelline
membrane
Zona pellucida
Fig. 10. Typical eggs. A, Amphio.xus, approx. X70 (after Wilson, in Willey).
% F r o g , - X 8 . C, Hen, X % {ajter Duval). D, Human, X250 (after Allen, in
Arey). *
The Egg of the Chick (_ f e Z « / C^^^^J

The hen's egg (Fig. IOC) is extremely telolecithal. The cytoplasm,
with the nucleus in its center, forms a small germinal disc upon the
great mass of yolk. This yolk is arranged in concentric layers of yellow
Germinal disc
Vitelline — Shell
membrane
Outer shell-membrane
White yolk
Inner shell-membrane
Air cell
Chalaza Dense White
Inner thin white
Concentric
layers of white Outer thin white
and yellow yolk
Fig. 11. Diagram of sectioned hen's egg {after Adamstone).
and white material around a central mass of white yolk, called the
latebra (Fig. 11). From this latebra a stalk of white yolk (the neck
of the latebra) extends upward and spreads outward as the isthmus of
Pander. The germinal disc rests on this isthmus. The yolk and
T h e Germ Cells 37
terminal disc are surrounded by a delicate vitelline membrane
(primary). This in turn is surrounded by the albumen, a viscous terti-
ary membrane twisted spirally from left to right, starting from the
broad end of the egg. There are several layers of albumen of different
densities. The denser albumen next to the vitelline membrane is pro-
longed into 2 spirally twisted cords, the chalazae, one at either end of
the yolk. The albumen is in turn surrounded by 2 parchment-like
shell mernbranes, of which the inner one is the thinner. These two are
separated at the blunt end of the egg, thus forming the air chamber.
The egg shell is a calcareous deposit upon the outer shell membrane.
Its color is due to bile pigments of the hen. It is porous, a fact that can
bd easily demonstrated by injecting glycerine into the egg by means of
a hypodermic needle. The germinal disc is about 4 mm. in diameter,
the yolk about 40 mm. The size of the egg as a whole varies widely,
depending on the amount of albumen deposited around the yolk, sj
pellucida
Nucleus
Sperm
to same
scale
Fig. 12. Human egg (ovarian), X200 {.a\tex TFaZde^yer),
Giant and dwarf eggs are sometimes recorded. In the hen's egg,
double- and triple-yolked eggs are known, as well as those which have
no yolk at all. A very strange abnormality is known as the "ovum in
ovo," where one egg is formed around another. The eggs of birds are
either male-producing or female-producing, a statement based prima-
rily on evidence ,from genetics but confirmed by direct cytological
observations by Suzuki and others.
The Human Egg

Like those of other placental mammals, the human egg (Figs. lOZ),
12) is very small, its diameter being about 0.13 mm. No yolk is demon-
strable in the egg (Gatenby and Aykroyd, 1940). There is a delicate
38 T h e Germ Cells
vitelline membrane surrounded by. a thick zona pellucida, which is a
clear homogeneous layer and is probably a secondary envelope. When
the egg is first discharged from the follicle, the zona pellucida is still
surrounded by a layer of follicle cells which make up the corona
radiata. The corona soon disintegrates or is stripped off the egg. / T h e
work of Hartman indicates that the life of the egg, or at least the
period in which it can be fertilized, is probably not more than 24 hours
in man since it does not exceed 3 days in the monkey.
Comparison of the Egg and the Sperm

Both gametes are morphologically complete cells. Each has a nucleus
and a cytosome containing representatives of the centrosomes, mito-
chondria, and Golgi bodies. Each has a plasma membrane. Yet neither
is capable of independent, continued existence, for physiologically they
are unbalanced. The egg is large, inert, contains a vast store of, meta-
plasm, is protected by egg envelopes, and has lost the power of continued
division. The sperm is small, highly motile, contains little cytoplasm
and no metaplasm, is devoid of protective membranes, and in itself has
lost the power of continued division. We shall now turn to the study
of the development of the germ cells and see how the structural dif-
ferences, at least, arise.
COMPARISON OF THE VERTEBRATE EGG AND SPEEM
Cell structures Ovum Sperm

Cytoplasm ' Large amount ' Small amount
Centrosomes One, disappears in matura- Two, retained in rnatura-
tion tion
Mitochondria Diffuse In middle piece
Golgi bodies Diffuse AcroSome,
Plasma mem- Present Present
brane
Nucleus Vesicular Compact
Nucleolus Present Indistinguishable
Nuclear mem- Present' Present '
brane
Other differences
Size Large Small
Movement Quiescent Swims actively
Motile organs None Flagellum
Protection Egg envelopes None
Shape Spheroid Tadpole
Numbers pro- Few to many Vesy many
duced
The Germ Cells 39
Zygote
PHmordial <
Germ Cells
/\/\A/\/\/\/\A l\/\/\/\/\/\/\i\
Gonia <
\
/I /\
• • • •
•1-
(/ • $
Auxocytes •<
4-
t
Meiosis -^
ft
;
Gametes
Zygote \ «>/
Fig.'13. Diagram of gametogenesis: male on left, female on right {after Wilson).

40 T h e Germ Cells
Tlie Origin of the Germ Cells
After the discovery of Mendel's laws it .was soon realized that the
germ cells constitute the only hereditary bridge from one generation to
the next. Consequently the question arose whether or not an animal
could transmit to its offspring characteristics acquired during its life-
time. The question became the basis of an extensive controversy, and
distinguished biologists ranged themselves on opposite sides of the argu-
ment. Among these, the great German zoologist August Weismann is
responsible for a theory known as the Theory of the Continuity of the
Germplasm, which holds that the germ cells are set apart completely
from all the other cells of the body (soma cells) at a very early stage
in development (Fig. 13) and hence are not subject to the environ-
mental influences which affect the body cells. There is other evidence
in support of this theory in the embryology of a few invertebrate
animals such as Ascaris, a parasitic roundworm. In the very first
cleavage of the fertilized egg of this form, the 2 daughter cells show a.
striking difference, for when one of the daughter cells divides it retains
all the chromatin of its nucleus, whereas the other gives up a portion of
this material to the cytosome. This phenomenon has been called
chromatin diminution, and the cell showing this characteristic becomes
a soma cell, that is, jt contributes to the development of the soma or
body of the animal. The other is known as a stem cell (Fig. 14), and in
its division it produces one cell which will be a soma cell and one which
will be another stem cell. Eventually the stem cell gives rise to 2 ideiiti-
cal cells, both of which are known as primordial germ cells. From this
time on, they and their descendants produce germ cells only.
• This theory of the distinction between germ' cells and soma cells, has
held an important place in the.history of biology because it seemed to
deny the possibility of the inheritance of characteristics' acquired after
fertilization. In other words, such characteristics would be,acquired
• by the soma cells, whereas, according to the theory of Weismann, in-
heritance is a function at the germ cells, which are entirely isolated
from external influences. .This argument has been weakened by .evi-
dence that the nuclei of all cells are identical, at least in early cleavage,
an4 thff belief of many investigators that in the mammals, at least, the
primordial germ cells degenerate without leaving descendants, and that
the functional germ cells arise from epithelial cells of the gonads. -!,
PKIMORDIAL GERM CELLS. In vertebrates, primordial germ cells are'
recognizable in a good niany forms, e.g., in the elasmobranch fish where
they accumulate among the endodermal cells of the wall of the mid-gut.
These cells are distinguishable by their large size, clear cytoplasm, and
heavily staining nucleus (Fig. 15). From the gut waiU, they migrate
The Germ Cells 41
S,(AB)
Fig. 14. Origin of stem cells in Ascaris. A, First cleavage. B, C, and D, Second
cleavage. Pi and P 2 a r e stem cells. Si (which gives rise to A and B) and
S2 are soma cells. (From Richards, after Boveri.)
into the dorsal mesentery suspending the gut from the roof of the
coelom and thence laterally to the ventral side of the mesonephros just
beneath the wall o| the coelom. Here they multiply rapidly and pro-
duce 2 longitudinal ridges, which are the primordia of the sex glands or
the gonads.
Primordial germ cells have also been recognized in the endoderm of
the chick just anterior to the head fold (Swift). Bounoure (1939)
claims to have identified stem cells in cleavage stages of the frog (Fig.
42 T h e Germ Cells
16), using silver-impregnation techniques. More recently, Witschi
(1948) also recognized primordial germ cells in the developing gonads
of human embryos.
Mesonephric duct
. 1
Pig. 15. Primordial germ cells in the frog (Rana sylvatica). Part of transverse
section through 10-mm. larva, showing coelomic roof, X375. (After Witschi.)
T H E GONIA. There^ are two opinions concerning the fate of the

primordial germ cells in vertebrates: one that they give rise to all the
later generations of germ cells'; the other that they degenerate, serving
Primordial >
determinants gejm cells C
Fig. 16. Germ cell determinants and primordial germ cells in the frog. A,
Fertilized egg. B, Four-cell stage. C, Blastula. (After Bourioure, 1939.)
only to organize the overlying peritoneal epithelium to form the defini-

tive gonad in which the germ cells develop.
In any case, the developing germ cells whicli continue to multiply
actively in the gonads are known as gonia: spermatogonia if they are
to give rise to sperm, oogonia if they give rise t,o eggs.
The Germ Cells 43
Gametogenesis v /
When the individual becomes sexually mature^ production of mature
germ cells begins. The gonia first undergo a ptJriod of rapid growth,
after which they are known as aux-
ocytes or meiocytes (Fig. 17). In
the male they are called spermato-
cytes and in the female oocytes.
^The process by which the auxocytes
become mature germ cells is known Idiogome Golgi bodies
as gametogenesis: spermatogenesis in Centrosomes
the male, "and oogenesis in the fe-
male. By this process each auxocyte Fig. 17. iJiagram of an early
gives rise to 4 daughter cells as auxocyte. {After Wilson^
a result of two cell divisions '*^-
called the maturation divisions. These divisions are unique since
certain special nuclear phenomena are involved. These are discussed
in detail below.
STAGES IN GAMETOGENESIS
Spermatogenesis General Oogenesis

Stem Cells
Primordial Germ Cells
Period of Migration and Multiplication
Spermatogonia Gonia Oogonia
Period of Growth
Spermatocytes Auxocytes Oocytes
Period of Maturation
I Spermatocyte I Oocyte
II Speratocyte II Oocyte + I Polar Body
Spermatids Mature Ovum + II Polar
Body
Period of Metamorphosis
Sperm
Spermatogenesis
The processes involved in maturation of the male germ cells include
two special cell divisions known as the maturation divisions. During
the first of these each primary spermatocyte produces 2 secondary
spermatocytes. In the second maturation division each of the second-
ary spermatocytes produces 2 spermatids which undergo transformation
into spermatozoa.
CYTOLOGICAL CHANGES INVOLVED DURING SPERMATOGENESIS. The
male primary spermatocyte is a large cell containing a large vesicular
44 T h e Germ Cells
nucleus, more or less eccentric. In^tlie human spermatocyte (Fig. 18^1),
according to Gatenby and Beams, the Golgi bodies plus the centrosomal
material form a complex body, the idipsome, lying next to the nucleus.
This Golgi-idiosome complex consists of an inner, lightly staining,
chromophobic mass, surrounded by an outer, chromophilic or heavily
staining layer. Within the chromophobic mass are the 2 centrosomes,
and a number of proacrosomic granules, each in a tiny vacuole.
Throughout the cytoplasm are numerous granular mitochondria.
Centrosome
Fig. 18. .Transformation of the spermatid into the mature sperm. A, Sperma-
tocyte. B, C, D, E, Spermatids. F, Immature sperm. G, Mature sperm,
(After Gatenby and Beams, 1935.)
At the end of the two maturation divisions the mifochondria and

Golgi bodies are diffused (Fig. .185). Soon the proacrosomic,material
of the spermatid is condensed to form a proacrosomic bead in a vacuole
surrounded by a chromophilic sheath (Fig. 18C), and the centrosdrq.es
move to the opposite side of the cell in proximity to the plasma mem-
brane. Here they give rise, apparently together, to the axial filament
which penetrates the plasma membrane of the spermatid. Thereafter
they separate, and the distal centrosome forms a ring around- the axial
filament. A little later they move towards the nucleus, which now
shows the beginning of the postnuclear cap (Fig. 18D) on the side*
opposite the Golgi-idiosome complex. The mitochondria are most
numerous in the centrosomal side of the spermatid.
In a later stage in the transformation of the spermatid (called spermi-
ogenesis or spermioteleosis), the nucleus condenses (Fig. 18.EJ) and the.
T h e Germ Cells 45
rosomal bead spreads over its anterior surface to form the acrosome.
The remainder of the Golgi complex drifts down the side of the nucleus
, foj-m the Golgi remnant. Meantime the postnuclear cap is enlarg-
ing the distal or ring centrosome has enlarged, the axial filament is
ereatly lengthened, and the cell has become an elongate body with the
nucleus at the proximal end.
The immature sperm, as we may now call it, attaches itself to a
Sertoli or nurse cell at the proximal end, while all the cytoplasm
gathers at the distal end (Fig. ISF). The distal or ring-shaped cen-
trosome slips down the axial filament to mark the posterior end of the
future middle piece. Around the axial filament, between the two
centrosomes, there is an aggregation of mitochondria.
Finally the cytoplasmic mass, including the Golgi^ remnant and
numerous mitochondria, is sloughed off to leave the mature sperm
(Fig. 18G).
Polarii)odiea
Egg
nucleusi
Sperm
nucleus
Fig. 19. Maturation divisions in egg of guinea pig. A, First maturation division.
B, Fertilization. C, Second maturation division. (After Lams.)
Oogenesis
The female auxocyte or primary oocyte is very much lilie the primary
spermatocyte. But the period of growth prior to the maturation divi-
sions is prolonged while large amounts of yolk are formed. The
nature of the maturation divisions (Fig. 19) is also different, for the
first" division, instead of giving rise to 2 secondary oocytes of equal
size, produces 1 vej-y large cell and 1 excessively minute cell called a
I polar body. In the second division the large secondary oocyte again
divides into 1 large, cell and 1 very small cell, the II polar body. At the
same time the small I polar body may or may^not divide into 2 equal
cells or II polar bodies. In this way 4 ootids are produced (or 3, if the
the small I polar body fails to divide), of which the single large cell is
46 T h e Germ Cells
the mature ovum and the smaller, cells are polar bodies. These latter
are incapable of fertilization and degenerate.' As they are formed at the
animal pole of the egg, the polar bodies are often of practical value in
orienting the egg.
We shall defer to a later section an account of the details of nuclear
activity during the maturation divisions, remarking here only that one
of the principal results is that the chromatin is sorted out so as to pro-
duce unlike nuclei. The centrosomes are often difficult to find in the
primary oocyte and have not been found in the ovum. The idiosome
and the mass of mitochondria are often associated in a yolk-nucleus
complex. During the maturation divisions a large amount of nuclear
material is cast out into the cytoplasm.
Unlike the male gametes, whose maturation is completed within the
testis, the oocytes do not complete their maturation until after leaving
the-ovary, and, in vertebrates at least, the second division is not com-
pleted until after the entrance of the sperm. The significance of this
situation is not understood although it has been suggested that it is a
device to insure that the egg shall be freshly matured at the time of the
union of the pronuclei.
4
Fertilization
The union of the two germ cells, egg and sperm, to form a fertilized
egg or zygote is known as fertilization. Prior to tiie actual union of
the gametes two preliminary processes occur: ovulation, or discharge
of the egg from the ovary; and ejaculation, the enîssion of the sperma-
tozoa.
OVULATrON
Within the ovary of the vertebrate the developing egg cell and its
surrounding nurse cells make up a follicle (Fig. 20). Here the egg cell
enlarges and may undergo its
first maturation division. Pe- Wall of ovary
riodically, mature eggs are dis-
charged from the ovary. This
occurs once a year in most Follicle cells
Oocyte
vertebrates but once a month in
Oogonium
the human species and daily
in the domestic fowl. The
number of ova discharged at
a single ovulation varies from
one, as in man or the fowl,
to thousands in the frog and
even millions in many' fish.
The Causes' of ovulation are
not entirely understood, but ^^- ^^ Transverse section through part
of frog ovary, X95.
the factors involvqd are prob-
ably quite diverse, varying with the species under consideration, The
available eyidence points to the following possibilities:
1. MUSCULAR CpNTEACTioN. The ovaries of many vertebrate species,
e.g., the frog and rat, contain delicate bands of involuntary muscle
fibers associated with the ripening follicles. Contraction of these muscle
fibers may aitk in the rupture of the follicle and the liberation of
the egg.
47
48 Fertilization
2. ENZYME ACTION. The secretion of an. enzyme which digests and
thereby weakens the outer wall of the follicle is another possible factor
to be considered.
3. TURGOR. In mammals a follicular fluid is secreted in the cavity, of
the follicle surrounding the egg. This causes a great increase in inter-
nal pressure or turgor as well as a stretching and thinning of the follicle
wall which finally ruptures, thereby liberating the egg.
A similar situation is found in the developing follicles of the ovary
of the bird, where the accumulation of large quantities of yolk produces
increased turgor. In this case, however, it is possible to inject even
more fluid into the egg by way of the follicular stalk without causing
rupture of the follicle. •
4. RUPTURE OF THE STIGMA. In some vertebrates, notably the birds,
there appears on the surface of the follicle a somewhat whitish linear
area devoid of blood vessels along which rupture of the folliclg occurs.
This area is called the stigma, and a possible weakening of the follicle
wall in this area may occur at ovulation. - '•
5.. HORMONE ACTION.' In many vertebrates ovulation can be induced
at certain times by the injection of a hormone secreted by the anterior
lobe of the pituitary gland. Rugh (1935) has demonstrated that in the
frog this hormone produces contraction of muscle fibers in the ovary,
which, in combination with the digestive action of an enzyme, weakens
the follicle wall, causing ovulation. ' "^
A somewhat similar situation exists in certain mammals such as the
rabbit, cat, and ferret, in which ovulation is related to copulation. In
the rabbit it has been shown that, if the pituitary body is removed from
the female immediately following copulation, ovulation does not occur.
However, if an interval of 20 minutes is allowed to elapse beôre^re-
moval of the pituitary, then ovulation occurs in the normal manner.
Apparently, in this brief interval, enough of the pituitary hormone is
liberated iiito the blood stream to bring about ovulation.
OviPosiTiON. When released from the ovary the eggs are caught up
in the open end of the oviduct, down which they pass to the exterior.
In many aquatic forms they are discharged directly into the water.
In others they accumulate for a time in an' enlarged j^rtion of the
oviduct known as the uterus, awaiting discharge from the body; such
animals are described as oviparous (amphioxus, frog, chick). In still
others the egg remains in the uterus until development has reached an *
advanced stage; these are the viviparous animals including the
mammals. i\
Many zoologists use the term ovoviviparous for such vertebrates' as
certain snakes, in which the egg remains for some time in the uterus
Ovulation 49
^vhile the young develop within the egg envelopes. The young snakes
hatch from the eggs while still inside the body of the mother, and are
discharged later.
EJACULATION. This term is applied to the discharge of the sperm.
These cells remain in the testis (Fig. 21) until mature, often attached
to the Sertoli cells. When discharged they pass through the tubules
of the testis into the sperm duct. They become motile upon reaching
the medium in which fertilization takes place. Enormous numbers,
often many millions, are produced at a single discharge. In the lower
vertebrates the sperm and liquid material in which they are suspended
Sperm
Tubule
Interstitial Spermatogonia
cells
Spermatocytes
Fig. 21. Section tlirougb-part of frog testis, X200.
ioxm a milky fluid called milt. In the mammals, the sperm are mixed
with the secretions of the seminal vesicles and the prostate gland, form-
ing a viscid, gelatinous material called seminal fluid.
In aquatic animals such as the amphioxus and fish the two sexes con-
gregate together at the breeding season, the males and females often
swimming close together in pairs, so that the eggs and sperm are dis-
charged in proximity. Some aquatic animals such as the sharks have
copulatory organs which introduce the sperm into the oviduct, thus
bringing about internal fertilization. In alPterrestrial vertebrates
fertilization is internal and is regulated to some extent by copulation.
This is accomplished by the mere apposition of the cloaca of two
individuals in -some species, but in other forms the male is provided
with an intromittent organ for transfer of the seminal fluid to the
reproductive .tract of the female.
In this case, however, another problem presents itself, namely, the
cause of'the rapid ascent of the sperm up the female reproductive tract.
50 Fertilization
It seems highly improbable that the spermatozoa actually swim the
whole distance. On the contrary, there is considerable evidence to
show that the seminal fluid introduced into the cloaca of the bird or
into the vagina of the mammal reaches the upper portion of the ovi_duct
in a matter of minutes. Contractions in the female reproductive ducts
stimulated by copulation may be the explanation of this phenomenon.
FERTILIZATION
The actual fertilization of the egg has been observed in the amphi-
oxus and the frog, but our detailed knowledge of the process is obtained
from study of such marine invertebrates as the sea urchin. The essen-
tial feature of fertilization is the entrance of a single sperm into the
Q Copulation path
Fig. 22. Diagram to show fertilization of the egg. A, Fertilization cdne: B,

Penetration path. C, Female copulation path, and rotation of sperm head.
D^Male copulation path. E, Cleavage path. F, First cleavage.
egg and the coming together of the nuclei of the germ^ cells (Fig. 22).
This phenomenon is preceded by other events concerned with bringing
the sperm to the egg.
a. ATTRACTION. When sperm cells come into the vicinity of the egg
they usually congregate around it. This constitutes the process of
attraction, and,"as a result of studies on invertebrate, eggs, severai
factors are believed to be involved as follows:
Chemotaxis is the movement of the sperm toward the egg attracted
to it by the liberation of some chemical substance from the egg or
female sex organs. In echinoderm eggs, when sperm are introduced
Fertilization ' 51
'nto sea water in a watch glass in the approximate area from which egg
cells have just been removed, the sperm will swim toward the spot
recently occupied by the egg.
Thigmotaxis. Sperm swim in a spiral path, and, when they approach
a small solid body, even a grain of sand, they may move directly toward
it The same action may be operative in attraction, and if the spiral
brings a sperm obliquely toward the egg the contact flattens out the
qpiral, causing the sperm to remain in contact without penetration.
But, if the sperm arrives at the egg in a radial direction, penetration
is facilitated.
Enzyme Action. Lillie has shown that the sea urchin egg emits an
enzyme, fertilizin, which brings about agglutination, i.e., a temporary
and reversible adhesion of the sperm heads in clusters. Fertilizin is
produced only after the egg is mature and before it is fertilized. ^
b. PENETRATION.* The sperm penetrates through the egg en^lopes
but then apparently comes to rest against the plasma membrane. In the
eggs of some invertebrates such as certain echinoderms there has been
observed at the surface of the egg a cone or even a long filament of
cytc^lasm with which the sperm head.comes in contact. When this
occurs the cone or filament then retracts, drawing the sperm into the
egg and engulfing it (Fig. 22A, B)T''Thereafter, commencing at the
point where the sperm head makes contact or is engulfedîe vitelline
membrane is transformed into the fertilization rhembrane: I t has been
demonstrated by the use of special methods that a sudden change
sweeps over the vitelline membrane accompanied by a change in opti-
cal properties. ^'The fertilization membrane has been considered to be a
bar to the entrance of extra sperm cellsT Apparently after the fertiliza-
tion membrane is formed the egg decreases in diameter owing to the
secretion of some fluid which thus separates or elevates the fertilization
membrane. Okkelberg describes a loss of 14 per cent in the volume of
the egg of the brook lamprey. The formation of this membrane with
its perivitelline fluid underneath marks the successful fertilization of
the egg. In the frog the fertilized egg can rotate freely within this
membrane. i
In the mammal 'an obstacle to the contact of egg and sperm is the
presence of the corona radiata in association with the liberated ovum.
It has been suggested that the accumulation of spermatozoa in prox-
imity to the egg may result in the liberation of an enzyme (possibly
hyaluronidase, which is produced abundantly in testicular tissue), and
this may cause the coronal cells to fall away from the egg so that the
sperm cells can reach it.
c. CONJUGATION OF THE PRONUCLEI. In the vertebrates the egg
52 Fertilization
undergoes the second maturation division and gives off tlie second polar
body after the entrance of the sperm. The nucleus of the ovum, which
is now large and vesicular, is called the female pronucleus. It is situ-
ated near the animal pole. The sperm nucleus by contrast is still.near
the periphery of the egg at the point of penetration but it loses its com-
pact form and becomes the large vesicular male pronucleus. The sperm
now rotates 180°, so that as it moves toward the center of the egg its
centrosome and middle piece go first, followed by the male pronucleus'
(Fig. 22C). Finally the two pronuclei come together (Fig. 22D, -E) by
a route which may be analyzed into the following components: (1) the
sperm penetration path, which is usually the radius of the egg at which
the sperm entered; (2) the sperm copulation path, which is directed
toward the point at which the pronuclei will meet and is often at a
considerable angle to the penetration path; (3) the egg copulation path,
along which the female pronucleus moves towards the meeting point;
and (4) the cleavage path (Fig. 22E), along which the two pronuclei
move to their final position on the egg axis, often slightly nearer the
animal poleT The two pronuclei may unite at this time to form a
common cleavage nucleus. This union of the pronuclei is known as
conjugation. On the other hand, the two pronuclei may merely remain
close together and contribute independently to the first nuclear division
of the zygote (Fig. 22F). See also Chapter 9.
The centrosome of the egg disappears after the second maturation
division. The centrosome of the zygote, therefore, is either the centro-
some of tiie sperm or, possibly in some cases, a new one developed in the
egg cytoplasm near the engulfed sperm head.*/ . ^
Thet mitochondrial material oJ the sperm fragments and is distributed
tfiroughout tiie cytoplasm of the zygote. The later history oj the
aerosome has not been followed. • ^' -
There is much divergence among different kinds of animals with
respect to those parts of the sperm which are actually ehgulfed.in the
egg. In some, it is the entire sperni; in others, only the sperm head.
Fertilization of the Amphioxus Egg

In 'the amphioxus, fertilization is external. The males and females
leave their burrows in the sand to swarm in the shallow waters during
late afternoons of spring and sumnler. Eggs and sperm are discharged,
from the segmental gonads in which they develop, into the cavity of
the atrium, and escape to the exterior through the atriopore. The first
polar body is given off before fertilization. Immediately after the
entrance' of the sperm the fertilization membrane* expands greatly,
leaving the egg in a large perivitelline space ( F i ^ . 24, 10^4). The II
Fertilization 53
nlar body which is given off after the formation of the fertilization
membrane remains attached to the egg; the first is usually lost.
Fertilization of the Frog's Egg

Fertilization of the frog's egg is external, but the sperm are brought
into proximity with the eggs during the sexual embrace or amplexus
which occurs during mating. At this time the male clasps the body of
the female from the dorsal side with his fore-legs, so that the cloacas
of the two individuals are close together while the germ cells are being
extruded. Hence, fertilization, though external, is assured. The sperm
make their way through the layers of egg jelly before these envelopes
have attained_their final thickness. The first sperm coming into con-
tact with the vitelline membrane enters the egg, usually within 40° of
the animal pole. The vitelline membrane is elevated to become the
fertilization membrane, leaving a perivitelline space within which the
egg may rotate. The second maturation division then occurs, followed
by the conjugation of the pronuclei. The penetration and sperm copu-
lation paths are marked by a trail of pigment dragged in with the
sperin head. The tail of the sperm is left outside or near the surface
of the egg cell.
Fertilizgjion of the Hen's Egg

In the fowl, fertilization is internal. The sperm, introduced into the
cloaca of the female during copulation, make their way to the upper end
of the oviduct, where they may remain for 2 weeks or more. As each
egg, i.e., the yolk with its germinal disc of protoplasm surrounded by a
vitelline membrane, escapes from its ovarian follicle and enters the
oviduct, 5 or 6 sperm enter the germinal disc, where they remain in-
active until after the second maturation division. One of them then
moves inward" until it comes in contact with the female pronucleus,
which has -itself rtioved downward from the surface of the germinal
disc. The supernumerary sperm move outward to the border of the
disc, where, after a few divisions, they degenerate. The fertilized egg
moves slowly down' the oviduct while the tertiary envelopes are forming
about it.
r
Fertilization of tê Human Egg

In man fertilization is internal and probably occurs near the upper
end of the Fallopian tube. Sperm received by the female at coitus
rapidly ascend the oviduct, and it is probable that a single sperm enters
an egg cell which has just recently been released from the ovary after
the first maturation division, as in the guinea pig (Fig. 19B). Further
54 ' Fertilization
details are lacking since no direct observations have been made, but
it is probable that the ovum must be fertilized within 24 hours and
before degenerative changes set in. Clinical evidence presented by
Hertig and Rock (1944) indicates that ovulation probably occurs very
close to the fourteenth day before*the onset of the next menstruation,
although there appears to be some variation in this regard.
Parthenogenesis
* Under normal circumstances the egg of the vertebrate does not begin
to develop until after fertilization has occurred and the diploid number
of chromosomes has been restored. Among some organisms, however,
such as the honey bee and the plant aphids, development of the unfer-
tilized egg may occur naturally. In the bee the unfertilized egg devel-
ops into a male (drone) and the fertilized egg becomes a female
(either a queen or a worker) according to the type of food* supplied.
Moreover, artificial parthenogenesis has been induced in the eggs of
many other invertebrate animals by various means. Among' verte-
brates, fish, amphibia, and mammals have been the objects of successful
experiments. In the frog's egg artificial parthenogenesis has been pro-
duced by slightly puncturing the egg with a finely pointed glass needle.
Most of the parthenogenetic eggs do not go far in development, but
Loeb was able to raise a few adult frogs (15 males, 3 females, 2 doubt-
ful) out of many thousands of eggs treated. ^
The fact that artificial parthenogenesis can be induced in niany
animals raises the important question: What are the effects of the union
of sperna and egg that accompany the beginning of embryonic devf^l-
opment?
Effects of Fertilization on the Egg Cell . *

When development" gets under way it has been found that a number
of important reactions occur in the newly fertilized egg cell:
a. INCREASE IN METABOLIC ACTIVITY. This reaction is indicated by
a very great increase in oxygen uptake, often many times' that of the
unfertilized egg. This is, of course, accompanied by a corresponding
increase in carbon dioxide output and a slight increase in temperature.
It seems probable that the increase in rate of chemical processes'is a
result of setting in motion various reactions controlled by enzyme
activity in the cell.
b. INCREASE IN VISCOSITY. The cytoplasm of the egg cell shows a
I'cmarkable increase in viscosity immediately after fertilization, often
accompanied by a loss of water from the egg.
c. INCREASE IN PEBME.ABILITY. The egg membranes also undergo a
Cytoplasm of the Fertilized Egg Cell 55
striking increase in permeability, thus allowing easier penetration of
various substances into the egg and easier metabolic exchange.
ORGANIZATION OF THE CYTOPLASM OF THE FERTILIZED EGG CELL

Organ-Forming Areas
In many different kinds of eggs, students of cellular embryology have
been able to recognize different regions by differences in the cytoplasm,
such as the presence or absence of pigment, mitochondria, and yolk,
and to trace the distribution of these materials into the different
(5) Ground
protoplasm
Presumptive
brain
•> Presumptive
©Grey {• neural
crescent J plate
Presumptive
notochord
B
&) Grey yolk
Fig. 23. Organ-forming areas in tunicate eggs. A, Fertilized egg of Styela, from
left side (after Conklin). B, Unfertilized egg of Ascidiella, from right side (after
Vandebroek, in Dalcq). Approx. X250.
daughter cells as cleavage takes place. These organ-forming areas, as

they may be called, are'usually more easily demonstrated after fertiliza-
tion. For example, before fertilization the living egg of the tunicate
Styela (Fig. 23^1), according to Conklin (1905), has yellow pigment
granules uniformly distributed in its outer layer of cytoplasm. During
fertilization, following an intricate series of streaming movements, the
yellow pigment is concentrated in a crescentic area at what will later
be the posterior surface. On the opposite side of the egg, marking the
anterior surface, i^ a gray crescent. Below these crescents the vegetal
hemisphere is marked by the presence of yolk granules. In later
cleavage, the yellow crescent will be distributed to the cells which form
the mesoderm of the, tail, the gray crescent to the cells which form the
notochord and the neural plate, the yolk to the cells of the endoderm;._
and +liV^niainderô|ê,%g goes f ' S ^ f c e i r ^ i e ^ g i ^ e r r n i s ^ ^ l ^ ' f '
56 Fertilization
results have been confirmed and extended by Vandebroek (19317)
through the use of vital stains appHed to the unfertilized egg (Fig. 23B).
Similarly, in the egg of the echinoderm, the use of the dark-field
microscope has shown that the area surrounding the vegetal pole
appears different in color from that of the animal pole. Experiments
have shown that these areas give rise to endoderm and ectoderm re-
spectively. Ectodermalization or endodermalization can be augmented
by removing parts of the egg from the appropriate regions or by the
use of certain chemicals. Hence in the normal egg there is a certain
balance between the potential materials present. This can be dis-
turbed by appropriate means. Although the factors located in these
areas are as yet unknown, the word "field" is applied to the organiza-
tion comprising these organizing factors. The area possessing such a
field is referred to as a "field district."
ir Polar body
Anterior
Ventral
Pronuclei
Vitelline
membrane
Posterior
Dorsal
Presumptive Presumptive
endodenn mesoderm
%
Fig. 24. Organ forming areas in egg of the amphioxus, 1 hour after fertilization.
Sagittal section, approx. X230. (After Conklin, 1932.)
Organ-Fprming Areas of the Amphioxus Egg

The fertilized egg of the amphioxus (Conklin, 1932) show§ in sections
(Fig. 24) a crescent of more deeply staining protoplasm on the side of
the egg that will give rise to the posterior part of the body. This cres-
cent will form the cells of the mesoderm (compare the yellow crescent
of Styela). Opposite this is a less clearly defined crescentic area from
which the cells of the notochord and neural plate will be, formed (com-
pare the gray crescent of Styela and of the frog). The .'material of tlte
vegetal hemisphere, bounded above by these crescents, will form the
endoderm; the material of the animal hemisphere above the crescents
will form the epidermis.
Cytoplasm of the Fertilized Egg Cell 57
Organ-Forming Areas of the Frog's Egg
Immediately upon fertilization thie cortical cytoplasm of the egg
rushes toward the point of sperm penetration, carrying with it the black
nielanin pigment of the animal hemisphere. Upon the side of the egg
opposite the point of penetration there appears a crescent-shaped area
Vitelline
membrane Polar bodies
, „ ^ I, /^^^Msgâ \ : ^Pigmented
Jelly "T^^^ I /^^^^^âi I hemisphere
Gray
crescent
Sperm
Unpigmented
hemisphere
Fig. 25. Diagram of frog's egg aftenk fertilization to' show gray crescent. The
line immediately external to the vitelline membrane and polar bodies represents
the "chorion." XIO.
in which the pigment is less dense and which is therefore known as the
•gray crescent (Fig. 25). This area gives rise later to the notochord and
mesoderm, or chorda-mesoderm, and is especially significant in the later
organization of the ernbryo (Chapter 8). It is sufficient at this point
to indicate that the appearance of the gray crescent gives the egg a
bilateral symmetry.
Artificial Fertilization
Artificial fertilization, whereby the male and female germ cells are
purposely brought together, is a process of considerable economic
importance. I t has found successful use in fish culture work, and in
recent years (1952) special methods have been devised for use with
cattle. Seminal fluid of valuable bulls, mixed with glycerine, may be
slpwly frozen to temperatures of —79°C and, when carefully thawed,
even months later, may be used successfully for artificial insemination,
thus helping to maintain and disseminate valuable herd character-
istics.
5
The Mechanism of Heredity

The germ cells are really cells detached from the bodies of the parents.
When they unite in fertilization they bring together material tram, both
parents. Herein lies the explanation of the inheritance of'parental
characteristics, of the fact that the fertilized egg develops in a way
characteristic of the species, and of the fact that individuals differ from
one another. According to modern theory the individual' units of
heredity are the genes which are borne on the chromosomes. The
chromosomes are distributed precisely to the germ cells during matura-
tion, brought together in the zygote during fertilization, and passed on
from cell to cell during cleavage. A brief review of the,mechanism of
ordinary mitotic cell (Jivision and of the peculiar features of the meiotic
or maturation divisions is necessary at this time as well as a consider-
ation of the role of the genes.
Toward the close of the 19th century and in the early years ,of tha
20th a series of parallel and more or less independent discoveries were
•made, which, fitted together, provide a working explanation of the role
. of the chromosomes in the mechanism of heredity. About,1866^Gre'g&r
"^'Mendel had studied and formulated the basic principles underlying the
orderly transmission of hereditary characters but with-'no reference to
chromosomes. Previously a number of investigators including Von
Mohl and Schultze had worked out the details of mitotic cell division.
Chromosomes were recognized by Van Beneden (1883) and/nansed by
Waldeyer in the same year. Moreover, the intricate process of chromo-
some manipulation during the maturation divisions of the germ cells
had already been studied and described. In 1891 sHenking observed
that during spermatogenesis in certain insects two classes of sperma-
tozoa were formed on the basis of the numerical distribution of the
I chromosomes during maturation. In the female, by contrast, all mature
ova received the same number of chromosomes. At the outset, however,
no particular significance was attached to these observations.
Paralleling these discoveries were certain important theoretical devel-
opments. Sutton in 1900 realized that during maturation of the germ
58
T h e Chromosomes in Mitosis 59
cells the chromosomes behave in a manner exactly paralleling what
^vould be expected if they were the actual bearers of the determiners for
hereditary characteristics as postulated by Mendel. Moreover, in 1905
McClung pointed out the real significance of Henking's discovery,
namely, that it offered a simple explanation of the transmission of sex
as a hereditary characteristic.
It was soon apparent that the number of hereditary characteristics in
most species of animals far exceeds the number of chromosomes. This
led Johannsen (1911) to propose a much smaller hereditary unit, the
gene, which is borne on the individual chromosomes.
From the embryological standpoint this implies that some mechanism
must be provided whereby the hereditary determiners may be passed
on to the daughter cells during cleavage so that at the proper moment
in development the necessary genes may be present in the cells in a
given area to control the unfolding of a particular character.
THE CHROMOSOMES IN MITOSIS

The division of most cells is accompanied by the formation and
longitudinal division of threads of chromatin, called chromosomes, in
the nucleus. This type of cell division is known as mitosis (Fig. 26).
Some cells, however, divide without the appearance of chromosomes
(amitosis), and the daughter cells are thereafter incapable of mitotic
division. The term karyokinesis is used for the division of the nucleus
in mitosis and cytokinesis for the division of the cytosome.
4lC3ryokinesis
Before cell division the metabolic or resting nucleus contains a
reticulum of chromatin lying in the fluid karyolymph along with a
nucleolus, the whole surrounded with a'nuclear membrane (Fig. 26^1).
In mitosis four stages may be distinguished: prophase, metaphase, ana-
phase, and telophase.
In the prophase the reticulum separates into its constituent threads,
chromonemata, by ithe breaking down of the smaller threads connecting
th-em. Very early ;it can be seen that these threads are double or split
longitudinally (Fig. 2&B). Soon thereafter a matrix is visible about
the two chromonepiat^. This compound structure, consisting of the
two chromonemata and the surrounding matrix, is a chromosome
(Fjg. 26C). The number of chromosomes so formed is the same in
every cell of every individual belonging to any particular species.
(This statement is subject to exceptions. See pages 68ff.) Toward
the end of the prophase the chromonemata are usually invisible.
eo T h e Mechanism of Heredity
Finally, the nuclear membrane disappears, and the karyolymph assumes
the form of a double cone or spindle (Fig. 2GD).
In the metaphase (Fig. 26E), the chromosomes line up in an equa-
torial plane through the spindle. Each has a definite region of attach-
Fig, 26. Diagrams of somatic mitosis. A, Metabolic ("resting") stage. B,--Early

prophase showing chromonemata and attachment points. C, IVJiddle, prophase,
matrix appearing on chromonemata. D, Late prophase^ cliromonemata obscured
by matrix. E, Metaphase. F, Anaphase. ' G; Early telophase, matrix' disappear-
ing. H, Middle telophase, nuclear membrane forming. /, Late telophase, reticu-
lum developing.' (Based on a diagram by S/ioVp.)
ment to the spindle known as the centromere, which lies in the

equatorial plane even though the ends of the chromosomes may lie
outside this plane. . . -
In the anaphase (Fig. 2&F) each chromosome separates longitudinally
into 2 daughter chromosomes, each containing one of the original
The Chromosomes in Mitosis 61
chromonemata with surrounding matrix. Preceded always by its at-
tachment region, each daughter chromosome moves towards a pole of
the spindle. Carothers (1934) describes the growth of a fiber from the
attachment region of each daughter chromosome to the nearest pole
of the spindle. Eventually two equivalent sets of chromosomes are
formed, one in the vicinity of each pole, both sets containing a daughter
chromosome derived from each of the original chromosomes formed in
the prophase.
In the telophase (Fig. 26G, H, I), each set of chromosomes reverts
back to the metabolic condition. The matrix loses its staining capac-
ity, and the chromonemata reappear, often already split longitudinally
in preparation for the next division. The nuclear membrane is formed
about each group, the chromonemata are united by tiny cross-strands,
the nucleolus reappears, and the nucleus is seen to be filled with
karyolympii. The cell now contains 2 daughter nuclei, each identical
with the other and with the parent nucleus. The division of the cyto-
plasm called cytokinesis usually follows immediately.
Cytokinesis
Other striking events take place in the cytosome during mitosis.
During the prophase the centrosome, if not already divided, separates
into 2 daughter centrosomes, which move apart. About each of them
is a spherical mass of protoplasm, often containing radial striations,
known as the aster. Between them there appears a central spindle
apparently containing fibers. Cytologists distinguish'three types of
fibers: (1) primary or continuous fibers extending.from centrosome to
centrosome, (2) half spindle components extending from chromosome to
centrosome, and (3) interzonal connections extending between the
separating daughter chromosomes (Schrader). The centrosomes reach
the opposite sides of the nucleus just as the nuclear membrane dis-
appears. The karyolymph material between the two centrosomes
• apparently participates in the formation of the mitotic spindle along
which the chromos6n:ies move during the anaphase. In the telophase,
asters and spindle disappear, the nuclear membrane reappears, and the
• centrosomes alone remain in the positions they occupied at the poles of
the mitotic spindle. Sometimes they divide in anticipation of the next
mitosis. I, i»
The mitochondria usually-divide en masse (Fig. 2'IA). This division
of the mitochondrial is approximately an equal one, and some investiga-
tors believe that the individual mitochondria divide during mitosis or
just prior to it, but they often form a ring around the periphery of the
cell during division.
62 T h e Mechanism of Heredity
The Golgi bodies, even when aggregated into a Golgi apparatus,
separate during mitosis and are segregated into the daughter cells,
usually associating themselves with the two centrosomes (Fig. 27B).
It is uncertain whether each Golgi body divides individually at mitosis,
but some evidence has been brought forward to support this contentipn.
In animal cells the cytosome as a whole divides by constriction.
In this process the cell elongates in the direction of the spindle during
the anaphase and telophase. Following the reconstruction of the
Fig. 27. The mitochondria and Golgi bodies in mitosis. A, Mitochondria.

B, Golgi bodies. (After Bowen.) ^
daughter nuclei in the telophase, a furrow appears at the periphery of

the cell, around the equatorial belt, and at right angles tb the axis of
elongation. This furrow advances towards the center of "the celi unfil
the cell is completely divided. ' '
DISTRIBUTION OF THE CHROMOSOMES. Each daughter cell has approx-
imately half the cytoplasm proper, half the mitochondria and Golgi
bodies, a centrosome derived from that of the parent cell, ^nd a nucleus
built up from a set of chromosomes, each of which was produced by the
division of the chromosome in the parent cell. It is apparent" from the
foregoing account that the key to the complexities of mitosis is the
division of the chromosomes. The achromatic figure is the .framework
upon which this division takes place. The division of the mitochondria
and Golgi bodies is still too little understood. But the chromosomes,
appearing in the prophase, halved with such accuracy in metaphase and
anaphase, and disappearing again in the telophase, are characterized
by a constancy in number, an individuality evinced' in form and be-.
T h e Chromosomes m Meiosis 63
havior, and a persistence from generation to generation. In some
favorable- material it has even been possible to demonstrate that the
chromonemata arise in the prophase exactly as they merged into a
reticulum in the previous telophase. From the statements above, it is
not unreasonable to draw the conclusion that the chromosomes are
directly concerned with inheritance in cell reproduction.
THE CHROMOSOMES IN MEIOSIS
During the two maturation divisions by which the gametes are

formed, the number of chromosbmes is reduced to one-half the number
characteristic of the species. Since in the ordinary somatic mitosis the
number of chromosomes given to each daughter cell is exactly the same
as that of the parent, it is evident that we are dealing with a peculiar
type of mitosis (Fig. 28). The name meiosis is frequently applied to
the maturation divisions.
First Meiotic Division

The essential feature in which the first meiotic division differs from
ordinary somatic mitosis is that dih'ing one stage of the prophase the
chromosomes unite in pairs (Fig. 29, 2). This pairing is synapsis and
occurs only in the first meiotic division. Since each of the chromosomes
always divides during the prophase (Fig. 29, 4), the net result is that
at the end of the propha'se there appear to be only half the number of
chromosomes seen in somatic mitosis, but each of these consists of four
parts (chromatids) instead of two (Fig. 29, 5). These compound bodies
consisting of 4 chromatids are called tetrads (Fig. 29, 6). The quad-
A -A
ripartite nature of the tetrad may be expressed by the formula—'—,
a:a
where A represents one of the synaptic mates and a the other.
In the anaphase (Figl 29, 7), each of the daughter chromosomes
possesses 2 chromatids and is known as a dyad. As to the manner in
which the tetrads are divided, the best evidence appears to indicate
that the 2 chromatids, derived from each synaptic mate remain together.
Thus the dyads which separate may be represented &s A:A and a-.a.
The telophase (and prophase of the second meiotic division) is some-
times omitted if the second division succeeds the first immediately.
Second Meiotic Diyision
If these phases are omitted, each of tlie daughter cells divides im-
mediately, the chromosomes, still in the dyad condition, lining up on
the spindles for the metaphase of the second meiotic division. But even
ABCobc ABCobc
DIAGRAM COMPARING ^ \ ^
SOMATIC MITOSIS WITH
THE MEIOTIC MITOSES
First column! Ec\vaViona\

division of a diploid somatic
chromosome complement.
Second column'. The meio+Ic

divisions, changing the diploid
to t h e monoploid sti-ite.
obC ABc
Fig. 28. Comparison of somatic and meiotic mitosis {jrom SharpX.

64
The Chromosomes m Meiosis 65
Fig. 29. Diagram ilhi,strating chromosomal behavior during meiosis. Stages 1-8:
First meiotie division,! 1, Prophase, leptonema stage (relaxed, elongate chromo-
somes). S, Prophase, zygonema stage (synapsis or pairing of chromosomes).
3, Prophase, pachynema stage (thickening of chromosomes). 4, Prophase,
diplonema stage (formation of tetrads). 5;. Prophase, diakenesis stage (condensa-
tion of matrix). 6, IVêtaphase (tetrads on equatorial plate). 7; Anaphase (show-
ing dyads). 8, Telophase (daughter nuclei formed).
Stages 9-12: Second meiotie division. 9, Prophase (dyads united at attach-

ment points). 10., Metaphase (dyads on equfrtorial plate). 11, Anaphase
separation of chromatids which composed dyads). 12, Telophase haploid number
of chromatids in each of the four germ cells). {From Sharp.)
if the telophase of the first and prophase of the second meiotic divisions
are not omitted (Fig. 29, 8), it is obvious that the chromosomes arising
in the prophase (Fig. 29, 9), and forming the metaphase plate (Fig. 29,
10), are dyads and that they need undergo no other longitudinal split.
The anaphase of the second meiotic division (Fig; 29, 11) merely sepa-
rates the 2 chromatids of each dyad from each other. The final result
is that each of the 4 cells produced by the meiotic divisions (Fig. 29,12)
has 1 chromatid from each tetrad or y<>, the number of chromosomes
found before meiosis took place. This is expressed in another way by'
saying that the number of chromosomes has been reduced from the
diploid to the haploid (monoploid) number.
The second division always distributes the two chromatids of, each
dyad into different cells. Each of the 4 daughter cells receives 1
chromatid from each tetrad, and therefore 1 representative from either
one of the two synaptic mates {A or a), but not from both. .,. •
DisTBiBUTiON OF THE CHROMOSOMES. As cach tetrad orientg itself
independently upon the spindle it is evidently a matter of chance which
half of a tetrad, or of a dyad, goes to either pole of the spindle. Accord-
ingly, if 8 chromosomes, A, a, B, h, C, c, D, and d, were present in some
particular species, they, would unite in synapsis to form 4-double
chromosomes, Aa, Bb, Cc, and Dd. These would form the 4 tetrads,
—'-— , —'-—, —'—, and —'•— After the two meiotic divisions the
a:a b:b c:c d:d
mature germ cells would .receive 4 chromosomes (the haploid nurnber),
but only 1 chromatid representative of' each synaptic pair (îg. 30).
The possible combinations are 2*, or 16, namely, ABCDjÂBCd, ABcd,
Abed, ABcD, AbCD, AbCd, aBCD, aBCd, aBcd, abed, aBeD, abeD,
abCD, AbeD, and abCd. ' , •/ ,
It is easy to work out in a similar manner the numbCTit)f. gamete
types for various diploid chromosome numbers, in whi?h case the-;fol-
lowing data are obtained. . ,»
Diploid chromosome number 4 6 8 10 • 2ra
Haploid chromosome number 2 3 4 5 n.
Number of gametes 4 8 16 32. .
Number of gametes = 2^ 2-^ 2* 25 '2"
Obviously the number of different types of gametes in^ any given case
; may be determined by use of the formula 2", where n is the haploid
number of chromosomes.
THE CHROMOSOMES IN FERTILIZATION

Evidently when the egg and sperm unite in fertiRzation, the pro-
nucleus contributed by each contains the haploid. number of chromg-
The Chromosomes in Fertilization 67
Fig. 30. Diagram showing the distribution of tlie cliioniosoines in fertilization

and the following meiotic divisions. {After Wilson.)
somes. In this way the diploid number characteristic of the species is

restored. It is obvious that, unless the number had been reduced by
meiosis, it would be doubled in each new generation.
Further, it is clear that each germ cell contributes a homologous set of
chromosomes, and that in synapsis the chromosomes unite in homol-
ogous pairs. In the example referred to above, chromosomes A, B, C,
D came from one parent and a, b, c, d came from the other. We can now
visualize each synaptic pair as consisting of 1 paternal and 1 maternal
chromosome.
During meiosis the paternal and maternal chromosomes are sorted
out into different combinations in the different germ cells. During
. fertilization these different assortments are brought together in random
recombinations. • •
It has been seen that in any species of animal having 8 chromosomes
each parent could produce sixteen different types of gametes. Obvi-
ously one particular type of sperm produced by the male parent could
unite with any one of the sixteen types of eggs produced by the feniale
parent. Thus sixteen possible combinations are available to 1 sperm.
Since sixteen spenn types are produced, the total number of random
recombinations would be 16 X 16, or 16^ Many of these would be
duplicates, and it can readily be shown in this case that, by eliminating
the duplicates, the exact number of different or genotypic classes of
zygotes, according to theix combinations of chromosomes, would be 81
/
or 3*. Again, a general formula 3" (where n is the haploid, number of
chromosomes) can be derived by working out the actual combinations
in a few of the simpler cases.
If the chromosomal juggling that occurs during meiosis and the vari-
ations in recombination that can occur during fertilization are" con-
sidered, it seems evident that these mechanisms are concerned with
!5si
• ^
5^.
Fig. 31. Chromosomes of Protenor. k, A', Male diploid group.'B, B!, Female
diploid group. The X-chromosomes are indicated by Xy {Ajttr Wihon.)
increasing the variability of offspring while at the sarne time/maiptain-

ing the basic hereditary constitution of the species. ' f'. ^
SEX CHROMOSOMES, X - 0 TYPE. In many animals, such as the insect
•Protenor, the male has 1 less chromosome than the female, the^humbers
m Protenor being 13 and 14, respectively (Fig. 31). If the synaptic
pairs are assembled, it is clear that the male has six'pairs of ordinary
chromosomes (autosomes) and an extra one, the X-chromosome. The
female has six pairs of autosomes and a pair of X-chromosomes. Li the
female the X-chromosomes unite in synapsis, form a. tfeirad, and are
segregated in the meiotic divisions so that every egg has a complete set
of autosomes and 1 X-chromosome {A -\- X). In the male, on the other
hand, the single X-chromosome has no synaptic mate and so goes on the
spindle of the first meiotic division as a dyad, which is carried to one
pole of the spindle entire. In the second meiQtic division the dyad is
divided as usual. The end result is that Only half the spermatids
T h e Chromosomes m Fertilization 69
receive an X-chromosome, and two classes of sperms are formed, either
with or without an X-chromosome {A + X ov A + 0). If a sperm
with an X-chromosorae fertihzes the egg, the female combination
Meiotic Sperm
divisions /^ ^ ) Meiot
Meiotic
diâsions
Spermatogonium 7 ^
Ovum Oogonium
Sperm\^
?Zygote
Fig. 32. Diagram showing history of the X-chromosome during meiosis and fer-
tilization (after Wikon).
tcct<t*
ttM«M
Fig. 33. Chromosomes. of Lygaeus. A, A', Male diploid group. B, B', Female
diploid group. X and Y indicate the X- and Y-chromosomes respectively.
" ' (After Wilson.)
K
{2A + 2X) is restored. If a sperm without the X-chromosome pene-
trates the e g ^ the male combination (2A + X) is formed (Fig. 32).
SEX CHROMOSOMES, X ' Y TYPE. But the sexes do not always differ in
chromosome number, for in many animals, like the insect Lygaeus
(Fig. 33), the X-chromosome of the male is furnished with a synaptic
70 . T h e Mechanism of Heredity
mate which differs from it in size, form, and probably composition, and
is therefore linown as the Y-chromosome. The male forms a tetrad
—^—, and the sperm therefore have either an X-chromosome or a
Y-chromosome. Fertilization by a sperm bearing the X-chromosome
results in the development of a female {2A + 2X), whereas if a sperm
bearing a Y-chromosome enters the egg the embryo will give rise to a
male {2A + XY). ' ' '-^
FEMALE DIGAMETY. . As an exception to the general rule am'ong the
vertebrates, the birds have dissimilar sex chromosomes in the female.
The cytological details are difficult to interpret, but the theoretical
f
_r^ *s^=> 'A'l
*>'^
Fig. 34. Metaphase plates of male diploid chromosome groups. A, Frog (after
Witschi). fi,-Chick (after Hance). C, Man (after Painter)., -j
explanation is that the female has the two dissimilar sex chrpniosomes
X and Y, whereas the male possesses 2 similar sex bhrombsonies of the
X type (Fig. 342?). In this group, therefore, it is the^vum which deter-
mines the sex of the embryo rather than the sperm._,'Thi§,Explanation
• agrees with the data obtained from genetics. • . ,
Chromosomes of the Amphioxus • ' , ' •

The diploid number is 24. ' . •
Chromosomes of the Frog -i

The diploid number is 26, and the sex chromosomes of the male are
of the Z - y type (Fig. 34A).
Chromosomies of the Chick v

The diploid-number is 36. The sex chromosomes have not been
positively identified, but genetic evidence (Haldane) indicates that the
sex chfomoV)mes of the female are of the Z - . / type (Fig. 34B).
T h e Genes 71
(^liromosomes of Man
The diploid number, according to the most recent researches, is 48.
The sex chromosomes are of the X-Y type (Fig. 34C). I t is interesting
to note that with 48 chromosomes the possible types of gametes number
2^* or 16,777,300, and that from these 3^* zygote recombinations are
possible.
THE GENES
It has already been said that the behavior of the chromosomes might
suggest that these bodies are concerned with the transmission of heredi-
tary characters. -However, since the number of hereditary characters
usually far exceeds the chromosomes, smaller units than the chro-
mosomes must exist.
The unit of genetics is the gene. These genes are arranged in linear
order in the chromosomes. They exist in great numbers; in the fruitfly
Drosophila it is estimated that there are between 2000 and 3000. The
genes are known by the effects their presence induces, and named
according to the most obvious of these effects.
Since each chromosome contains a large number of genes it follows
that many of them remain in groups during meiosis and fertilization.
The number of these linkage groups, as they are called, corresponds to
the haploid number of chromosomes. But there are enough exchanges
of genes between chromosomes so that percentage values of these cross-
overs can be determined. On the hypothesis that the percentage value
of crossing over corresponds to the distance between the genes con-
cerned, chromosome maps (Fig. 35) have been constructed.
The work of Painter, Bridges, and others has demonstrated that in
Drosophila and other Diptera the exceptionally long and stout chromo-
somes in the cells of the s'alivary glands (Fig. 36) are marked by swell-
ings, constrictions, and transverse markings. Painstaking studies of
'these chromosomes has led to the identification of the regions in which
the genes are located, Whether or not the markings correspond to the
genes themselves is still debatable.
I
The question naturally arises as to the origin of the genes which are
allelic to the so-called normal genes. In Drosophila, the abnormal
genes, or mutants as(,they are called, arose in laboratory cultures. I t
has been discovered, that the rate of mutation, i.e., the number of
mutants arising in a' given number of flies, may be increased by high
temperatures (Plough) and by irradiation (Miiller). When one of these
genes is altered in any way to become a mutant, the course of develop-
ment is disturbed. Most mutant genes disturb the course of develop-
n m tv
y e l l o w (a) -|- 0. t e l e g r a p h (W) T 0. r o u g h o i d CE)
t Hairy wing CW} bent Cw)
t s c u t e (H)
4 ?. Star CE)
+ 3.± orristcilessCB) s h o v e n CB)
I lethal-T
e y e l e s s CE)
i b r o a d (W) •• 6.± e x p a n d e d fw)
p r o n e CE) r o t a t e d CB)
i W h i t e CE) M i r t u t e - K Ol)
fcce+CE) 12.i 6 u l l CW)
t Notch CE) . . 13. T r u n c a t e CW)
> Abnormal (B) • • I4.± dachsous (B)
> e c h i n u s (E) 16. S t r e a k CB)
) b i f i d (W)
i ruby (E)
' crossveinless CW)
tclubCW) 20. divergent (W)
t deltexCW)
c u t CW)
s i n g e d CH)
i t a n CB) 31. dachs CB) 26. sepia CE)
1 l o z e n g e (E) 26.5 h a i r y ( 6 )
••35. Ski-n fW)
vermillionCE)
m i n i a t u r e Cw) - - 4 1 . J a m m e d Cw) 35. r o s e CE)
! d u s k y CW) 36.2 c r e a m - m ("E)
t f u r r o w e d CE) 45.+ M i n u t e - e CH) 4 0 1 M i n u t e - h CH)
4a5 b l a c k CB) •• •• 40.2 t i l t Cw)
s a b l e CB) 48.7 J a u n t y CW) 40.4 D i c h a e t e CH)
I garne^t CE) 42.2 t h r e a d CB) male fertility
54.5 p u r p l e CE) 44. s c a r l e t CE)
57.5 c i n n a b a r CE) • • 48. p m k (£)

64.2 s m a l l w i n g - - 497 m a r o o n CE)
: •- 54.5rudimentary OV)' 60.± safraninCE) |50.± d w a r f CB)
56.5 f o r k e d CH) J50. c u r l e d CW)
-•'• 5 7 . B a r CE)
- 58£ s m a l l e y e - • 64.± pink-wing CEW) • - 54B Hairy wing supr
1 E8.2 Stubble CH)
'•'- 59. f u s e d (W) i 58.5 spinelessCH)
. - 59.6 B e a d e x CW) 67. v e s t i g i a l (w)
62. M i n u t e - n (H) 68.± t e l e s c o p e CW) - \ 587 bithoraxCB)
'"59.5 blthorax-b
- - 65. cleft Cw; -,62. s t r i p e CB)
• -72. L o b e CE)
'"63.1 g l a s s CE) Long bristled
74.± grapCw) 66.2 beltaCW;
— 1 70. bobbedCH) 75.B curved CW • - 69.5 h a i r l e s s C H )
• - 707 e b o n y C B ) I
•• 72. band,CB)
. . '7S.7 c a r d i n a l C E ) '
•835 f r i n g e d Cw) 76.1 w h i t e ocell.r(E)
• 90. h u m p y CB)
M
w - - 99.5 a r c Cw)
- t005 p l e x u s Cw)
102.± T e t h a l - n a
91.1
93.
9J.8
94.1
r o u g h CE)
crumpledtw)
B e a d e d Cw)
P a i n t e d CW)
1007 c l a r e t C E )
l o t . M i n u t e CH) ^
I male fer+illt-y
'
J - 106.2 M i n u t e - g CH)
FIG. 35. 'The chromosomes of Drosophila melanogaster and map shewing the
positions of many genes as determined from, crossover ratios.. Letters in paren-
theses indicate part of body affected; B, B o d y ; E, e y e ; H, hair; W, wing.
AVrows indicate position of attachment point. All genes in IV are closely linked.
T h e exact position of genes in Y still undetermined. (From Sharp, ajter Morgan
et al., 1925, and Stern, 1929.) '
72 « ' •
The Genes 73
ment so greatly as to cause death (lethal mutants). A smaller number
produce visible changes when present in each chromosome of the
synaptic mates (recessive mutants). A few produce visible changes
if contained in a single chromosome (dominant mutants). Accordingly,
every species of animal contains a certain number of mutant genes
(500 in Drosophila). As these enter into new genetic combinations
according to the behavior of the chromosomes in meiosis and fertiliza-
SCALE I—5iM-*|
fmmm
Fig. 36. Chromosomes of Drosophila. Above, metaphase of oogonium, arrow
pointing to pair of chromosomes IV. Below, pair of chromosomes IV in salivary
gland. Both to same scale. {From Curtis and Guthrie, after Bridges.)
tion, they give l-ise to individual differences in development. But the

greater number of stable or non-mutant genes hold development true
to the specific type.
The question of the role of the genes in the control of embryonic
development is so important that a great deal of experimental work
has been directed to this problem. However, in spite of the fact that
much information has been obtained, the exact manner in which the
genes affect developrnent is not yet entirely clear. A few aspects of this
work will be considered.
One of the earliest investigations of this sort was the attempt by
Ephrussi and Beadle to determine the mechanism for control of eye
color in Drosophila. The method used was to transplant the imaginal
eye discs from larvae of one genetic constitution into larvae of another.
74 T h e Mechanism of Heredity '
thus bringing tissues containing different genes into close association.
It was found that the genes for eye color control an elaborate series of
interactions. Furthermore, the implanted material appears to control
the eye color developed, but no direct information was obtained as to
the exact way in which the genes produce this effect.
In the vertebrates the situation is somewhat similar. In birds, for
example, it has been shown by Dushane that feather color pattern is
governed by the gene. Transplantation experiments were made, involv-
ing the mutual interchange of small pieces of dorsal ectoderm and
associated neural crest tissue between 3-day-old chick embryos of
different colored breeds such as White Leghorn and Barred Rock.
When feathers were developed in the transplanted area they exhibited
the color pattern which would have developed had they remained in
the donor animal. Furthermore, the neural crest tissue gives rise to the
pigment-forming cells, and the activities of these-cells must'be under
control of the genes carried by them. I t seems reasonable to suspect
that some enzymatic action is involved. - '
It also appears quite evident that the cytoplasm of the blastomeres
is affected in every case. In eggs in which organ-forming substances
can be identified at fertilization it is clear that as cleavage progresses
these substances aVe.relegated to individual groups of blastomeres;
hence the cytoplasm of particular groups of cells must become increas-
ingly different. Consequently, although the nuclei of these cells afe
apparently identical, a time will arrive when th* genes of the cells in
a given area may react with the special type of cytoplasm contained
in these cells to bring about the development of a particular ,structure.
Nowhere else in the organism will this same situation.prevail. Hence
new structures will be developed in the new organism atf the,proper
.place and in the proper sequence. , " . ' *
On the other hand, in eggs which remain highly plastic .the process
of gastrulation must establish permanent differences in-the. cytoplasm
of the cells in particular areas. Thereafter interaction'of'the genes
with the cytoplasm of these cells probably brings about the dilferen-
tiation of cell types necessary for,the differentiation of'special struc-
tures. An example of this situation is to be found in the differentiation
of epidermis and neural tube from ectoderm cells all'vOf which have
similar nuclear constitution, but the neural cells come uiider the direct
influence of the organizer (notochord) whereas the epidermal cells
do not. *
Chromosomes of Vertebrates
By contrast with Drosophila not much is known concerning the loci
of genes on the chromosomes of vertebrates because of the large number
The Genes 75
I
n Two pairs of homologous chromosomes
m showing positions of allelic genes.
ai J, A a A
Crossing over. The chromosomes of the
B(T)6 B b pair shown in A may twist about one an-
c 1 C c c other as in C and break in the plane of the
dotted line so that comparable sections are
d D d D
exchanged as shown in D.
a A a A
Deletion. One member of the chromo-
b B b B some pair shown in A may twist on itself
C d C as in E and break in the plane of the dotted
D D line so that an internal section containing
gene c is lost, or deleted, as shown in F.
E
a A a A
C Inversion. One member of the chromo-
b Q b C some pair shown in A may twist on itself as
c D c B in G and break in the plane of the dotted
line so that the section containing genes B
d d D
and C is inverted as shown in H.
G H
Duplication and deficiency. If one mem-
A
ber of the chromosome pair shown in A
a a
comes to lie across the other as shown in I
b b B
Y and a break occurs in the plane of the
c
d
V
Jo '
c
d
a
1
dotted line, the chromosome on the left in /
will have a duplication and contain both
D gene d and gene D, whereas the chromo-
4 some on the right_will have a deficiency of
the section containing gene D.
Translocation. One member of the chro-

mosome pair shown in A may come to lie
across one member of the chromosome pair
shown in,B, as seen in K. If a break occurs
in the plane of the dotted line, sections
of non-homologous chromosomes are ex-
changed, or translocated, as shown in L.
Fig. 37. 'Diagrams to show crossing over and various chromosomal aberrations
ijrom Curtis and Guthrie).
of chromosomes involved in most cases and the difficurty..-of testing
a mutation for linkage. Some information is available in a few forms
such as the mouse and the fowl. In the fowl Hutt (1949) has assem-
bled data showing the approximate locations of 24. linked genes on
6 chromosomes. ' •
Fig. 38. Intersexes and supersexes in Drosophila, occurring in the pr'qgeny of trip-
loid females. A, Female-type intersex. B, Male-type intersex. - C, Superfemale.
D, Supermale. a, h, c and d are the chromosome groups characte'fistie of A, B, C,
and D respectively. {From Curtis and Guthrie, after Morgan et al.)
Chromosomal Aberrations \
Of particular interest to the student of embryology 'are the new
types of individuals arising from disturbances* in .the uûal course of
meiosis. Some of these chromosomal aberrations, are shown graphically
in Fig. 37. One of the most striking types of aberration is known as
non-disjunction, which may affect one to all of the chromosomal pairs
during meiosis. In total non-disjunction, the me.mbers-of each synaptic
pair fail to separate during a meiotic division so that one daughter cell
êts a double set of chromosomes while its sister cell receives none.
The Genes 77
As a result there will be 1 gamete with the diploid number of chromo-
somes. If such a gamete with the diploid number {2A + 2X) is fer-
tilized by another with the haploid number {A + X), the zygote will
have 3A + 3X, the triploid number. Such a fly is a female, and her
progeny will show many interesting characters due to the chromo-
somal aberrations involved, as shown in the table below.
SEX AND GENIC BALANCE
gg formula Sperm jormula Zygote jormula Ratio X/A Sex

A + 2X A+X 2A + 3X 1.5 Superfemale
(Fig. 38C)
2A + 2X A+X 3A + 3X 1.0 Triploid
Female
A+ X A+X 2A + 2X 1.0 Diploid
Female
24+ X A+X 3A + 2X . 0.67 Intersex
A + 2X A+Y 2A + 2X + Y 1.0 Diploid
Female
2A + 2X A+Y 3A + 2X +Y 0.67 Intersex
A+ X A+Y 2A+ X +Y 0.5 Male
2A+ X A+Y 3A+ X +Y 0.33 Supermale
(Fig. 38£>)
Examination of the ratio between the X-

chromosomes and other chromosomes (auto-
somes) suggests that the determination of sex
depends on some sort of ratio between the
•genes in the X-chromosomes and the auto-
somes. Bridges (1921) has formulated a
theory of genic balance to account for the
observed results. In the development of the
intersexes, the individuals commence as males
but at a particular time shift to the type of
development characteristic of females. The ^'S- 39. Gynandromorph
characters determiried before the shift are ^^ Drosophila. Note eosin
male, those'after it are females. As the time eye and miniature wing on
right as compared to red
at which the shift takes place is variable the eye and long wing on left.
intersex may be of the female type (Fig. 38A) This fly is male on the right
or of the male type (jFig. 3 8 B ) . side and. female on the
.GYNANDROMORPHS; Intersexes must not be <
' =f*^- ^^^^^': ô'-s«" "'"^
BvzdoGs)
confused with gynaiidromorphs, which are in-
dividuals with one part of the body male and the rest female.
Bilateral gynandromorphs in Drosophila (Fig. 39) arise from female
zygotes {2A + 2X), but during the first cleavage division one of
the X-chromosomes is lost on the mitotic spindle. The result is
that one of the daughter cells has the female complex (2A + 2X)
while the other has the male complex {2A + X). Sometimes such an
aberration takes place in a later cleavage division so that there is only
a small area of male cells. Such individuals are called chimeras.
TERATOLOGY. All students of embryology are familiar with the fact
that development does not always proceed normally. Abnormal em-
bryos are known as monsters, and their study forms the subject-matter
of the embryological subscience known as teratology. I t is clear from
the sections just preceding that many of these monsters must be due
to chromosomal aberrations with consequent disturbance of the genie
balance. Others, as will be noted in Chapter 10, are due to environ-
mental factors.
Cleavage and Formation
of the Blastula
The fertilized egg is a complete and balanced cell. It has^two entire
sets of chromosomes each with a full complement of genes, one set
received from each parent. These nuclear elements are combined in a
cell whose cytoplasm is principally of maternal origin. Furthermore,
the process of fertilization supplies some stimulus whereby the develop-
ment of a new individual is set in motion. This is manifested by the
occurrence of a series of mitotic cell divisions. In this way a large
number of cells is formed and the process of cleavage culminates in. the
formation of a blastula where the embryo is in the form of a hollow
sphere or disc. Following the formation of the blastula further changes
occur in the embryo resulting in the segregation of the three primary
germ layers. This process is called gastrulation, and as a result of it
an outer layer of ectoderm, an inner layer of endoderm, and an inter-
mediate layer of mesoderm are formed.
It is very necessary to understand clearly the significance of the
processes involved in cleavage and the formation of the blastula and
gastrula. These processes are in reality far more than the mere
mechanical division of the fertilized egg cell into 2, 4,8, etc., blastomeres
and the simple rearrangement of these cells to form the germ layers.
They involve a* profound reorganization of the materials present in the
fertilized egg cell and bring into play intricate forces and influences
which guide the process of development to its normal conclusion.
: LAWS OF CLEAVAGE
In general, cleavage is an orderly process and the cleavage planes

arise according to a fairly definite pattern and in a particular relation-
ship to each other. As a result, certain rules have been formulated to
express the simpler geometrical relationship between the blastomeres.
These are Well illustrated by the early cleavages of amphioxus and
frog eggs.
79
80 ' • • Cleavage and Formation of the Blastula
Rules of Cleavage
1. Sachs' rules
a. Cells typically tend to divide into equal parts.
b. Each new plane of division tends to intersect the preceding one at
right angles.
2. Hertwig's rules
a. The typical position of the nucleus (and he'nce of the mitotic figure) is
in the center of its sphere of influence, i.e., of the protoplasmic mass in
which it hes.
b. The axis of the spindle hes typically in the longest axis of the proto-
plasmic mass, and division, therefore, cuts this axis transversely.
3. Balfour's law, . The rate of cleavage is inversely proportional to the
amount of yolk present in the egg.
Types of Cleavage
Ift
On the basis of the amount and distribution of yolk several different
types of eggs can be recognized. The amount of yolk present in the
egg influences profoundly the kind of cleavage pattern-whibh occurs,
and several types of cleavage may be distinguished on this basis.
Holoblastic^ cleavagejis_ characteristic of both isolecithal and moder-
ately telolecithal _e|gs^ and in it the cleavage planes divide' the egg
A . B ' -C* . *
Fig. 40. Diagram to show main types of cleavage in vertebrates. A, lilqual-holo-

blastic. B, Unequal holoblastic. C, Meroblastic. ^
completely info separate blastomeres. In i^n1p>citlialegg;s. such as that

of amp^higxus. the blastomeres are usually equal m size, hencp_^cleavage
is equal holoblastic (Fig. iOA); whereas, in moderately- telolecitlTal
eggs, such as that of the frog, the blastomeres are unequal and hence
cleavage is described as unequal holoblastic (Fig. 405). MeroMaatf^—
clegiiage (Fig. 40C), on the other hand, is characteristic^)!: extremely
N / telolecithal eggs in which the cleavage planes do not pass through the
"yolk; hence_the_bfastomeres come to he upon a mass of undivided yofe,
a i in the chick.
Laws of Cleavage 81
Cell Lineage
I t must not be thought tha-t cleavage results in a mass of identical
blastomeres. Painstaking examination of dividing eggs has shown that
in the normal development of favorable material the origin and fate
Fig. 41. Cleavage of Styela egg. A, 4-cell stage, from left side. B, Same stage,
from animal pole. C, 8-«cell stage, from left side. D, Same stage, from animal
pole. Explanation of labeling of cells: Capital letters == cells of animal hemi-
sphere ; lower caê letters == cells of vegetal hemisphere. A or a = anterodorsal,
B or b = posteroventral. Letters underlined = cells of right side. Exponents—
• 1st figure = cell generation; decimal = number of rows from vegetal pole.
(From Richards, after Conhlin.)
of every blastomerej can be determined accurately. The genealogical

history of the blastomeres is known appropriately as cell lineage. One
of the most clean-cut examples, in forms allied to the vertebrates, is
the cell lineage of^the tunicate Styela (Cynthia), worked out by
Conklin in 1905. Using an ingenious method for identifying individual
blastomeres, he w^s able to follow these cells and determine their
ultimate fat? (Fig. 41),
'*By the sixth generation (32-cell stage) the organ-forming regions
have been segregated into different blastomeres as follows: .
, ' 82 Cleavage a n d Formation of the Blastula
Animal hemisphere: • ,
14 Ectoderm, epidermis.
2 Ectoderm, neural, plate.
Vegetal hemisphere:
4 Ectoderm and mesoderm, chorda-neural plate.
4 Mesoderm, gray crescent.
2 Mesoderm, yellow crescent.
6 Endoderm cells
32 ' •
The cell lineage of many types of invertebrates has been investigated

in a similar manner, but the only vertebrate form in which the cell
lineage has been reported is the minnow, Fundulus (Oppenheimer,
1936). In normal development it may be concluded that during
cleavage the successive generations of blastomeres show a progressive
differentiation. Earlier or later, the organ-forming materials of the .
fertilized egg are segregated into different groups of blastomeres,-which
thus become the organ-forming areas of the blastula.'
Later (Chapter 10), experiments will be described which indicate
that individual blastomeres may, under proper experimental conditions,
give rise to parts of the embryo other than those which they normally
produce.
^ T H E BLASTULA. The period of cleavage terminates in the appearance
'^ of the blastula, but this does not mean that cell division comes to an'
end. (Th_e blastula is generally defined as a^lioHow^sphere of blastor
meres__jurrouii3lng a cavity, the blastocoel.) This definition;, however,
(Toes not fit the blastulae formed by merobla'stio cleavage. Accordingly, •
three classes of blastulae are recognized, as follows: , t
1. Coeloblastula, a blastula in the form of a hollow sphere resulting
from holoblastic equal cleavage as in the egg of amphioxus (IJig.>42A).
A variation of this type in which the blastocoel is displaced toward the
animal pole, as in the frog (Fig. 42B), is the result of unequal holo--
bjastic cleavage. i
'"^ 2. Discohlastula, a blastula which is the result ofmieroblastic' cleav-
age and in which the blastomeres form a flat disc, or'blastoderm, resting
on the yolk mass (Fig. 42C). The segmentation cavity later combines
I with the yolk cavity formed by digestion of the'yolk underlying-the'
blastoderm and so forms a blastocoel. Such a blastocoel is therefor^
ropfed with cells but has a floor of yolk.
^ 3 . Blastocyst, a type of blastula which is found only in mammals
(Fig. 42D). A solid morula .formed during cleavage develops a cavity,
Laws of Cleavage 83
the blastocoel, which enlarges until it almost completely separates off
an outer layer of cells, the trophoblast, from an inner cell mass, the
embryonic knob.
PBESUMPTIVE ORGAN REGIONS OF THE BLASTULA. As might be in-
ferred from *he results of cell-lineage studies, the regions of the blastula
will give rise to different parts of the embryo in normal development.
Blastocoel
D
Fig. 42. Diagrams of vertebrate Mastulae. A, Coeloblastula following holo-
blastic equal cleavago' (amphioxusT. B, Coeloblastula following holoblastic un->
equal cleavage (frog*/, i C, Discoblastula following meroblastic cleavage (chick).
: 35, Blastocyst (mammalsK
In the tunicate and amphioxus, Conklin has mapped out the presump-
tive organ regions of the blastula, and Vogt and his students, by means
of a most ingenious technique, have accomplished the same result for
the amphibian blastula. Experimental evidence (Chapter 4) indicates
that'in the tunicateiând amphioxus the fate of organ-forming regions
is definitely determined even in the fertilized egg, whereas, in amphib-
'ians, t h e ' regions haVe a greater plasticity and may under proper
circumstances give rise to parts of the embryo quite different from those
formed in normal development.
84 Cleavage and Formation of the Blastula
Cleavage
The Amphioxus ^^^ »—'~^
In the egg of the amphioxus (Fig. 43), which is isolecithal, cleavage
is holoblastic and almostequaJL The first cleavage cooftnences as Ja
furrow at the animal pole, which later assumes a groove-hke form and
elongates until it becomes a wide meridional furrow extending around
the egg. This constriction deepens until the egg is completely divided
Anterior
Fig. 43. Cleavage oi, the amphioxus egg. A, Before cleavage. 5 , Commencing
first cleavage, from posterior side. C, Second cleavage, from vegetal, pole". D\
Third cleavage, from left side. E, Fourth cleavage, from vegetal pole. ;¥, Fifth
cleavage, side view", segmentation cavity indicated by dotted lines^ X't66. (After
Conklin, 1932.) / ••^' .'»
into 2 blastomeres each of which assumes a spherical' shape. ,The.

second cleavage, also meridional, commences at the animal pole' and
is at right angles to the first, following Sachs' second "rule. • The third
plane of cleavage is at right angles to both the first and second. Hence
it would be equatorial, but, since the yolk is slightly concentrated at
the vegetal pole, tlie third cleavage plane, following Hertwig's firstrule,
is latitudinal and slightly nearer the animal pole. The quartette of cells
in the animal hemisphere is therefore smaller than those,in the vegetal
hemisphere. The smaller cells are called micromeres; the larger ones,
macromeres. The fourth division divides each of the 8 existing blasto-
meres in two. There are two planes of cleavage, each meridional, at
right angles to the third, and also at right angles to each other. Some-
Laws of Cleavage 85
times the cleavage planes of the fourth division are parallel to each
other instead of being at right angles. This makes the bilateral sym-
metry of the dividing egg quite
Presiiinptive
obvious. In the fifth cleavage ectoderm
32 cells are produced, again by
two planes of cleavage, at right
angles to the planes of the fourth,
but this time latitudinal and
parallel to each other. From
this time on cleavage becomes
more and more irregular. The
early cleavages have been fairly Presumptive
mesoderm
regular; each has' divided the
entire egg mass; and the blasto- Presumptive
endoderm
meres, with the exceptions noted,
have been almost equal. The Fig. 44. Blastula of the amphioxus, sag-
ittal section, X155 (after Conklin).
blastomeres round up as each
cleavage is completed, and a jelly is secreted between them. In this
way a small cavity called the segmentation cavity or blastocoel IS
formed.
Conklin (1933) states that comparison of the cleavage of the amphi-
oxus with that of the tunicates shows a general .resemblance between
the two in the distribution of the organ-forming substances to the
blastomeres, in the generally bilateral type of cleavage, and the order
of division; but in all respects the tunicate egg is the more precise and
the more precocious in differentiation.
Jn the development of the amphioxus we find a good example of the
coeloblastula (Fig. 44). The blastomeres are arranged in a single layer
around the enlarged blastocoel, which is entirely cut off from the
exterior. The blastomeres at the animal pole are rmcromeres; those at
the vegetal pole are; ma'croraeres; the cells at the equatorial belt are
transitional in type.
The cells which are to form the mesoderm are rounded and in active
mitosis. They are arranged in a crescent on one side of the egg, whereas
those which will forrn the chorda-neural plate make up a corresponding
crescent on the other. The endoderm cells are the larger cells of the
vegetal hernisphere. '-
The Frog ;
The frog's egg (Fijg. 45) is telolecithal with holoblastic unequal
cleavage. Here the first division commences as a depression at the
animal pole, which elongates and extends around the egg as a shallow
86. Cleavage and Formation of the Bias tula
furrow until the ends meet at the vegetal pole. The constriction also
extends inward, most rapidly at the animal pole, and eventually bisects
the egg into 2 blastomeres which round up very slightly. The plane of
the second division is also meridional and through the aninial pole but
at right angles to the first. The first two cleayage planes intersect" each
other at the animal pole.
/
({
Unfertilized Gray crescent 2-cell 4-cell
0 Hours 1 Hour 3.5 Hours 4.5 Hours
8-cell It) Ctll 32-cell Mid-cleavage

5.7 Hours 6.5 Hours 7.5 Hours 16 Hours
/"*\
•IS
Late cleavage Dorsal lip Mid-gastrula Late gastrula

21 Hours 26 Hours 34 Hours 42 Hours
Fig. 45. Cleavage and gastrulation in the frog, Rana pipiens,'-Ages given%re at
a temperature of 18°C; XIO. {Rearranged from Shumway, Anat.'R%c.(78:143.)
As the blastomeres round up, however, two of them which are diag-
onally opposite each other are pushed away from the point of inter-
section by the other two. These last flatten against each other to form
a short polar furrow. The third cleavage is latitudinal, but about 45°
from the animal pole, and the micromeres are considerably'smaller than
the macromeres. Theoretically the fourth and fifth planes of cleavage'
bear the same relationships to the earlier ones as do those'of amphioxu's,
but actually they are more irregular. The two planes of the fourtli
cleavage often fail to reach the vegetal pole and hence become vertical
rather than true meridional planes. As these planes originate in the
animal hemisphere, the micromeres are divided before the macromeres,
so that a 12-cell stage intervenes between the 8-cell and 16-cell stages.
Laws of Cleavage 87
Similarly, following Balfour's rule, the latitudinal cleavage plane of
the fifth division in the animal hemisphere often appears and is com-
pleted before the corresponding plane in the vegetal hemisphere, so that
there is a 24-cell stage before
the 32-cell stage is attained.
The cell lineage of the frog's
egg has not been followed in Marginal •
detail as has that of the ^®'*'
tunicate or amphioxus. It is
known, however, that the first
cleavage plane ordinarily di-
vides the gray crescent into two
symmetrical halves, so that ^^'
cleavage is normally bilaterally
symmetrical from the outset. The segmentation cavity, visible from
the third cleavage on, is-displaced toward the animal pole and toward
the gray crescent side of the cleaving egg.
' The blastula of the frog (Fig. 46) resembles that of the amphioxus
in all essential characters, but shows minor differences due largely to
the greater amount of yolk present. In the first place, the blastoderm
is no longer one layer of cells in thickness. Tangential divisions have
increased the number of cells .so that at the animal pole the blastoderm
may be 3 or 4 cells deep. Furthermore, the greater difference in size
between the micromeres of the animal pole and the macromeres of the
vegetal pole results in the-blastocoel occupying an eccentric position
entirely within the limits of the animal hemisphere.
_ The blastula of the frog shows certain regional differentiations. Thus
the cells of the animal hemisphere are smaller than those of the vegetal
hemisphere, and contain pigment granules. Between the micromeres of
the animal pole and the macromeres lies a band of cells of intermediate
size, known as the marginal belt or germ ring. This region corresponds
to the region of the! gray crescent.
Vogt has demonstrated the fate of different regions of the amphibian
blastula in normal |development by marking them with such harmless
dyes as Nile blue dnd neutral red. The stain persists long enough so
that the migration of the colored cell groups can be traced through
gastrulation and qyen later. In the fire-toad {Bombinator igneus)
Vogt has succeedetl in mapping out the surface of the blastula into
presumptive organ'regions (Fig. 47). Another anuran [Discoglossus)
has been stttdied by Pasteels (1936) with similar results. Although the
frog (Eana pipieus) has not yet been similarly studied it seems fairly
certain that its organization is similar.
Cleavage and Formation of the Blastula
Laws of Cleavage 89
The Chick
In tfelolecithal eggs with meroblastic cleavage, such as that of the
ig^l, only the protoplasm of the egg, i.e., the blastodisc, is divided, and
the cleavage planes do not segment the yolk (Fig. 48). The first furrow
Fig. 48. Cleavage of .the hen's egg. A, First cleavage. B, Second cleavage. C,
Third cleavage. D, Later cleavage. All from animal pole. Approx. X12 (A, B,
D, after Kolliker; C, after Patterson.)
commences at the animal pole and extends outward toward the edges
of the blastodisc. The second is formed by two furrows, at right angles
to the first, one in each blastomere, which grow toward the first furrow
and also toward the edge of the blastodisc. They may join the first
furrow at'a^roximately the same point or at separate points, in which
case a polar furrow is formed. These 4 cells are incomplete, as the
furrows do not extend all the way to the yolk nor to the edge of the
blastodisc, but remain connected both belaw and at their- margins.
From this point on, cleavage is irregular; Some cleavage planes are
circular and cut off central cells from marginal. These may be com-
pared with the latitudinal planes of the holoblastic type. Others are
radial, like the first and second. Still others are tangential and divide
the central cells into upper and lower layers, as in the frog's egg.
The blastula of the chick (Fig. 49) is a discoblastula. The -blasto-
derm consists of _an inner group of micromere_s completely separated
from each other by cleavage planes, and of an outer ring of marginal
cells partially separated from each other by incomplete radial'cleavage
'planes only. These latter cells are in direct protoplasmic continuity by
means of an outer ring of undivided cytoplasm called the periblast.
Blastocoel Blastomeres
Hypoblast \ / Periblast
Yolk * • • • •
Fig. 49. Section of early chick blastula. Compare Fig. 48Z). (.4/fer Patterson.) <
Beneath the central cells there is also a thin layer of undivided cyto-
plasm (hypoblast), which soon disappears. The inner micronieres are
separated from the underlying yolk by a thin cleft or yolk cavity which
is sometimes called the blastocoel. It is probably not hDmologou§j.with
the blastocoel of other species. • ~ .
As the blastoderm expands over the yolk new cells are added to the
inner cell mass at its outer.border. The periblast contributes its. cyto-
plasm to the formation of these new cells. Meantime the outer riin
continues to grow out and over the yolk. With the dis^pearance of the
hypoblast, the cells overlying the yolk cavity constitute a region of the
blastoderm known as the area pellucida because when detached from
the yolk it is free of yolk particles and hence appears quite transparent'
especially in prepared mounts. The outer zone beyond the area pel-
lucida makes up the area opaca, so called because particles of yolk
adhere to its under side when removed from the egg and render the
region less transparent. As the edge of the blastoderm advances the
cells at the extreme periphery are lifted slightly above, the yolk to form
the margin of overgrowth. The cells just inside the margin of over-
Laws of Cleavage 91
growth, and still in contact with the yolk, form the zone of junction.
Those just inside the zone of junction and recently added to the area
pellucida are known as the germ wall (Fig. 71).
Man and Other Mammals

The cleavage of the human ovum has not yet been observed, but in
the egg of the monkey and rabbit the cleavage is clearly of the equal
hmbblastic tjipe (Fig. 50). In the rabbit*the first cleavage takes place
about 2 2 ^ Iwirs after coitus. It is equal and complete. The second
cleavage f o l ^ ^ ^ i n about 3 hours. Here the two cleavage spindles
Fig. 50. Cleavage in mammalian egg. A, First cleavage. B, Second cleavage.

0, Third cleavage. 4, B, C, Monkey, X170. (Ajter Lewis and Hartman, in
Arey.) D, Third cleavage. E, Fourth cleavage. F, Fifth cleavage. D, E, F,
' Rabbit, X180. {After Gregory.)
frequently lie at right angles to each other so that the 4 blastomeres

assume the form of a cross. Cleavage is now irregular, 5-, 6-, 7-, and
8-cell stages appearing in order. The 8-cell stage is attained about 32
hours after coitus.. There is now considerable difference in size, the
largest blastomerCj being almost twice the size of the smallest. The
16-cell stage is reached in another hour and a half. In reaching this
etage one tangential cleavage has occurred so that 1 cell is completely
enclosed.; -Jn later divisions more tangential cleavages occur, and this,
with the shifting of the blastomeres upon each other, results in the
formation of a solid mass of cells called a morula.
No human embryo in the blastula stage has been recorded,- so A
description of the blastocyst of the rabbit will be given in its place.
About 75 hours after coitus and while the egg is still in the oviduct, a
cleft, the blastocoel, appears in the morula, apparently due to the ac-
cumulation of fluid. This cavity extends rapidly until the trophoblast
is separated from the embryonic mass. The separation is almost' com-
plete (Fig. blA), extending about 270° of the possible 360°. By this
/Embryonic knob
Albumen Embryonic '<fs
disc
Fig. 51. Sections of rabbit blastocysts, X200 (after Gregory).
time the blastocyst has reached the uterus and the amount of fluid has
greatly increased, expanding the blastocoel and stretching the tropho-
blast cells. The embryonic mass flattens against the trophoblastj .and'_
the entire blastocyst increases greatly in size (Fig. 51B). ^This flatten-
ing 5f the embryonic mass is not characteristic of all mammalian
blastocysts. . . '
ORGAN-FORMING REGIONS. It is noteworthy that, unlike the amphi-
oxus and the frog, the segregation of presumptive organ-fDrming regions
in the chick and man is not clearly established when the blagtula'ia
formed. However, the process is carried to completion during âstrii"-
lation
7
Gastrulation and Neurulation

GASTRULATION
The vertebrate blastula is converted into a stratified embryo or
gastrula by the pr'ocess of gastrulation, as a result of which the three
primary germ layers, ectoderm, mesoderm, and endoderm (entoderm),
are ultimately segregated. This is accomplished by the migration of
cells from the exterior to the interior of the embryo. When this occurs
the blastocoel is obliterated and replaced by a new cavity, the gastrocoel
or archenteron. In forms with a coeloblastula, like amphioxus and the
frog; this cavity communicates to the exterior by means of an opening,
the blastopore. In forms with a discoblastula, like the chick, or with
a blastocyst, like the mammal, the blastopore is replaced by a longi-
tudinal groove, the primitive streak.
During the cell migrations characteristic of gastrulation a two-
layered stage intervenes between the blastula and the completed
gastrula. This results from the fact that in forms such as the frog the
ectoderm separates out first, leaving endoderm and mesoderm tem-
porarily associated as mesendoderm. In other cases such as the chick,
the endoderm is segregated first, leaving ectoderm and mesoderm associ-
ated as mesectoderm. In all cases the middle germ layer soon separates
itself from the endoderm or ectoderm with which it was temporarily
associated. It is then seen to be composed of the notochord, an axial
supporting rod found onlyîn the vertebrates and'their allies the proto-
chordates, and two lateral sheets of mesoderm, one on each side of the
notochord. Later, wandering ameboid cells, originating for the most
part from the mesoderm, and known collectively as the mesenchyme,
make their appearance.
Gastrulation in the jA^mphioxus

The first indication of gastrulation is a flattening of the macromeres
of the vegetal hemisphere (Fig. 52A). These cells divide less frequently
and become more oplumnar, whereas the others divide more rapidly
and become more cubical or spherical. This change in the shape and
93
94 Gastrulation and Neurulation
rate of division, according to Conklin (1932), is the principal cause of
invagination (Fig. 52B), although it may be due also in part to the
resorption of material from the blastocoel jelly, or to exosmosis, for
the contents of the blastocoel become less viscous as gastrulation
proceeds.
In later stages of gastrulation the gastrula increases in length,.owing
to the backward growth of the lips of the blastopore (Fig. 52C), "While
Presumptive ectoderm
Presumptive
chorda-
neural plate
mesoderm Presumptive
endoderm
Verli I
Notochord
Neural plate
^ D
Blastopore
Fig. 52. Sections of amphioxus embryos during gastrulation. A, Blastula ,'(6 hours
after fertilization). B, Gastrula OVa hours). C, Gastrula (12 hours)._ D, gastrula
(14 hours). Animal pole indicated by presence of polar body. Anteroposterior '
axis shown b y arrow. All sagittal sections, X180. {Ajter Conklin,)
this is taking place, cells are being rolled from the exterior ovei the rim
of the blastopore, into the interior, a process called involution.^ The
lips of the blastopore grow unevenly, the ventral lip finally turning"
upward to reduce the blastopore to a very small opening (Fig. 52D).
This -was thought to be due to concrescence or the growing together of
the right and left halves of the dorsal lip of the blastopore, b't^t Conklin
expressly denies that this occurs. The cells left on the exterior after
gastrulation is complete are ectoderm. Those which have been carried'
to the interior are endoderm, and presumptive chorda-mesaderm. j In
late gastrulation the cells of the ectoderm develop cilia,- by mean's of
which the embryo rotates within its fertilization membrane. The cells
of the mesoderm and notochord form the lip of the blastopore', the noto-
chord cells at the dorsal lip, mesoderm at the ventra4jpd lateral lips.
Gastrulation 95
A.S the. lips of the blastopore grow backward, these cells are carried to
the interior by involution.
When the ventral lip grows upward, the mesodermal crescent is tilted
up behind so that its arms run in an anteroposterior direction at the
angles between the dorsal and lateral sides of the blastopore. From
each point of the crescent a band of mesodermal cells grows forward,
while between them the notochord also grows forward to form a median
band.
SEGREGATION OF THE MESODERM. At the completion of involution in
the amphioxus, the floor and sides of the gastrocoel are formed by
Neural plate
Notochord •
Mesodermal
groove
Gastrocoel Gastrocoel
Mesodermal Blastopore
groove
Notochord
Neural
plate
Blastopoie
Fig. 53. Optical hemisections of amphioxus gastrula (14-hours after fertilization).

A, Interior view of left half. B, Posterior end to show notochord and mesodermal
grooves. X166. {After Conklin.)
endoderm and the roof is formed of a median strip of chorda-mesoderm

with a strip or sheet of lateral mesoderm on each side. The completion
of gastrulation _ is marked by the withdrawal of the notochord and
mesoderm from the roof of the gastrocoel. The cells of the mesodermal
bands, being shortenthan those of the notochord or endoderm, cause the
bands to appear as grooves in transverse section (Fig. 53J5). As these
grooves deepen (Fig. 67) their edges come together. Thus a solid
notochordal rod is separated out in the mid-dorsal line, and the meso-
dermal pouches beciome more pronounced. Transverse constrictions
appear in the mesodermal pouches, which divide them into a series of
enterocoelic pouches. 'Finally, these pouches are constricted off from
the gastrocoel and l|)ecome the paired mesodermal somites (Fig. 68).
Meanwhile the endoderm which formed the floor and sides of the
g'astr-ocoel extends upward dorsally beneath the mesoderm and noto-
chord as they separaite out, thus forming new sides and a new roof.
The gastrocoel is now completely lined with endoderm for the first time
and constitutes the priniordium of the digestive tube.
96 G a s t r u l a t i o n ' a n d Neurulation
While these steps are in progress the beginning of differentiation of
the neural tube from the ectodermal neural plate has begun. This
constitutes the process of neurulation, which is considered in detail later.
Gastrulation in the Frog

The-gastrulation of the frog embryo has been interpreted in various
.ways by different investigators. The earher accounts were based on
the supposition that fhe embryo
passed through a two-layered
stage consisting of ectoderm
and endoderm and that later
the notochord and mesoderm
split off (delaminated) from
the endoderm. Vogt, after his
work on gastrulatioa in the
urodele amphibia' (1925), in
which he followed the move-
ments of the organ-forming
areas of the blastula by means
of vital dyes (Fig. 54)', studied
C D the gastrulation of an anuran
Fig. 54. Diagrams of the Triton egg show-
(Bombinator). Later Pasteels''
ing movement of surface areas stained with
Nile blue and neutral red during gastrula- (1937) confirmed these' results
tion. Areas on surface shown with sharp using another anuraji (Dis-
outline, those on interior without outhne. coglossus). yhe orga-n-form-
{After Vogt.) ing areas in the blastula of the
frog {Rana) and their subsequent migrations have, .not iyet,_ been
studied by the Vogt technique, In the account which follows it is
assumed that the • blastula has the same organ'-f orming' areas as
other anura {Bombinator and Discoglossus) and that the^mpyenients of
these areas are also essentially similar, ' -
In reading the following account of gastrulation,the illustratLons
should be carefully studied. Surface views of the embryo during gastru-
lation are shown in Fig. 45. Photographs of sagittal'sections-are
shown in Fig. 57. Interpretation of the surface views according to the'
findings of Vogt and Pasteels is presented in Fig. 55, and a similar
interpretation of the sections is given in Fig. 57. ' ' *
The fiilst stage in the gastrulation of the frog is the formation of a
crescentiq groove on what will later be the dorsal side of the embryo
in the region formerly occupied by the gray crescent (Fig. 45). The
location of the groove is 23° below the equator Of th^ blastula.- Aloiig
Gastrulation 97
this groove, cells are pushed into the interior (involution), while at the
same time the cells immediately above the groove are growing down
over the surface of the embryo to cover them (epiboly). In this way a
two-layered fold is produced at the dorsal lip of the blastopore
(Fig. 57).
Presumptive
epidermis
Presumptive
neural plate
Presumptive
notoehord
Prechordal plate
^— Dorsal lip
Presumptive Dorsal lip
endoderm Ventral lip
Presumptive
niesoderni
Neural plafe
Dorsal lip
B D
Fig. 55. Surface maps of stages in gastrulation of the frog. All from l^;ft side.
A, Dorsal lip stage (10). B, Lateral lip stage, midgastrula (11). C, Ventral lip
stage, late gastrula (12). D, Neurula, yolk plug stage (13). (Stages as listed in
, Chapter 8.)
. As the two-layered fold grows down over the cells of the vegetal
hemisphere, it' extends llaterally, thus forming the lateral lips of the
blastopore (Fig. 45). And, since the fold is covering a spherical sur-
face, its ends eventually meet to form the ventral lip (Figs. 45, 57).
Epiboly and involution take place at all points on the lip of the blasto-
pore, but chiefly at the dorsal lip, which moves approximately 65°
around the egg. At'this time the egg presents the appearance of a black
sphere with a small white circular area known as the yolk plug.
As a direct result of the fact that the small cells of the marginal
zone grow over the larger blastomeresand roll in at the dorsal lip, it
i's obvious that the^ must also converge toward the median line at the
dorsal Up', '^hich may be thought of as a bottleneck. Once inside the
bottleneck they tend to diverge from the median line. These move-
ments are illustrated in Fig. 56. To these four types of movement.
"98 Gastrulation and Neurulation
epiboly, involution, cdnvergonce, and divergence, must be added a fifth,
.elongation, or growth in length, which prevents a heaping of material
in the median line.
With these mass movements taking place dur.ing gastrulation, the
history of the organ-forming areas may now be followed. Just before
the appearance of the dorsal lip,
the area formerly occupied by the
gray crescent, or marginal zone,
is presumptive chorda-mesodferm,
with the notochord occupying the
median portion (Figs. o5A, 57A).
Below the marginal zone .is the
white presumptive endoderm with
its large yolk-laden cells. Just
below the presumptive _^nbtochord
is* a small area of endoderm which
will naturally undergo involution
before the notochord and is known,
from -its final location, as the pre-
chordal plate. Above the. marginal
zone is the ectoderm, from' which
the material later destined to form
the neural plate forms a crescent*"
immediately adjacent to the pre-
sumptive notochord.
When involutipn commences at
the dorsal lip of the blastopore, the
first material turned in will be-en-
dodermal (Figs. 5'5B,' 57.B}'' This
will form the anterior wa,ll and sides
of (he gastrocoel. The roof in the
Fig. 56. Diagrams to show direc- mid-line will be formed, by' the pre-
tion of cell movements during am- chordal plate. This will be fol-
phibian gastrulation. A, From lowed by the notochord in the mid-
posterior surface. B, From left side. line, with a wing-like extension of
Thick lines on exterior surface. Thin
lines on interior. (After Vogt.)
mesoderm on either side. As the
chorda-mesodermal crescent under-
goes involution, the presumptive neural plate will undergo fconvergenSe
and elongation as it moves toward the dorsal lip (epiboly). In this way
it will come to lie over the chorda-mesoderm (Figs. 55C, 57C). By
this timq the ventral lip of the blastopore has been formed, and the
gastrocoel is still a slit-like cavity. The huge ydlk-laden ceils of
presumptive endorterra, which appear externally as a large circular
Epidermis
oi ^ 1 '^J^t—Neural plate / ' ' .r"'

Blastocoel ):.\ /j s
Notochord \\- '' '
Prechordal plate ';,
• Dorsal lip
Mesoderm Endoderm
X
/ •
A . ^ \
• • • ' - • • : • - /
Gastrocoel
Dorsal lip
Ventral lip''^ Q
Blastopore
Pig. 57. Sagittal sections of frog embryos in gastrulation. A, Dorsal lip. B,

Latteral lip. ,C, Ventral lip. D, Neurula. X22.
S9
100 Gastrulation arid Neurulation
yolk plug, continue inward to form the floor of the gastrocoel. They
are in direct continuity with the smaller endodermal cells which were
the first to undergo involution.
The gastrocoel now expands at the expense of the blastoeoel (Fig.
57D), which is either pressed out of existence or merged with the
gastrocoel by the rupture of the thin-partition separating them.. The
yolk plug" has withdrawn into the interior as the lips of the blastopore
close together. This closing process commences at the dorsal side, and
the two lateral sides of the blastopore press together to form a short
slit (sometimes called the primitive streak). The blastopore closes
last of all at the ventral extremity of the slit. I t is claimed that in
some species of frogs the ventral portion of the slit remains open and
will later form the anus, but this is not the case with the Rana -pipiens
material studied by the authors. In the closing stages of ga«tfulation
the rearrangement of the heavy yolk-laden cells brings about a_rotation
of the gastrula, of approximately 80°, so that the blastopore is now at
the posterior end of the embryo (Fig. 55D).
During this period, the neural plate and notochord' are greatly
elongated. Mesoderm turned in at the ventral lip of the blastdpore
unites with that from dorsal and lateral Jips, but there is still a circular
area (mesodermal lacdna) in which ectoderm and endoderm are in
contact. Cells from the endodermal lateral walls of the gastrodoel are
growing upward, under the mesoderm, to form a new roof of endoderm,
but there is still a strip roofed only .by notochord. This is known as
the endodermal lacuna (dorsal lacuna, Dalcq and Gerard), which dis-
appears by the, continued upward growth of the endoderpi during-neuru-
lalion when final segregation of the mesoderm is completed (page 110).
Gastrulation in the Chick ' -^ ' .^

w Gastrulation in the chick embryo is accomplishe'd in two stages.
First the endoderm separates from the mesectoderm, and-.second,. a
primitive streak develops in association with which the chor'da-meso-"
derm cells move inward between the endoderm and ectoderm.
There has long been considerable difference of opinion as to the
precise manner in which the first stage of the process is acdomplished.
Ollacher's theory of delamination (1869) involved the splitting of th'e
blastoderm, which is several layers thick, into an upper surface layer
and a lower endodermal layer; Patterson (1909) explaine/i the process
as an involution (or rolling in) of cells along the posterior margin- of
the blastoderm as in the pigeon (Fig. 58A); and Pasteels (1937) sug-
gested a process of polyinvagination (Fig. 58B, C) whereby multiple,
localized invaginations of groups of cells from the surface layer pro-
duced an underlying sheet of endoderm. The last two explanations
Gastrulation 101
have now been largely abandoned, and at the present time there is a
reversion to OUacher's idea that endoderm is formed largely by a
process of delamination whereby cells separated from the surface layer
spread out below as part of the endoderm.
d.b.
''polyirivagination
Fig. -58. A, Sagittal section through early gastrula of pigeon (36 hours after fertili-
zation). Posterior half of section only, ih., Dorsal lip of blastopore. (From
Richards, after Patterson.) B arid C, Polyinvagination in the chick blastodisc.
B, Diagram to show area of polyinvagination. C, Section of unincubated blasto-
derm. (After Dalcq, from a preparation of Pasteels.)
Mesectoderm Endoderm Developing Yolk

(epiblast) (hypoblast) gastrocoel
..v.v;V;':v::;«:-.
Pig. 59. Diagrammatic llongitudinal section of chick blastoderm to illustrate
delarninatioii of yolk-laden endoderm cells and addition of more endoderm cells
by segregation from the epiblast to form a single layer of ectoderm cells. A,
Anterior end of blastoderm. B, Posterior end.
The beginning of the segregation of the upper mesectodermal layer

(or epiblast) *from the endodermal layer (or hypoblast) is marked by
the accumulation of large yolk-filled cells toward the lower surface of
the blastoderm. The cells of the upper surface are largely yolk free
•-and are aligned in .a layer 1 cell thick. Thus two distinct layers of cells
are present although they are still in contact. Delamination' o^the two
layers is probably brought about by the development and coalescence-
of scattered irregular slits between the two layers. Thus an endodermal
layer is separated off beneath the mesectoderm. In all probability it
spreads anteriorly by the addition of small groups of cells formed Irom
individual cells forced or squeezed out of the overlying layer. In addi-
tion, it appears that more endodermal cells are separated from the
thickened area where the primitive streak will be formed, and these are
added to those set aside by delamination (Spratt, 1946) (Fig. 59).
FIG. 60. Diagrams showing four stages in the process of primitive streak it)r-
mation by concrescence. (After Lillie.) / •", .
• - / f ••
DEVELOPIMENT OF THE PRIMITIVE STREAK. Before the presum{5tive
mesoderm is finally segregated from the, presumptive ectoderm of the
epihlast a linear thickening, the primitive streak, is forrqed on the sur-,
face of the blastoderm. Again, much uncertainty has existed, in regard
to -{he mode of origin of this structure.* Patterson attempted /to explain
it on the theory of concrescence (Fig. 60). The work of Spratt, how-
ever, has given reliable information concerning it. His method was
to mark the blastoderm with insoluble carbon black so that movements
of the cells and adhering particles could be followed. It thus' appears
that the primitive streak is formed by a posteromedial shiftitig or
crowding of the cells toward the mid-line so as to form a linear thickeft-
ing on the surface of the blastoderm (Fig. 61).
. Gastrulation 103
SEGBEGATION OF MESODERM AND ECTODERM. When the endoderm has
been segregated, the embryo is composed of the endoderm or hypoblast
(lower layer) and the mesectoderm or epiblast (upper layer). Pasteels,
Hoadley, Willier, and others have worked on the organ-forming areas
of the embryo at this stage and, although the accounts differ in minor
D E
Fig. 61. Diagrams iljustrating the formation of the primitive streak. A postero-
medial crowding of,cells toward the mid-line accompanies forward elongation of
•the primitive.streak. In the diagram, cells in large clear and dark, circles move
into the streak. {Modified jrom Spratt.)
details, the general organization of the embryo is fairly well agreed

upon. For this account!we shall use the original description of Pasteels
(19.37)', according to whom the greater part of the embryonic area is
composed of the ectoderm (Fig. 62^4). A crescentic region occupying
the posterior part of the ectodermal area' is the presumptive neural
plate. Immediately posterior to this is another crescent with the pre-
sumptive notookord inthe central portion. Posterior to the presump-
tive notochord comes the prechordal plate separating two wings of
presumptive mesoderm which will give rise to the somites. Behind this
104 Gastrulation and Neuru:^^^^^^
phe bands o'f presumptive
area on each side of the primitive Streak are f
lateral mesoderm.
Area opaca
-A Area peUutida
Presumptive
' epidermis
'resumptive _'
1 neural plate /
IPresumptivej
I notochord ;
Prechordal \
plate \
Presumptive
axial mesoderm
Presumptive _,'' Primitive
lateral mesoderm •' streak
Prechordal plate
Prechordal plate
Notochord
Endoderm
Lateral
mesoderm
C C
T-.- /.t^ 1.T r ii r • r ii chick embrvos foUowmg the
,Fig. 62. Map of the organ-iormmg areas oi the . , ", . . .
J. ... otr the
lormation ,, primitive
• ••• streak.
. 1 < r>
A, f
before • wation
mcuf . , and alter'. polymvagma-
, . , ,
,. n Au i. o u c • u i- /-ii iu t 15 hours ot iinoubation, Jeft
tion. B, About 8 hours of mcubation. Ci, Abou, r^., ,,' „ , ,
, ,, , ô c. i • U4- t, ij? 1 layer. £)i. About 24 hours of
half, upper layer. €•', oame stage, right halt, lower . , , ,v , , , •,,
u 4-- 1 j-4. t. ir 1 r.0 o i ,-ight halt, lower layer. (After
incubation, left half, upper layer. D'', bame stage, '
Pasteels, modified.)
At the anterior end of this streak, the w i n f .^^ ^ê neural and meso-,
dermal crescents turn toward the mid-line (^^S- 62B). Now the pre-
sumptive mesodermal material nearest the P ^ ' t i v e streak migrates
Gastrulation 105
downward through the region of the primitive streak and turns outward
between the surface layer and the lower layer of endoderm. At the
anterior end of the primitive streak, i.e., the primitive node, the pre-
chordal plate turns in first, followed by the notochord (formerly known
as the head process) Figs. 62D% 63). At the sides the lateral meso-
Primitive node Mesoderm Ectoderm Primitive streak
Fig. 63. Blastoderm of chick to show early stage in development of notochord.

A, Surface yiew at 20 hours {after Duval). B, Transverse section, left half only.
C, Sagittal section. {B, C, after Lillie.)
derm turns in first, followed by the axial mesoderm. The mesoderm of

the future tail bud turns in at the posterior end. During this process
the embryo elongates, arid the primitive streak seems to be drawn
toward the posterior end, with the result that the wings of neural plate
close together in front of it (Fig. 62D^). The embryo at this stage
may be compared with the neurula of the frog.
Gastrulation in Man
The mammalian blastocyst at the time of implantation consists of an
outer layer of trophoblast and an inner embryonic mass. No human
embryo in this, stage,of development has yet been described. In the
rhesus monkey, however, Streeter (1938) has shown that just prior
to implantation the embryonic mass consists of-three kinds of cells.
A thin layer of cells (Fig. MA) on the side of the mass away from its
point of attachment to the trophoblast represents the endoderm. Cer-
tain large cells are interpreted as "formative cells" which will give rise
to the rest of the embryo proper. Joining the trophoblast are smaller
"polar" (no'dal) cell^j, whose fate will be discussed in a later section
(page 142). ' '•'
The origin of the endoderm is still uncertain, some writers considering
that it originates by splitting (delamination), others that it originates
by certain cells wandering away from the lower surface of the embry-
onic massto.form the endodermal layer. In later stages the formative
Mesectoderm Polar
(Formative cells) trophoblast
Chorion
Trophoblast
Endoderm
Trophoblast
Amniotic
cavity
Mesectoderm
Endoderhi
"'^^^^^
Fig. 64. Early primate embryos during germ liLyerfonnation. .4, Monkey (8
days), before implantation, X370 (after i^treeter). B, Human (12 days), after
implantation, X200 (after Hertig and Rock). C, Human (1.5 days), X 130 (after
Brewer.)
P cells flatten out to form a layer of cells in contact with the underlying
endoderm. These two layers form the embryonic disc or shield. Above
the disc a space develops, the precursor of the amniotic cavity, to be
discussed in a later chapter (page 130).
The youngest human embryo yet described, Hertig-Rock'(1945), is
about. 7 days old (Fig. 65). The embryonic disc consists of a thick
layer, which may be considered embryonic mesectoderm,.and a thin
layer of endoderm. An amniotic cavity is present, and the trophoblast
consists of an outer syncytial layer, the plasmotrophoblast, ^nd an
inner cellular layer, the cytotroplioblast. Delicate cells grow into the
cavity of the blastocyst. These latter cells have been interpreted as ex-
traembryonic mesoderm. It is difficult to avoid the conclusion that the
trophoblast is a layer of extraembryonic ectoderm, precociously formed
during the process of implantation. Referring to the early gastrula of
the chick, the trophoblast may be compared to the area opaca, the em-
bryonic disc to the area pellucida. The endoderm cells migrate into the
cavity of the blastocyst, where they become arranged in the form of a
hollow vesicle which later becomes the yolk sac.
In later human embryos a primitive streak appears in the embryonic
disc, much as it does in the chick (Fig. 66^4). In this streak there is
Gastnilation 107
a well-marked primitive grou\x' terminating in a primitive pit at the
anterior end.. Just in front of the pit is the primitive (Hensen's) node.
In a longitudinal section (Fig. 66B) it can be seen that the primitive
node marks the point from which the notocliord, preceded by the pre-
•»<t>i
r"^'~
:*
Fig. 65. Section fhroush human embryo (Heitig-Rock. 7699) ju.st uftei- implanta-
tion. E.stimated age. 11 day.s. XIOO. (From Contributions to Embryology,
Vol. 29, Carnegie Institute of Washington, by permission.)
chordal plate, has grown forward. The notochord at this stage is

hollow with a prominent notochordal canal which opens to the exterior
by means of the primitive pit. In the days of phyiogenetic embryology
there was much argument as to whether this pit represented a persistent
blastopore or neurenteric canal. In any case it soon disappears through
the (.lisintegration of the cells which form its floor. The embryonic
mesoderm grows out from the sides of the primitive streak as in the
chick. With the backward growth of the primitive node, the length of
embryo is increased.
Although, for obvious reasons, the human embryo has not been
mapped with vital dyes, there is no reason to supjxise that the areas are
not similar to tliose described for the chick blastoderm.
L
NEURULATION
Even while the germ layers are being segregated, further differen-
ce^ tiation is taking place, the process being continuous. This is particu-
larly prominent in the ectoderm when formation of the neural tube
gets under way. To mark this stage the term neurula was .originally
applied to the amphibian embryo at the stage when the neural plate
Yolk sac
Fig. 66. Human fmbryo in primitive streak stage. A, Surface yiew. B, Sagittal
, section. X50. (After Heuser.) >
first becomes visible. Nowadays authors use the word neurulation as

a convenient expression to designate the period during which the neural
plate is transformed into the neural tube. This process takes place
by the formation of neural folds at the margin of the neural plate.
As the folds rise and arch over toward the hiid-line, a neural groove
develops between them. Finally the folds meet, converting the groove
Neurulation 109
into'a tube. The' inner layers of the folds fuse to form the lining of
the tube while the outer layers become the epidermal covering of the
dorsal surface. The cells where inner and outer layers were originally
continuous are cut off between the tube and its epidermal covering to
form a band of tissue known as the neural crest (Fig. 176).
Neurulation in the Amphioxus

During' gastrulation the area of the chorda-neural crescent nearer
the^b^stS pore was turned inward to form the notochord plate.
Anterior ,
neuropore^^
Level of B - t o
Fig. 67. Sections of amphioxas embryo (19 hours after fertilization). A, Para-
sagittal section. B, Transverse section. X166. (After Conklin.)
The cells of the chorda-neural crescent remaining on the exterior

of \he embryo give rise to the neural plate on the dorsal surface. A
longitudinal ridge arises On each side at the edge of this plate (Fig.
67) and grows- toward the mid-line to fuse over the neural plate
(Fig. 68). At the posteribr end of the embryo the folds unite with the
ventral lip of the blastopore, which here consists solely' of ectoderm.
In this way the neural plate comes to form the floor of a tube which is
open at the anterior end (anterior neuropore), and communicates with
the gastrocoel at tîei posterior end by a short passage (neurenteric
canal) (Fig. 67A). The.folds referred to correspond only to the outer
(epidermal) portionsiof'the neural tube in the frog and other verte-
brates, for the inner (Jneural) portions do.,not appear until a later stage
(Fig. 68B)u'
NOTE; With this section, our account of the early development of

amphioxus will be concluded, since in later development it diverges
widely from that of the vertebrates. It should be noted, however, that
no Gafetrulation and Neurulation
by this time the primordia of the gut, mesodermal structures, and
neural tube have already been differentiated.
Level of E-
Notochord
Fig. 68. Sections of amphioxus larva, (24% hours after fertilization)." .4, Frontal
section. B, Transverse section. X166. {Ajter Cohklin.)
Neurulation in the Frog

During this period the egg of Bana pipiens elongates until it is
approximately 2.5 to 2.7 mm. in length. Some of the epidermal cells
develop long cilia, by the aid of which the embryo rotates slowly
inside its envelopes of jelly. The neural plate (Fig. 69) forms typical
Neural plate Neural fjMs Rotation Neural tube Tail bud

."iO Hours 62 Hours 67 Hours 72 Houi-s 84 Hdure
Fig. 69. Neurulation in tlie frog embryo, X10. {From Shumway, Anat. ,Rec.
?8;143.)
folds which are more widely separated at the anterior end. The' folds
meet in the mid-line and finally fuse to form a neural tube. Jn the
head region, well forward on either side of the .neural plate, • is the
sense plate, from which the primordia of the nasal pit, lens of the eye,-
and inner ear will develop. Posterior and lateral to the sense plate is
Neurulatiou 111
the gill plate in connection with which the visceral grooves (furrows)
appear. The first is betjveen the sense plate and gill plate. The fifth
is posterior to the gill plate. At a later stage the second, third, and
fourth will appear, in the order named, on the gill plate itself.
While the neural folds are forming, two pigmented bands of ectoderm
on the ventral side of the head thicken to give rise to the oral suckers
(Lieberkind, 1937). These are adhesive, cement-forming glands by
means of which the einbryo attaches itself to the egg jelly or other
objects after hatching. Between these bands a longitudinal groove
foreshadows the stomodeum, which will invaginate at a later stage to
open into the fore-gut and form the mouth. The proctodeum, on the
other hand, is represented' by a pit which persists after the closing of
the blastopore and invaginates while the neural folds are closing. In
this way communication is established with the hind-gut to form the
cloacal aperture or vent.
Sections through embryos of the stages just described show that the
ectoderm has split into two layers, a thin outer epidermal layer and
an inner thicker nervous layer (Fig. 70A). The appearance of the
neural plate is due to the thickening of the nervous layer of the ecto-
derm, most marked in the region from which the neural crests will
form. A similar thickening of the nervous layer is seen in the sense
plate and gill plate. This nervous -layer of the, ectoderm moves toward
the mid-line from either side, heaping up to make the neural folds
(Fig. 70B). I t increases rapidly in thickness especially on the median
si"de of each fold, thus elevating the folds (Fig. 70C), causing them to
arch over, aiid eventually to fuse (Fig. 701)).
• SEGREGATION" OF THE MESODERM. The roof and sides of the gastrocoel
are first covered with chorda-mesoderm, the position of the notochord
being marked .by a median thickening (Fig. 70A). The wings of endo-
derm are seen growing upward underneath the mesoderm to form the
' new roof (Fig. 70B). In this stage they are separated only by the
lower portion of the notochordal band, which is still attached to the
mesoderm on-either side, and" now unites with the endoderm. This
lower part of the notochordal band (Fig. 70C) later loses its connection
with the remainder of the notochord, the mesoderm, and endoderm
and will become the Kypochprd, or subnotochordal rod (Fig. 70D).
This structure is found only in pmphibian embryos during early stages.
Both its evolutionary significance and function are unknown.
Neurulation in the Chick

The first indication of the formation of the neural plate (Fig. 71)
is seen in a thickening of the ectoderm in the mid-line of the area over-
lying the notochord a^nd in front of the primitive streak. Around the
Neurulation 113
anterior and lateral margins of this plate, the neural folds appear,
jBUch as in 'the frog except that no division of the ectoderm into
epidermal and nervous layers is apparent. At the end of the first day
Fig. 71. Diagrams to sliow embryonic and extraembryonic areas oJ chick embryo
at 24 hours- of• incubation. Above, surface view. Below, transverse section.
of'.incubation the neural folcls have come together on the dorsal side
of the head (Fig. 71).' The body of the chick is marked off from the
blastoderm by the outgrowth of the head, which becomes a fingev-like
projection above the blastoderm due to undercutting by the subcephalic
Notochor^
Epidermal laye^.
Nervous layer
Mesoderm
Endoderm
Neural folds
Notochord
Mesoderm
Endoderai
Notochord
•Hypochordal
plate
Mid-gut
Neural crest
Neural tube
Notochord
Hypochord
Mid-gut
Kg. 70; Transverse sections of frog errlbryoi

stage. B, Neu>al fold stage. C, Stage of roti, during neUrulatigri. A, Neui-ula
. . tube stage. Xa,tion, late neural f6ld. D, Neiiral
112 24.
114 • Gastrulation and Neurulation
pocket. As this undercutting works backward the sides of^the body
are clearly delimited by the lateral sulci, which are grooves undercut-
ting from the sides. In this manner the body is lifted from the general
level of the blastoderm but a tail fold does not appear imtil later.
The formation of a head fold involves both ectoderm and endoderm.
The endodermal pocket reaching into the head is the primordium of
the fore-gut, and its posterior opening is called the anterior intestinal
portal (Fig. 71). • ' •
The backward movement of the primitive node prolongs the noto-
chord toward the posterior end as it is growing forward at its anterior
end. Thus it comes to lie between the sheets of mesoderm.' In these
sheets transverse constrictions appear next to the notochord,. thus
cutting off somites, pair after pair, until the first six pair^ have been
formed at the end of the first 24 hours. Beyond the somite region
the mesoderm delaminates into an upper layer of somatic mesoderm
next fhe ectoderm and a lower layer of splanchnic mesoderm next the
endoderm. This split does not extend all the way to the somite^, leav-
ing a short strip of intermediate mesoderm )vhich is neither segmented
nor split. The segmented region corresponds to the epimere of the
frog, the intermediate zone to the mesomere, and the delaminated layer
to the hypomere. It is to be noted that the mesodermal wings at tlie
24-hour stage.have grown forward and united in front of the head,
leaving an area devoid of mesoderm, a region known as the proamnion.
Neurulation in Man
The embryonic disc of tlie human embryo corresponds to the area
pellucida of the chick. In it a head fold and neural folds form an a
mann'er essentially similar (Fig. 77A) to that in the chick, • A fore-gut
has also been formed from the endoderrh. The rn^soderm. develops
axial, intermediate,' and lateral regions, and, in the axial region, the
first six pairs of somites have been formed by the end of the third week
(Fig.77B).* . ' - • - • .
8
Embryonic Form and

Extraembryonic Membranes
While the germ layers are being segregated, the primordia of several
great organ systems which will develop from them are being localized.
Before proceeding to an account of the way in which the organ systems
develop from the different germ layers, a process known as organogeny,
we must examine the way in which the vertebrate body assumes its
form. This is found to be closely connected with certain structures,
the adnexa or extraembryonic membranes, which also develop from the
germ layers and play an important part in embryonic (and fetal)
life, but which are discarded before hatching or birth. These extra-
embryonic structures are the yolk sac, amnion, chorion, and allantois,
as well as a structure found only in rriammals, the placenta.
During the period of neurulation the gastrula is transformed into an
early embryo with th^ cylindrical shape characteristic of the verte-
brate body.
Growth in Length
There are in general two methods of growth by which the cylindrical
shape is attained. In the first, characteristic of small-yolked eggs with
a spherical gastrula; the
main factor is growth in
length, along the antero-
posterior (cephalocaudal)
axis. - In the second type,
which is characteristic of
large-yolked eggs,^the em-
bryo is modeled frorii a fiat ^ ^
disc into the fdrm of a Fig. 72. Diagrammatic transverse sections show-
cylinder cqnuected (with a iîg effects of yolk on form of embryo. A, Small-
great yolk sac by SOtne sort y^'êd embryo (frogK S, Large-yolked embryo
^c J . i . 1 , TVT u . (chick). (After Assheton.)
of pedestal or stalk. • Much
of this modeling is done by the out-growth of the head and the tail
respectively, especially among the anamniote vertebrates, but there
115
116 • Embryonic F o r m and Membranes
is also some actual undercutting, especially evident among the-Amniota.
This undercutting is accompanied by the formation of amniotic, folds,
as will be seen in the development of the chick. A diagram of cross-
sections through the body of a small-yolked embryo (Fig. 72A) and a
large-yolked embryo (Fig. 72B) will make clear the difference between
the cylindrical embryo and the plate-like embryo before it has been
remolded.
Metamerism
With growth in length is associated a second factor in the develop-
ment of the vertebrate body, namely, metamerism, or the addition of
serially repeated parts. This is first indicated by the appearapce of
metameres such as the enterocoels in the amphioxus or somites in the
true vertebrates. In later organogeny further evidences of metamerism
are found in the nervous, nephric, vascular, and other systems.' How-
ever, the primary metamerism of the body is shown in the mesoderm.
The somites are formed successively, commencing at the anterior end,
and therefore afford a basis of classifying the early eriibryos of any
species by the number of these units present.
Fore-gut Mid-gut . Fore-gut Mid-gut „. , ^

• Hind-gut \ 7 Hmd-gut,
r> 4. J • ^. , Proctodeum
Stomodemn Proctodeum Stomodemn
Fig. 73. \ Diagrammatic sagittal sections showing effects of yolk sn form of em-
bryo'. A, Small-yolked embryo (frog). B, Large-yolked eftibryo (•'chick).
General Plan of the Body - ^ • ' '

The bod^ of the vertebrate is basically a tube within a'tube, i.e., s\.
digestive tube within a body tube. /
T H E DI'GESTIVE TUBE. The gut of the embryo is endoderm^l in
origin and is derived from the gastrocoel. Embryos of small-yolked
forms have a tubular intestine from the begiftning. It is only pecessary
to form anterior and posterior openings, for the blastopore either closes
or is roofed in by the neural folds. The new openings arise from ecto-
dermal pits, the stomodeum at the anterior end, the proctodeum at the
posterior end (Fig. 73A). In general these openings are not completed
until after the yolk has been wholly consuilied. The gastrocoel of a
large-yolked embryo has only a 'roof and sides of endoderm, for the
Developmental Stages, Frog 117
floor is composed of the yolk. Hence the rolling in or undercutting of
the body first at the head end, and later at the tail end, forms a pocket
at each end, the fore-gut and hind-gut, respectively (Fig. 73B). The
mid-gut is the remainder of the open gastrocoel connected with the
developing yolk sac by means of the yolk stalk.
Between the two tubes lies the mesoderm. The ventral mesoderm of
small-yolked embryos (lateral of large-yolked forms) splits into so-
matic and splanchnic layers. The somatic mesoderm is closely applied
to the ectoderm to form the somatopleure; the splanchnic mesoderm is
associated with the endoderm to form the splanchnopleure. The space
between is the coelom or body cavity.
T H E HEAD. The vertebrate body is distinguished by a well-marked
head region at the anterior end, containing the mouth, visceral arches,
special sense organs (nose, eye, and ear), and the highly developed
brain. Herein the amphioxus differs from the vertebrates, for it has so
little head that some zoologists make a special group (Acraniata) to
contain it.
The anterior end ,of the body is the region where the neural folds first
arise and where they first meet. I t is the first part of the body to be
freed of the yolk in the large-yolked embryos. This region contains
the fore-gut," from which, among other structures, the pharynx and the
visceral clefts (often 'called the pharyngeal clefts or gill clefts) are
formed. • - •'
T H E TAIL. All vertebrate embryos, even those of species in which
the adult is tailless, e.g., frog, man, possess a tail in early stages. This
region is characterized by the absence of a digestive tube and coelom.'
The tail arises from a caudal bud appearing at the point where the
posterior ends of the neural folds fuse together immediately above the
region where the cloaca; will open. Here the cells are small, their divi-
sion is rapid, and the various structures appear suddenly, so that the
contributions of th^ several germ layers cannot well be distinguished.
• T H E APPENDAGE^.. The paired appendages-of vertebrates arise as
buds, which later develop into fins or limbs.
Developmental Stages, Frog

In Chapter 7, under the discussion of neurulation, the body form of
the early frog embrjyôis described. In .the following paragraphs will be
found a short sketch of the later development of the external embryonic
structures. These include "the primordia of the sense organs located
in the head, namely,' the nose, eye, and ear; and also the stomodeum
and proctodeum; the visceral clefts and arches; the limb buds; and the
tail. The serial developmental stages for R. pipiens are as follows
118 ' Embryonic F o r m and Membranes
(Figs. 45, 69, 74, 75), and all future references to stages are based on
this classification.
1. UnfertUized egg.
2. Fertilized egg (gray crescent).
3. Two-cell stage.
4. Four-cell stage.
5. Eight-cell stage.
6. Sixteen-ceU stage.
7. Thirty-two-cell stage.
8. Mid-cleavage stage.
9. Late cleavage stage.
10. Dorsal lip (early gastrula) stage.
11. Lateral lip (mid-gaitrula) stage.
12. Ventral lip (late gastrula) stage.
13. Neural plate (neurula) stage.
14. Neural fold stage.
15. Stage of rotation (late neural folds).
16. Neural tube stage. '.
17. Tail-bud stage.
18. Stage of muscular response (to mechanical stimulation).
19. Stage of heart beat (and gill buds).
20. Hatching stage (capillary circulation in first gill).
21. Stage of mouth opening (cornea of eye transparent).,
22. Stage of tail-fin circulation.
23. Opercular-fold stage.
24. Operculum over right gills.
25. Operculum complete.
EMBRYONIC FORM
Frog
On either side of'the head the optic vesicles, which are the prinjordia
of the eyes, push out from i h e brain and make well-marked bulges.
The ectoderm immediately external to 'each optic cup will' later give
rise to the lens of the eye. Anterior to each eye is' a depression in the
ectoderm, the nasal or olfactory pit. .These pits are the primordia of
the nose. Posterior to each eye a similar otic (auditory; acoustic) pit
originates as the primordium of the inner ear. On the ventral side"
folds of ectoderm rise to form the oral suckers. Between them there
appears an ectodermal pit called the stomodetim or primordium of the
mouth. On the ventral side of the body, just anterior to the base of the
tail, is a similar pit, the proctodeum, or primordium of the cloacal
opening.
On the sides of the head 5 dorsoventral grooves appear (in the order
STAGE NUMBEIR
AGE: IN HOURS AT 15° CENTIGRADE.
LENGTH I N MILLIMETERS
16 96
MUSCULAR RESPONSE.
Ilfi
ME.ART BE.AT
20 14C 6
GILL CIRCULATION HATCHING
21 /62
MOUTH OPEN CORNEA TRANSPARE.NT
22 192 a
TAIL FIN CIRCULATION
Fig. 74. Stages in development of frog after neurulation, X7y2, (from Shumway,
Anat. Rec, 78:145).
119
5TA6E NUMBER
AGE IN HOURS AT 16° CENTIGRADE
LENGTH I N MILLIMETERS
23 216
OPERCULAR FOLD TEETH
24240 10
OPERCULUM CLOSE.D ON RIOHT
25 \?m II
OPERCULUM COMPLETE.
Fig. 75. Stages in development of frog, coiltinued from Fig. 74, XIV^ ijrom
Shumway, Anat. Rec, 78; 147).
120
• PHARYNGEAL DERIVATIVES*
Pouches Grooves
Aortic (From
(From Arches Clefts
Arches ectoderm)
endoderm)
Visceral Aortic
arch I arch I
(mandibular)
Visceral Visceral Visceral
pouch I cleft I groove I
(hyoman- (spiracle of
dibular) elasmobranchs)
Visceral Aortic
arch II arch II
(hyoid)
pouch II cleft II groove I I
Visceral Aortic
^ arch. I l l ' arch III
(1st branqhial)
pouch I I I cleft III groove I I I
Visceral Aortic
arch IV- arch IV
(2nd branchial)
pouch IV S cleft IV groove IV
i Visceral Aortic
arch. V arch V
(3rd branchial)
Visceral t
Visceral Visceral
pouch V cleft V groove V
1
Visceral Aortic
arch VI arch VI
(4th branchial)
t
Visceral , Visceral Visceral

cleft VI
pouch VI •>-
• (vestigial in ,
' I, ' (lacking in
groove VI
(lacking in
1
frog) • frog) frog)
* The chart is arranged to show that viscera! arch I is foils wed by visceral cleft I;
visceral arch II, by visceral cleft II, etc. That is, the arches and clefts alternate.
Moreover, visceral cleft I is formed by the union and breakthrough of visceral
pouch I and visceral groove I, etc. The aortic arches flow through the corre-
sponding visceral arches, e.g. aortic arch I flows through visceral arch I.
121
122 Embryonic F o r m and Membranes
I, V, II, III, IV). These are the visceral or branchial grooves, some of
which will later break through into corresponding outpushings from the
fore-gut, called the visceral or pharyngeal pouches, to form the, visceral
clefts or gill slits (see chart p. 121). For the present we need simply
note that they separate 6 transverse bars or ridges, which are known as
the visceral arches. Arch I (the mandibular) contributes to the forma-
tion of the jaws. Arch II (the hyoid) contributes to the gill cover or
operculum and to the support of the tongue. Arches III, IV, and V are
often known as branchial arches 1, 2, and 3, respectively, and on these
are developed delicate filamentous outgrowths which become the exter-
nal gills or branchiae. Those developing on arch V are rudimentary.
Later thin opercular folds grow backward from arch II, covering the
external gills completely on the right side but leaving a srhall opening
on the left known as the opercular aperture. While this is taking-place
the grooves between arches II, III, IV, an^ V break through and join
the corresponding visceral pouches to form the visceral clefts. Internal
gills develop in the clefts, and the externa!îlls areresorbe^.' Mean-
time the mouth has opened and developed horny jaws.
The tail arises by the backward growth' o^ the'tissue"of the neural
folds (Bijtel) at the point where they unite oyer the blastopore. The
notochord and neural tube grow backward into the developing fail,
carrying epidermis and muscle-forming material with them. Thin
dorsal and ventral extensions arise on the tail to form the tail fin.
The paired limbs arise as limb buds. Although the posterior buds are
the first to make their appearance, the anterior buds arise first but are
concealed beneath the ogefBulum until the time of metamorphosis.
The one on the left side appears first, pushing through the opercular
aperture.
Chick ' ' .

, 1
The developmental stages of the chick are usua.Uy. expressed in

number of hours of incubation at I03°E. Heweve?, Lillie (1908)
pointed out the value of the somite number as an inde^ of development,
and this method of identification is frequently employed by modern
investigators (Fig. 7QA-D).
The head fold of the chick appears at the time of development of the
neural folds, and the head is lifted above the blastoderm at 24 hours of
incubation. At this time there are usually 6 pairs of somites.. On the
third day a posterior tail fold develops, accompanied by the-formation
of a subcaudal pocket. In the meantime, undercutting of the body
proper by lateral furrows paralleling .the long axis of thebody results
in elevation of the body of the embryo from the surrounding blastoderm
Embryonic Form 123
r^.^:§mm.
mi^s^mmm:!^;
•Sî^JlKig"."'''''
Fig. 76. Growth of the! chick embryo. A, 25 hours of incubation. B, 38 hours of

incubation. C, 48 hours of incubation. D, 68 hours of incubation. Compare
Figs. 217, 223; 229, 235. A, B, Approx. X9; C, D, approx. X4. (Ajter Duval.)
i
to which i£ is attached by a short pedestal, the umbilical stalk. The
head bend's down sharply at the cephalic flexure, but, pressing against
the yolk, it turns or twists toward the right, so that the left side of the
head rests on the yolk (Fig. 7&C, D). The ventral bend is known as a
flexure, the dextral t^x'ist is known as torsion. Flexure and torsion,
124 Embryonic Form and Membi'anes
which begin about the middle of the second day of incubation, continue
to progress in a caudal direction until, at the end of the fourth day,
the chick lies completely on its left s;de.
The primordia of the brain and sense organs arise much as they do in
the frog. A stomodeum .develops early in the third day of incubation,
and the proctodeum is formed during the fourth day. Four visceral
grooveSj arising in the order I, II, III, IV, and the 5 arches associated
with them, are formed between the end of the second and beginning'
of the fourth day of incubation. Only the first three clefts actually
open into the fore-gut, and they soon close again.
The tail originates from the backward growth of the tail bud, but it
never attains any great length.
The limb buds appear on the sides of the body during the third day
of incubation. The anterior limb buds are formed at, about the level
of the heart, and the posterior limb buds develop jûst in front of thg-tail.
A B Cv
Fig. 77. Growth of the human embryo. A, Neural folds (after, tngatls)'. B,
Neural tube commencing, 7 somites {after Payne). C, 10 somites {after Corner).
Man '
Students of human embryology distinguish three periods during intra-
uterine development: the period of the ovum, from fertilization to germ-
layer formation, which is about 2 weeks; the period of the erribryo from'
the time of germ-layer formation until the embryo has assumed a
definitely human appearance at the end of the second month;"and-the
period of the fetus, which lasts until "term" ,or the completion of
T h e Adnexa 125
development. It is the second of these periods with which we are
concerned.
By the end of the third week the head fold is formed, and at the fifth
the tail fold is developed, much as in the chick. Neural folds are
formed and unite to form the beginnings of the brain (Fig. 77). The
primordia of eye, ear, and nose also originate in a manner similar to
that in the chick. Five visceral grooves are formed, by the end of the
fifth week, separating 6 visceral arches; but, although the visceral
pouches appear and unite with the grooves, true visceral clefts are not
formed. By the end of the seventh week, the visceral grooves have
disappeared. A cephalic flexure appears in the fifth week. The neck
or cervical flexure develops in the week following and accelerates the
disappearance of the visceral grooves.
From the tail fold a tail is developed which is quite prominent during
the sixth and seventh week of development but is overgrown and
resorbed during the eighth.
Paired anterior and posterior limb buds make their appearance
toward the end of the fifth week.
THE ADNEXA
The Yolk Sac
Yolk sacs are found in the. development of all large-yolked eggs,
among both anamniotes and amniotes. As the name implies, this
structure is a larger or smaller bag protruding from the, body or
connected with it byâ yolk stalk*.
ORIGIN AND DEVELOPMENT. The yolk sac develops from the outer
margin 'of the blastoderm, which advances under the vitelline mem-
brane and around the yolk mass until the yolk is completely enclosed.
FUNCTION AND FATE. This sac contains the yolk, which, in mero-
blastic cleavage, is not diyided among the blastomeres. But it plays a
far more important part ih development than simply acting as a reser-
voir -for food reserves. It| is lined with endoderm just like that of the
intestine, and is' furnished ^yith arteries, veins, and capillaries, which
make up the area vasculdsa. The endodermal lining digests the yolk,
and the vitelline veins carry the digested food to the developing embyro.
We may think of the yolk sac as an extraembryonic intestine. I t is
interesting to note that (in some viviparous elasmobranchs, like the
dogfish, the yolk sac continues to be of use even after the yolk is con-
sumed. Pressed against the wall of the uterus it absorbs the uterine
"milk" secreted by the uterus and conveys it to the embryo through the
vitelline veins. A similar dfevice is seen among the marsupials (page
138). The yolk sac is usually drawn back into the body a^ the com-
pletion of development when tho'umbilicus closes, and the residue of
stored-up yolk which it contains is gradually used up while the yolk
sac is being resorbed.
The Disposition of the Yolk in the Frog

The frog has no yolk sac, for the yolk is divided among the large
blastomeres which later make up the floor of the intestine. The mass
of these cells, however, creates a bulge on the ventral surface of the
embryo (Fig. 74) which resembles externally a small sac.
The Yolk Sac of the Chick

The yolk sac of the chick is formed by the advancingêdge' of, the
blastoderrQT As we look down on the blastoderm of the chick at the
end of the first day of incubation, we can distinguish a series of con-
centric zones (Fig. 71). From the periphery inward, the firsl of these
is the area vitellina externa, consisting of the margin of overgrowth
and the zone of junction (page 91). Then comes the.area"-vitellina
interna, made up of two germ layers, the ectoderm and endoderm,
the endoderm closely applied to'the yolk. Finally, in the.center, is
the area vasculosa into which the mesoderm has already pushed, split-
ting, as it advances, into two layers: the somatic layer -(next to the
ectoderm) and the splanchnic layer (next to the endoderm). Between
the somatic and splanchnic layers lies the exocoel or extraembryonic
coelom, as the coelom is called where it extends beyond the boundaries
of the embryo. The blood vessels of the area vasculosa develop in
the splanchnic mesoderm. The exocoel separates-the splanchnopleure
(endoderm and splanchnic riaesoderm) from the soniatopleure (so-
matic mesoderm and ectoderm), so that in reality the'yolk sac- of the
chick consists' of splanchnopleure. By the end of 'the fourth' day of
incubation the yolk sac has grown dbwn completely around the yolk
except for a small area a t the vegetal pole, known "ias the yolk sac
umbilicus (Fig. 82C, D). When the chick hatches, t];i$'yollt sac, still
attached to the intestine, is drawn back into the coelom and, its contehts
are gradually used up. .
The Yolk Sac of Man and Other Mammals

In man, as in other mammals, the yolk sac arises during gastrula-
tion. The endoderm growing out from the lower surface of. the em-
bryonic knob apparently reorganizes itself, by splitting or migration,
to form a very small yolk sac (Fig^lSA). The roof of this sac becomes
the roof of the digestive tube when the gut is delimited in connection
T h e Adnexa 127
with the development of the head and tail fold (Fig. 78C). The
remainder of it constitutes the yolk sac proper. This sac is later
squeezed between the amnion and chorion (Fig. ISC, D), and loses
Allantois
•I'ronciosum
Fig. 78. Diagrams to show development of extraembryonib structures in human

embryo. Four stages illustrated by sagittal sections.- {After Corning.)
Rauber's cells
Embryonic
knob
-Trophoblast
Fig.' 79. Section of early bat embryo showing extension of endoderm beyond em-
bryonic knob (ajter Van Beneden).
its connection with ^he intestine through the degeneration of the yolk
stalk.
In other mammals (Kg. 79) the endoderm grows completely around
the interior of the trophoblast and forms a larger yolk sac. In the
rat, the embryonic knob hangs down.into the cavity of the blastocyst,
and is surrounded by the endoderm "which thus forms an external
covering (Fig. 80). This condition is known as entypy (endoderm
external to ectoderm). • In the guinea
pig the ventral wall of the yolk sac is
absent.
Among the marsupials, for example,
Placenta
in the oppossum [Didelphys), the yolk
sac sometimes presses against the cho-
rion, and hence indirectly against the
uterine wall. Its .area vasculosa par-
) Trophoblast ticipates in the placental exchange ajid
Endoderm \ serves to convey nutriment and'oxygen
from the blood vessels of the uterine
wall (Fig. 85). ^ '
Amniotic .»« •/
<^'''*y~u^f ^./ Amnion and Chorion
^^^^ Most of the anamniote v'ertebrates
lay their eggs in water to hatch and
Fig. 80. Section of embryo of
become larvae. In such a medium the •
white rat, to show entypy (after
Grosser). eggs are not susceptible to. violent
change^ in temperature, to desiccation,
or to mechanical injury. The tertiary egg envelopes in which they are
wrapped often protect them from being eaten. Among the amniotes,
however, the eggs either are laid under terrestrial conditions or are
retained within the body of the mother for a considerable period.
These eggs are protected by two membranes, kiaown as the amnion and
chorion, the chorion often being called the serosa or false amnion. • The
amnion or inner membrane is formed of somatopleure^ which is continu-
ous with the somatopleure oi tlie emhryo. I t contains anâmnioticfiuid
in which the embryo floats, attached by an umbilical stalk to iheyolk
sac. The chorion or outer membrane is likewise formed 06 spmato-
pleure. The cavity of the chorion is continuous with the coelom and
is therefore called the exocoel. The two membranes usually arise from
folds of somatopleure which unite on the dorsal side of the enabryo
(Fig. 81 A). The amnion and chorion are always associated in devel-
opment with another extraembryonic structure known as the allantois,
which will be described in a later section. • •• '
Amnion and Cliorion of the Chick • • -' '

In the chick the amnion is a thin sac of somatopleure completely
surrounding the embryo and continuous with the somatopleyre at the
T h e Adnexa 129
Allan tois
Allantois
Fig. 81. Diagrams to show development of extraembry-Q^jg structures Sag-

ittal sections. A, Amniotic folds. B, Folds united, allantois extending into
exocoel. C, Chorio-allantois. (After Kbi-y)
umbilical stalk. It surrounds an amniotic cavity JfiUed with amniotic

fluid. The chorion is a similar sac pressed against^thfe shell membrane
and connected with the amnion at the amniotic "^Skxih&r The process
of. amnion and chorion formation begins at about S^Q hours of incuba-
tion anterior to the head fold of the embryo in I\^Q region of the
blastoderm known as the proamnion (Fig. 217). 'This area which at
first contains no mesoderm and is made up solely of ectoderm develops
a crescentic thickening: which gradually extends ar.oyjj(} Q^ either side
in front of the head fold. This ridge-like thickening of \;^Q blastoderm
Is the forerunner of t t e head fold of the amnioij Mesoderm soon
grows into it so that iii is eventually composed of som'a.topleure. The
coelom on either side .of the head now enlarges torming the amnio-
cardiac vesicles (Fig. 220). This causes the ridge-like thickening of
somatopleure in frorjt of the head to rise up and begin to slip back
over the body of the p i b r y o . The inner layer of the amniotic fold
will form the amnion, land the outer layer will forijj the chorion. The
backward growth of the amniotic fold over the en^î-yo is assisted by
the downward bending of the head at the cepha^f^ flexure. Lateral
extensions of the amniotic fold give the structure the forin of an in-
verted U, the 'lateral extensions being known as the lateral folds of
the amnion. .
The tail fold of the amnion arises in the same manner as the head
fold at about 52 hours of incubation but quite independently, and at
the posterior end of the embryo just in front,of the primitive, node.
However, there is no area free from mesoderm in this region, similar
to the proamnion. Like the head fold of the amnion the tail fol(j
gradually advances over the body of the embryo extending laterally
as a U-shaped arch. Eventually the head and tail folds meet and
fuse, thus completing the f6rmation of the delicate arnnion and chorion
around the embryo. Soon after the amnion is complete, muscle fibers
arise in the wall of the amnion and initiate rhythmic contractions
which rock the embryo in the amniotic fluid and prevent adhesion to
the amniotic wall. The cavity of the chorion (exocoel) is. continuous
with the coelom as it is the space between the somatic and splanchnic
mesoderm. As the edge of the blastoderm grfcws down over the yolk,
the exocoel forms a great cavity separating the embryo, amnion, and
yolk sac from the shell membrane against which the chorion presses.
This cavity is interrupted only by the amniotic: raphe (Fig. 241),
where continuity with the amnion is preserved. Later the'exocoel is
obliterated by the ingrowth of the allantois (Fig. 82) .•
Meantime the lateral grooved or limiting sulci at th^ junction of
the embryo and amnion are undercutting beneath the body of the
embryo and approaching each other. The result is. that the somato-
pleure (of the amnion) crowds against the yolk stalk and, surround-
ing it, forms a short tube which is called the umbilical stalk.' For a
time there is a space within the umbilical stalk. between, its outer
wall of somatopleure and its inner, wall of splanchnopleure continuous
proximally with the embryonic coelom and di&tally with the exocoel.
This, is important in connection with the development of the
allantois.
In the chick it has been shown experimentally i h a t the cfells of the
proamnion 'and tail-fold'areas are necessary for the-development of
the amnion. Cautery of tlie tail-fold area does not prevent the forma-
tion of a complete amnion, but cautery of the proamnion is usually
followed by formation of an incomplete amnion. Destruction of both
areas results in an anamniote embryo.
Aihnion and Chorion in Man

In man the chorion is derived from the trophoblast^ which is devel-
oped precociously, consistent with its function of aiding the'implanta-
tion of the embryo in the uterine wall (Fig-. 65). After implantation
the trophoblast gives rise to the outer syncytial plasmofrophoderm,
which seems to be concerned with breaking down the surrounding
The Adnexa 131
Air
chamber Embryo
Shell
i membranes Amnion
Allantois
Umbilical
stalk
Fused,^/^
chorio-allaVitois
Chorion
Vitelline
membrane
Exocoel
Amnion
Amniotic
cavity
Allantois Allantoic
cavity
Chorio-
allantois
Yolk sac Yolk
Chorion Albumen sac
Yolk sac
umbilicus Albumen
D
1
Fig. 82. Diagrams of. extraembryonic structures in chick. Four stages illustrated
by transverse sections. (After Duval.)
maternal tissue, arid phe inner cellular cytotrophoderm, from which

the chorionic villi devfelop at a later stage.
The amniotic cavity arises, presumably, from the split in the em-
bryonic mass which \ye have already noted (page 106). This process
ha& been called cavitation" (Mossman, 1937). The floor of the cavity
gives rise to the mesectoderm of the embryonic disc, and the sides and
roof make up the ectodermal portion of the amnion (Fig. 64). The
mesodermal portion of the amnion comes from the somatic^mesoderin
of the embryonic shield growing out and around the ectodermal portion
In later development the amnion enlarges until it completely fills the
exocqel and fuses with the chorion (Fig. 78)'. . •
In many other mammals, such as the rabbit (Fig. 51), the embryonic
mass flattens out against the trophoblast to form the embryonic disc.
- Uterine wall -
Amniotic folds Trophoblast
Amniotic cavity
Fig. 83. Formation of amnion by folds in the rabbit. A, EaHy. B, Late.

{Ajter Mossman.) ' •. •
The trophoblast lying immediately over the disc (Rauber's layer)

degenerates so that the embryonic disc is temporarily exposed. Soon
thereafter amniotic folds (Fig. 83) appear much as in the chick but
completely encircling the 'blastodisc. The inner layer of the fold forms
the amnion, while the outer layer, which is continuous with the-tropho-
blast, forms the chorion. . ,• * , > -
Mossman "has described -methods of amnion formation intermediate
between fold formation and cavitation, and has suggested that fold
formation is characteristic of groups which have only A superficial
attachment between chorion and uterine endothelium, wheiftas cavita-
tion is found in those groups in which implantation is comparatively
deep.
The Allantois ,, '.

The development of an amnion and chorion is always accompanied
by the appearance of another sac, the allantois. This extraembryonic
structure develops as an evagination from the hind-gut and is tlierefore
lined with endoderm and covered with splanchnic megodern'i. It grows
The Aliantois 133
out through the exocoel of the umbihcal stalk into the exocoel of the
chorion, where it usually expands to occupy completely the cavity of
tJie exocoel. I t is filled with an allantoic fiuid, which receives the
nitrogenous wastes of the embryo in the form of uric acid (Needham)
and may be considered to function as an extraembryonic urinary
bladder. As it fills the chorion, its wall, being composed of splanchnic
mesoderm in the outer layer, easily fuses with the mesodermal layer
of the amnion, chorion, and yolk sac, whenever these structures come
together. Furthermore, it has an area vasculosa served by the allan-
toic or umbilical arteries and veins. This area vasculosa when applied
to the chorion is the region where the blood is nearest to a source of
atmospheric oxygen. Here an exchange of gases, carbon dioxide for
oxygen, takes place, and the aliantois may be considered as an extra-
embryonic lung.
In the cleidoic egg of reptiles, birds, and egg-laying mammals, the
aliantois also takes part in the formation of an albumen sac wherein
this material is digested. In the marsupials and placental mammals
it contributes to the formation of a placenta (hemiplacenta in
marsupials) whereby food is obtained from the maternal circulation.
These functions of the placenta are discussed in the sections following.
Aliantois of the Chick

Thfe aliantois (Fig. 84) arises toward the end of the third day as an
evagination from the floor of the hind-gut. It grows out between the
yolk and the wall of the siibcaudal pocket into the exocoel (Fig. 82).
Here it expands greatly until by the end of the ninth day it has filled
the entire exocoel. Its outer wall unites with the chorion (Fig. 82) to
form'a chorio-allantois; .its inner wall unites with the amnion above
and the yolk sac below.
The chorion, 'carrying with it an inner fold of aliantois, grows down
beyond the yolk-sac umbilicus (page 126), and around the mass of
albumen, which has been displaced toward the lower side of the egg
and has become more viscous through the loss of water. The albumen
is thus enclosed in a double-walled sac of chorion with the aliantois
squeezed between its two walls (Fig. 82). The layer next to the
albumen is the' ectoderm'of the chorion, but the mesoderm of the
aliantois supplies the bljood vessels. It is interesting to observe that it
is the ectoderm of the albumen sac which absorbs the albumen, whereas
m the yolk sac it is theêndoderm which carries on this function of food
absorption.
By the twelfth day of incubation the albumen sac is closed except
at the yolk-sac umbilicus, where it has an open connection with the
yolk- sac. By_the sixteenth day the albumen is consumed. On the
r

seventeenth the yolk-sac umbilicus closes by the constriction of a ring
of mesoderm derived from the old edge of the blastoderm.''The yol]j
Amnion
Embryo
Area
vasculosa
Allantois
Fig. 84. The embryo chick and its extraembryonic structures on the sixth day of
incubation, XIV2 (after Duval). , ' • '
sac with the remains of the albumen sac still attached is retracted into
the body cavity of the chick on the nineteenth 'day of incubation, aided
by contractions of the amnion and of the inner wall of the allantois.
Allantois of Man 1
In most of the mammals there is a well-developed -aUantdis, arising
like that of the chick, growing into the exocoel, anfl uniting with the
chorion to participate in the formation of the placenta, but the-primate
allantois is rudimentary."" I t arises as a minute tubular evagination
which develops from the endodermal roof of the gastrocoel, even before
the formation of the tail fold. It grows out into the body stalk (Fig.
78) for a short distance, but never gets as far as the chorion.. However,
the allantoic (umbilical) blood vessels continue down tihe-.'body stalk
to the chorion, where they form a chorionic area vascuiosa in the region
of the developing placenta. Bremer (1916) suggested that mammals
with a large allantois have large mesonephroi or fetal kidneys, (page
203), and a thick placenta, whereas those with a small allantois have
small mesonephroi and a thin placenta through which excretory
products can be discharged to the maternal, circulation.
The Reproductive Cycle
and Placenta of the Mammal
The development of the embryo of the mammals, with the exception
of the Prototheria, is coiriplicated by the fact thai the embryo is
retained within the body of the mother until it reaches a more or less
advanced stage of development. This necessitates the occurrence of
a series of changes in the reproductive tract of the female in prepara-
tion for the reception of the embryo. This phenomenon is called the
estrous cycle, or, in the primates, the menstrual cycle. Furthermore,
a very intimate relationship must be established between the mother
and the embryo to make possible metabolic exchange so that the fetus
may receive the necessary food and oxygen and eliminate its waste
products. This is accomplished by the development of a placenta,
which provides a very close connection between the rnother and the
embryo.
THE ESTROUS AND MENSTRUAL CYCLE

Before discussing the pl,acenta, the extraembryonic structure peculiar
to mammals, it is necessary to review the mammalian estrous cycle,
a phenomenoii intimately associated with ovulation and implantation.
The series of changes 'in the female reproductive tract concerned
with preparation of ^he 'uterine wall for implantation is a periodic
phenomenon among the mammals and is divided-into four stages. I t
commences with estrtis, the period of the sexual urge, which in most
mammals coincides wjith, the time of ovulation, and is the period in
which the lining of the uterine wall is thick, soft, and spongy owing
to changes in the capillary circulation and to proliferation in the
epithelial layer. If trie egg is fertilized after ovulation the uterine wall
takes part in the prpoess of implantation (page 138). If fertilization
does not take place the' innermost layer of the uterine lining is shed,
• sometimes accompanied by slight loss of blood. This stage, which is
of short duration, is known as the metestrum. Then follows a period
135
136 Reproductive Cycle and Placenta of M a m m a l s •
of rest and repair. In some mammals in which there areniany estrous
periods in the year this interval is of short duration and is called a
diestrum. In other cases where estrus takes place annually it is of
long duration and is called an anestrum. Before the next- estrus there
is a short period, known as the proestrum, during which the wall of
the uterus undergoes changes preparatory to implantation." The actual
length of the estrous cycle varies greatly in different mammalian
species. Thus it is of 4 days duration in the rat and mouse, 21 days in
the pig, and yearly in the deer. In general, the recurrence of breeding
periods follows a similar cyclic pattern.
It is interesting from the standpoint of the experimental embryolo-
gist who wishes to obtain embryos of known age that the phases of the
estrous cycle are also reflected in the condition of the vaginal epithe-
lium in many mammals. Hence, it is possible to determine the stage
of the estrous cycle, for a mature female, by using the so-called vaginal
smear technique in which cells scraped from the lining of the vagina
and spread on a microscope slide are studied with the microscope.
When this is done in the rat, for example, a characteristic picture is
seen for each stage of the estrous cycle,-as follows:
Proestrum—normal-nucleated epithelial cells.

Estrum—flattened, scale-like, cornified epithelial cells.
Metestrum—rounded or "balled" epithelial cells.
Diestrum—mucus and numerous leucocytes. .. •
Since these stages can be readily recognized in some forms such as
the rat, it is possible to determine the most likely time* of ovulation,
and matijigs may be arranged to produce embryo's of known age. •
The human cycle is known as the «ienstrual cycle bepause it is
almost monthly in its recurrence. I t varies considerably in individuals
and is easily affected by physical and emotional factors. In a general-
ized cycle of 28 days, four phases may be distinguished: (a) prolifera-
tion (days 7-15 after menstruation), during which the inner layer of
the uterus (endometrium) thickens; (5) secretion (days 16-28), during
which the glands of the uterus secrete a fluid rich in glycogen; (c)
menstruation (days 1-5), during which 'the proliferated layer is
sloughed off, accompanied by hemorrhages; (d) repair'' (days 5-6).
Formerly' we did not know whether there was any correspondence
between the stages of the estrous cycle and the. phases of the menstrual
cycle. If the two are compared it is at once evident that the phenome-
non of uterine desquamation which occurs during the metestrum is
remarkably similar to the changes that occur during menstruation.
This has been amply confirmed "by histological studies, so that a
definite parallelism can be seen in the two conditions, as shown below:
Implantation 137
Proestrum Proliferation
Estrum Secretion
Ovulation Ovulation (?)
Metestrum Menstruation
„. I Period of rest and repair
Diestrum J
It would seem probable in the light of modern information on the
subject that both the estrous and menstrual cycles are under hormonal
control. The ripening of the ovarian follicles is initiated by a hormone
j^nown as the follicle-stimulating hormone (F.S.H.) secreted by the
pituitary body. As the follicle matures it also produces a hormone
called estrin, which brings about proliferation of the uterine epithelium
and various other related changes. When the follicle reaches its maxi-
mum development the egg is discharged. After this has occurred the
cells of the empty follicle develop a new structure, the yellowish-
colored corpus luteum, which persists during pregnancy. This struc-
ture also has an endocrine function, and, under the control of the
luteinizing hormone; L.H., produced by the pituitary, it secretes the
hormone progestin, which is responsible for the maintenance of im-
plantation and the development of the mammary glands.
The current theory of the menstrual cycle may be stated substan-
tially as follows. F.S.H. stimulates the growth and ripening of the
Graafian follicle, which in turn produces the hormone estrin. This
hormone initiates the phase of proliferation in -the uterine wall. At
high concentrations estrin inhibits the secretion of FlS.H., thus per-
mitting the secretion of L.H. This results in ovulation and the forma-
tion of a'" corpus luteum which secretes progestin. This hormone
initiates the period of-secretion in the uterine wall. Unless fertilization
occurs the high concentration of progestin inhibits continuous secretion
of L.H. This is followed by degeneration of the corpus luteum and its
replacement by a white connective tissue scar, the corpus albicans.
As a result a new follicle begins to mature in the ovary, and the whole
cycle starts' over again. In the event that the egg is fertilized it
becomes implanted in the uterus and the menstrual cycle is inhibited
during pregnancy and for some time afterward. The corpus luteum,
maintained'now. by, placental hormones, persists for some time after
parturition. i,
IMPLANTATION
When the embryo reaches the uterus it is usually in the form of a
blastocyst, a hollow spherical vesicle composed of the trophoblast and
containingJthe embryonic knob (page 92). As it makes contact with
138 Reproductive Cycle and Placenta of M a m m a l s
some particular spot in the uterus it becomes closely associated with
the mucosa by a process known as implantation. In some cases, as in
the pig, the trophoblast merely conforms to the shape of the adjacent
mucosa, but in other cases such as the carnivores and primates a much
more intimate attachment is developed. This is brought about prima-
rily by the erosive activity of the outer layer of the trophoderm, and
possibly through enzyme action, as a result of which the mucosal cells
are destroyed and liquefied. Thereafter, in some forms, proliferative
activity on the part of the mucosa makes the attachment more secure
and the embryo may be even buried beneath the uterine surface. This
is the so-called decidual reaction.
The general relationship between the blastocyst and the wall of the
uterus at the time of implantation is illustrated in Figr 65.
Fig. 85. The extraembryonic structures of marsupials. Diagrammatic. ' A,

Didelphys. B, Perameles. {Ajter Jenkinson.)
JTIE PLACENTA ^
This structure has been defined (Mossman, 1937) ag an, apposition
or fusion of the fetal membranes to the uterine mucosa for physiologi-
cal interchange between the vascular systems of mother and-embryo.
The most external extraembryonic membrane of âminals is the
chorion, which in itself does not develop a -vascular area, and must
receive its blood vessels from some other source, either'the yolk sac
or the allantois. Accordingly, two main types of placentation are
distinguished: yolk*sac placentation, .and' allantoic placentation.
Among the marsupials, which~dD-Tioirdev'elop a true j3aceiTla7"a~lsub-
stance known as uterine milk is secreted by the uterine _ glands,
absorbed through the chorion and carried to the body of the embryo',
through the vascular system gf the yolk sac (Fig. 85), or the allantois,
' or. both. The human placenta is often described as chorionic because
The Placenta 139
o ca
O O P5
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-o "O , T3.
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"3 . 33
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fi -5
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the allantois is vestigial and never grows out to meet the chorion, but
the blood vessels of the allantois grow out from it and down the um-
bilical cord to vascularize the chorion where the placental attachment
Fig. 86.' Types of placentation in mammals. A, Diffuse, pig. B, Detail of A.

. C, Cotyledonary, sheep. D, Zonarv/dog. {From Arey.)
is developed. Mossman therefore Suggests that it should be designated

as a chorio-allantoic placenta. . ' ' '
The vascularized area of the chorion is distinguished by the presence
of villi. These are minute, finger-like outgrowths of the chorion,'which
Allantoic cavity
Exocoel
Pig. 87. Diagram of Extraembryonic structures in the pig {ajter Smith).
are provided with capillaries and either fit into depressions' of' the
uterine wall or penetrate more or less deeply into the maternal tissue.
Placentae provided with simple villi oi the'first type^ are 'known as
ihdeciduate, as exemplified by the pig- (Figs. 86, 87|, wh,ereas those
The Placenta 141
u'ith more elaborate villi which penetratp-tlfe uterine wall are known
og deciduate, as in the cat or man. \y^^
Types of placentae are also distinguished on the basis of shape.
That of man, for example, is discoidal, the cat, zonary; in the pig the
villi are scattered ove-r the surface of the chorion and the placenta is
Chorionic
'epithelium
Chorionic "- Uterine
epithelium
Uterine^
epitheliu^ Uterine
capillary
Uterine^,„-<^ - ^
capillary " "'
rhnrinnic g^ ^^®1
epithelium
Chorionic
epithehum
•Villus
Uterine,
capillary
Fig. 88. Sections through placentae of A, pig; B, cow; C, cat; and D, human
isemidiagrammatic, after Grosser). '
said to be diffuse. lÎuch more important, however, is the microscopic

structure of the placenta.
TKe simplest type! of villus-crypt relationship is found in the inde-
ciduate type' of placenta such as that of the pig. Here the crypts are
merely folds in the uterine wall, and the villi are corresponding ridges
which fit into the crypts. As shown in Fig. 88^1, the villus is made up
of a layer of chorionic êpithelium covering a core of mesodermal tissue
in which the embryonic blood vessels are distributed. The crypts, in
a similar manner, are composed of the uterine epithelium, and a core
of connective tissue in which the maternal blood vessels are found.
?

Thus, counting the endothelium of the blood vessels in each casp, there
is a series of 3 tissues on the embryonic side and 3 on the maternal
side separating the two blood streams, as shown in the accompanying
table based on Mossman's classification. As can be seen, five types
of placentae may be recognized, based on the intimacy of connection
between maternal and fetal tissues and culminating in the hemoendothe-
lial type found in the rat. In this type the embryonic blood is sepa-
rated from the maternal only by the endothelial wall of the fetal
capillaries. I t must be recognized that the progressive increase in
intimacy is brought about largely through the erosive action of the
blastocyst on the maternal tissue during implantation. This is well
illustrated in Fig. 8SA-D.
Development of the Human Placenta

It will be recalled that ovulation takes place in the human species
on the average of once every 28 days. The egg is fertilized, if sperm
are present, near the opening or ostium of the oviducal tube.-- The
fertilized egg usually spends three days (Hartman) in the tube, and
then, pushed by muscular contractions and possibly ciliary action, it
moves on to the uterus. During this time cleavage takes place, so that
the egg is probably in the morula stage on entering the uterus. In the
uterus it spends about a week free or loosely attached to the utefine'
wall. During this time it becomes a blastocyst and loses the zona
pellucida. About the ninth or tenth day it is implanted in the uterine
wall, which is now ready to receive it. . -.
At this time the polar cells undergo rapid proliferation,-producing
an outer syncytial layer, the pJasmotrophoderm, and an inner cellular
layer, the cytotrophoderm. The syncytial layer actively erodes the
surrounding maternal tissue, thus embedding the embryo-more deeply
and producing a liquid cellular debris called embryotroph, which serves
as food for the embryo. The attachment of the embryo J s further
aided by proliferative activity on the, part of the adjacent uterine
mucosa, which grows over the implanting ovum in the sorcalled decidual
reaction. Soon thereafter projections grow out from the cytbtropho-
blast of the'chorion to become villi. Through erosive action on the
uterine' blood vessels the villi are bathed in maternal blo.ijd, which' is
brought into the inteflvillous spaces'and, carried away by the uterine
capillaries. Only those villi which are in contact with the decidua
basalis (Fig. 89) persist; the others degeiierate, thus differentiating
the chorion into two areas, the chorion frondosum, which is provided
with villi, and the chorion laeve, which .is devoid of them.
The placenta is non-allantoic. I t will be recalled that th^ embryonic
T h e Placenta 143
knob retains its connection with the trophoblast as the body stalk.
Into the body stalk grows the small evagination from the hind-gut
Fig. 89. Diagram to show the uterine deciduae (human) (after Kollmann).
Allantoic cavity
Exocoel
Embryo
Pig. 90.' Diagram of extraembryonic structures in man {ajler KoUiker).
which represents the endodermal lining of the allantois. It never

comes in contact with the trophoblast and soon degenerates. The
limiting sulci of the amnion approach each other, and the-apinion
closes in around the body stalk and its associated structures to form the
umbilical cord. The latter contains (Fig. 90) the body stalk, yolk
Amnion
Yolk sac
Chorion
Villi
Decidua
basaiis
Decidua
vera and
capsularis
(fused)
Fig, 91. Diagram of fetus (near term) to show relationships of fetraembryonic

structures and deciduae (after Ahlfeld). ,'.
stalk, allantoic stalk, as.well as .the umbilical, arteries and 'umbilical

I veins which grow out frofn the body of the embryo toward'the tropho-
blast. These umbilical blood vessels represent the allantoic vessels of
all other amniotes. I ' •' '
T H E DEcmuAE. I t will be remembered that the blastocyst burrows
into the uterine wall, eroding epithelium, connective tissue, and blood
vessels.- As the embryo increases in,size, this erosion continues and
Parturition 145
the embryo sinks into the compact layer of the mucosa and comes in
contact with the spongy layer. The mucosa grows around the bur-
rowing embryo, shutting it off from the cavity of the uterus. There
may now be distinguished (Fig. 89) three regions in the mucosa: (1)
the decidua basalis, to which the blastocyst is attached; (2) the
decidua capsularis, which covers the blastocyst thus cutting it off from
the uterine cavity; and (3) the decidua vera, which includes the re-
mainder of the uterine lining with which the decidua capsularis has
fused, thus obliterating the uterine cavity (Fig. 91).
PARTURITION
The history of the extraembryonic structures, as well as that of the
deciduae, is terminated at birth or parturition. This occurs in man
about 280 days after fertilization. At this time a series of rhythmic
muscular contractions begin in the uterus, the cervix is dilated, and
the embryo is finally expelled. Shortly afterward the placenta, carry-
ing with-it the decidua basalis, and.the attached membranes repre-
senting the fused amnion, chorion laeve, decidua capsularis, and
decidua vera are cast off- as the caul, or "afterbirth."
10
Experimental Embryology
The great progress in vertebrate embryology has resulted so largely
from the application of experimental methods that some of the tech-
niques used and the results obtained must be reviewed. Within the
limits of this book only a few of the important fields of experimental
embryology can be mentioned, and the. student must be referred to
more extended treatises for further information concerning this rela-
tively new and important branch of embryology. '
The amphioxus and the frog have long been used by experimental
embryologists, and successful methods have been devised for the ex-
perimental study of the developing egg of the hen. Triton, in Ger-
many, and Ambystoma, in this country, are urodele amphibia whose
eggs have been particularly favorable for experimental embryology.
The eggs of mammals, difficult to obtain, and, so far, impossible to
orient during the early stages of embryogeny, have been employed to
a lesser extent. •"
The experimental embryologist alters the conditions under which
the egg develops in the hope of determining the factors involved iii
particular' developmental processes. It is appropriate to conclude .the
study of early embryology with a short account of some of the experi-
ments which bear directly on intrinsic factors includiilg-fertilization,
differentiation during cleavage, formation of the germ layers, and
neurulation, as well as extrinsic factors such as the direcjt effects of
environmental Influences up~bn development. • • ' . .
EXPERIMENTAL ASPECTS OF THE PROCESS OF FERTILIZATION

* «
The fertilized 6gg, as has been seen, is the product of the union of
two germ cells, the egg and the sperm. It contains two pronuclei, of
maternal and paternal originTrespectively, as well as a mass of cyto-
plasm which is almost exclusively maternal in origin. The riuclei
contain the parental contributions of genes, the units.which together
determine the hereditary characters of the developing individual.
146
Experimental Aspects of Fertilization 147
How the genes produce their effects is not known, but it is certain that
they must act directly upon the cjrtoplasm.
Artificial Parthenogenesis
In spite of the fact that parthenogenesis does not normally occur in
the vertebrates, successful attempts have been made to induce develop-
ment artificially in a number of cases. One of the earliest workers in
this field was Loeb, who carried out extensive experiments on echino-
derm eggs as well as on frog eggs. With echinoderm eggs he found that
a number of methods were successful in initiating development. Thus,
if the unfertilized eggs were immersed briefly in hypotonic solutions
of various salts and sugars, fatty acids, or fat solvents and then
washed and returned to fresh sea water, development could be started.
In the frog.it was found that pricking the egg with a glass needle
dipped in frog plasma was sufficient to start development. Eggs
treated in this manner passed through the early stages of cleavage and
gastrulation and in a few cases tadpoles and even adult frogs were
obtained. Similar experiments have been carried out by Parmenter
(1940), who induced development by smearing the eggs with frog's
blood and then pricking them with a fine needle. Of 619 eggs used in
these experiments 546 formed the second polar body, 63 underwent
cleavage, and 4 developed to the tadpole stage. ''
Artificial parthenogenesis has also been accomplished in the lamprey
and in the rabbit egg. Pincus reports the birth of a normal living
female rabbit from an egg activated by low temperature. It would
be expected that such embryos would possess the haploid number of
chromosomes.' Actually haploid, diploid, and even triploid embryos
are produced. Apparently the first cleavage division is delayed while
the chromosome number is doubled by a nuclear division. I t is sug-
gested that triploid embryos result from the extrusion of but 1 of the
4 nuclei formed in ineiosis while the remaining 3 unite into 1. The '
fact that males, females, and hermaphroditic individuals are formed
suggests that the diploid individuals are genetic females some of which
undergo sex reversal.
Rolie of the Pronuclei in Cleavage

The f&ct that thq.fertilized egg has the diploid number of chromo-
somes and of genes,' whereas the 2 gametes have the haploid number,
naturally leads to the question whether the diploid number is necessary
to continued development. I t has already been seen that experiments
on artificial parthenogenesis indicate that the sperm nucleus is un-
148 Experimental Embryology
necessary to initiate development. Experiments bearing on otlfer
aspects of this question must also be considered.
Gynogenesis
Sperm of the amphibian Triton, treated with an appropriate dosage
of radium emanations, have their nuclei injured in such a way ihat
they are unable to form normal pronuclei (Hertwig). But they retain
their mobility and are able to penetrate the egg and induce develop-
ment. The sperm head remains in the cytoplasm and passes to one
or another of the developing blastomeres, but takes no part in mitosis
and ultimately degenerates. The number of chromosomes in the
larval cells is usually haploid, although redoubling may occur. The
development of a new individual from a nucleus exclusively maternal
is known as gynogenesis.
Androgenesis
On the other hand, haploid individuals may be produced with a
paternal ûcleus only. This is known as androgenesis. Eggs of
Triton have also been, irradiated to inactivate the egg nucleus and then
fertilized with norrrial sperifl., .These eggs develop with the haploid
number of chromosomes, showing that either maternal or paternal
pronucleus is adequate for development.
Merogony
This term is applied to the development of individuals from enucleate
fragments of eggs which have been fertilized by normal sperin. A
similar result can be obtained in telolecithal vertebrate eggs, such as
those of Triton, where several sperm normally enter the egg. After
the entrance of the sperm, it is possible to constrict the egg înto
halves, by means of a fine hair loop, in such a way that,the female pro-
nucleus lies in one half (Fig. 92). This half will eventually have the
diploid number of chrbmosomes, for a sperm pronucleus will conjugate
with the egg pronucleus. The other half will have only fee haploid
• number. Both halves will develop into larvae, one qf which will have
haploid and the other diploid nuclei.
Partlienogenetic Development of Enucleate £ g g Fractions

By use of a high-speed centrifuge Harvey (1937) was able to divide
Arbacia eggs into various fractions, some of which were enucleate.
After exposure to hypertonic salt solutions some of the enucleate frac-
tions began to undergo parthqnogenetic development but ,did not suc-
ceed in advancing beyond thq blastula stage. This would appear to
Egg nucleus
Fig. 92. The experimental production of haploid larvae in Triton. A, Fertilized

egg with 2 sperm nuclei. B, Same, after constriction separating part of egg with
diploid nucleus (right) from part with haploid nucleus formed by supernumerary
sperm (left). C, Relatively more advanced diploid embryo (right) and less ad-
vanced haploid embryo (left). D, Diploid larva. E, Haploid larva. {After
Spemann.)
indicate that differentiation beyond the blastula stage is under nuclear

control. • i
The Equivalence of the Pronuclei

The experiments mentioned above indicate that a single set of genes,
paternal or maternal; is adequate for the development of an egg,
although development may be started in the absence of both nuclei.
It must be recognized, however, that the experimental haploid animals
are frequently less vigorous than normal diploid forms.
Species Hybrids
Many experiments have been performed in attempts to fertilize the
egg of one species with a sperm from another species. Often, as in the
teleost fish (Moenkhaus), both pronuclei take part in the subsequent
cleavage, although frequently the chromosomes from the two pro-
nuclei (Fig. 93) form separate groups on the mitotic spindle, a phe-
nomenon known as gonomery. But in other cases Hertwig has shown
that the male pronucleus takes no part in subsequent
cleavages, so that the embryo really develops par-
thenogenetically by gynogenesis.
di 9
m\ Natural interspecific hybrids in both plant and ani-
mal kingdoms are more common than was formerly
believed. Usually these interspecific hybrids, such
as the mule and many types of hybrid bony fish, ar«
infertile, hut they often grow to larger size and aj'e
more active than the parents and are said to show
^ \ /? hybrid vigor.
Organization of the, Cytoplasm

I t is mentioned in Chapter 4 that the fertilized egg
Fig. 93. Chromo-
somes in anaphase of many animals had markings such as the yellow
of iirst' cleavage of crescent of the ascidian and the gray crescent of the
a hybrid fish, Meni- amphibian. These particular areas lie on the surface
dia egg and Fiin- or crust of the egg (cortex, ectoplasm). When stud-
dultls sperm, illus- ied by the methods of descriptive embryology, includ-
trating gonomery
(after Moenkhaus). ing the use of vital stains, the prospective fate of
these areas was established. Similarly,'in the egg of
the echinoderm, the use of the dark-field microscope has shown that the
area surrounding the vegetal pole appeared in a different color-frqm.
that of the aniipal pole. Experiments showed that these areas gave rise
to endoderm and ectoderm respectively. Ectodermalizartion or- endo-'
dermalization could be augmented'by removing parts of the egg from
the appropriate regions or by using chemicals which produced jihe same
effects. Although the factors located in these areas are as yet un- •
known, the word "field" is applied to the organizatioTi comprising
these organizing factor^.- The area possessing such a field is referred
to as a "field district." . ' ''
POLARITY. The primary expression of the egg's organization is the
polarity already impressed• upon it in the ovary (page 33),. That
this polarity is itself not due to gravity is shown by the fact that
frog eggs which are kept in motion during early development give
rise to normal embryos (Morgan, Kathariner), But polarity i^ not
immutable, for many experiments in which the eggs of frogs have
been made to develop in an inverted position (Born, Pfliiger, Morgan)
gliow that the yolk streams down through the egg, and cleavage begins
in the relatively yolk-free region which was formerly the vegetal
pole. There seems to be good reason to suppose that the polar axis
represents a metabolic axial gradient (Child), for when dilute solu-
tions of lethal chemicals, e.g., potassium cyanide, are applied to the
frog's egg (Bellamy), disintegration begins at the animal pole and
continues toward the vegetal pole, which is the last part of the egg
to be affected.
BiLATEBALiTY. The animal pole marks the.anterior end of the de-
veloping amphibian embryo. Its dorsal side is marked by the gray
crescent. , The gray crescent often, but not always, appears on the
side of the egg opposite the point where the sperm entered. In uro-
deles, in fact, the gray crescent makes its appearance prior to the
entrance of the sperm. And in parthenogenetic eggs (when develop-
ment is initiated by puncture) the point of entrance oJ the needle
seems to have no constant relation to the subsequent bilaterality of
the egg.. This would indicate (Huxley and de Beer) that the egg has
an underlying bilaterality of its own.
ASYMMETRY. The vertebrate embryo is not, strictly speaking, bi-
laterally symmetrical. A third axis or gradient from one side to the
other (usually left to right) is often apparent, as seen in the develop-
ment of the opercular opening on the left side of the pharyngeal region
of the tadpole, the fact that the chick heart develops on the right side,
and that the head turns to the right in torsion. The stomach in all
vertebrates is twisted to" the left of the mid-line, and many other
examples might be mentioned.. When this asymmetry is reversed, the
phenomenon known as situs inversus is established, and this condition
can be reproduced experimentally. For example, it has been shown
by Spemann that, when 2 blastomeres which would ordinarily produce
the right and left sides of: ^n embryo are separated by a hair loop, the
left-hand blastomere gives rise to an asymmetrical embryo, while the
right-haad blastomere gives 'rise cither to an asymmetrical embryo or
to one.showingsitus inversus.
These few examples of experiments on the fertilized egg indicate
that the egg is a complex isystem with a definite organization indicated
by its three axial gradients corresponding t6 its three spatial dimen-
sions, viz., ari anteroposterior gradient corresponding to the direction
of the polar axis, a dorsoventral gradient, and frequently a left-right
gradient,
ORGANIZATION OF THE EMBRYO DURING CLEAVAGE

Cell-lineage studies seemed to indicate that the dividing egg becomes
a mosaic of blastomeres, each set apart from the others to form a
specific portion of the embryo. Roux (1888) was the first to reahze
that this might be tested experimentally. He destroyed one of the
V2-blastomeres of the frog's egg and observed that the remaining
blastomere gave rise to a i/^-embryo, thus apparently confirming the
mosaic concept. Then in 1891 Dreisch showed that in the sea urchin
a complete larva could be obtained from a single blastomere. This
led him to introduce the term "prospective significance" to .indicate
that the actual fate of any part of the original egg is only one of a
number of possible fates or prospective potencies. The egg may,
therefore, be said to be pluripotent.
Later investigators devised a number of methods by which blasto-
meres could be separated from each other, by shaking themf cutting
them apart with fine needles, constricting them with fine threads, or
placing them in artificial calcium-free sea w;ater. Blastomeres of
marine eggs in this medium separate immediately, and when returned
to normal sea water continue their deyelopment without 'further
separation (Herbst).
Regulation and Mosaic Eggs

The results of these and many other experiments seemed to indicate
• that in some eggs, e.g., those of the amphioxus (Fig. 94), either of the
-|/2-blastomeres might, when separated, give rise to complete embryos
(Wilson).' These were called regulation eggs and .were said to have
indeterminate cleavage. In others, such as Styela (Conklin) or the
mollusc Dentalium (Wilson), the %-blastomeres give'.rise only to
%-embryos (Fig. 94). These were called mosaic eggs and were said
to have determinate cleavage. . ' ' • '.
Experiments on frog's eg^s had been inconclusive until Improved
technique made it possible to separate blastomeres of J,he 2-c6ll stage
completely (Schmidt, 1930, 1933).' These experiments show that each
of the %-blastomeres can give rise tb a complete and perfect larva,
provided only that it contains some of the gray crescent region. If,
on the other hand, th.e egg is so constricted'that tlie first cleavage
divides it into an animal and a vegetal half, the a'nimal half, contain-
ing the gray crescent, gives rise to a complete embryo, while the. vegetal
half, lacking this region, is unable so to organize itself (Fig. 95). This
s'eems to indicate thaf Roux's results may have been due to the presence
of the injured blastomer? inhibiting complete development on the
Organization of the Embryo during Cleavage 153
part of the uninjured blastomere. In this connection it is interesting
to note that Witschi (1927) has described a case in which 2 eggs were
found in a single chorion. Each of them was flattened on the side next
to its neighbor and in later development showed deficiencies in the
corresponding region.
Fig. 94. Diagram to shovV the fate of isolated blastomeres from mosaic and regu-
lation eggs. A, Mosaic egg of Denlalium. At left, a complete embryo produced
by entire egg: at right, partial embryos produced by the %-blastomeres when
artificially separated. B, Regulation egg of Amphioxus. At left, embryo pro-
duced by entire egg; at right) perfect dwarf embryos produced by %-blastomeres.
' , (After Wilson.)
A beautiful demonstration that the cytoplasmT and not the nucleus

is concerned with differentiation during cleavage is afforded by an
instructive- experiment of Spemann. If the egg is tied off before
cleavage so that the nucleus is confined in one of its halves (Fig. 96),
all cleavage planes will be restricted to that half until eventually a
cleavage plane, in this case at the fourth cleavage, coincides with the
plane of constriction.' 'The nucleus which enters the previously enu-
cleate half is naturally orie which would serve a ^g-blastomere. If the
loop is now tightened ûntil the two halves are completely separated,
the portion containing this single nucleus will give rise to an embryo
^-
tM
1 «9
Fig. 95. Embryos arising from separated %-blastom_eres of the newt's egg. A, The
ligature separates the dorsal and ventral halves of the embryo. " B, The ligature
separates the right and left halves. C, Perfect embryo arising from dorsal
%-blastomere. D, Mass of cells arising from ventral Mi-blastomere.' E, Two
perfect embryos arising from right and left %-blastomercs. (-^jter Spe'mann.)
• 154 . '
Organization of the Embryo during Cleavage 155
like the one from the portion containing the 15 nuclei and exactly like
one arising from a complete fertilized egg.
PRESSURE EXPERIMENTS. Further examples of the regulative power
of some eggs may be seen in pressure experiments. If eggs of the frog
are placed between glass plates during cleavage, the third cleavage
Fig. 96. Experiment demonstrating equality of nuclei formed during cleavage

(Triton). A, ligature has ,been tied around the fertilized egg restricting the
nucleus to the right-hand portion. A, 16-cell stage, 1 nucleus passing into left-
hand portion. B, Ligature tightened to separate the two portions. C, Perfect
embryos formed by the separate portions. The nucleus of a ê-blastomere is
equivalent to that of a complete zygote. (After Spemann.)
i
plane will be meridional instead of latitudinal, and the fourth cleavage
plane is latitudinal (Fig. 97). Now if the eggs are released, their later
development 'will \\e quite normal even though the blastomeres are
occupying positions unlike those which they hold ordinarily.
DOUBLE EMBYROS. I Still another exaniple may be seen in the eggs
of Triton. If these are; freed from the egg envelopes, the blastomeres
at the 2-cell stage assuiiie a dumbbell shape. Mangold discovered
that,, by placing one embryo in the 2-cell stage over another (Fig. 98),
a double embryo resulted almost exactly, a m y a u i o ^ ^ i ^ q j j e p i b r j i o
in the 4-cell stage and would develop as such, provided only that the
gray crescent regions of the two fell in the same plane. Otherwise
double monsters resulted.
D C
3 c
B D
Fig. 97. Diagram to show new relationship of blastomeres in frog's egg resulting
from pressure during cleavage. A, Normal 8-cell stage. B, .8-cell stage formed
under pressure. C, Normal 16-cell stage. D, 16-cell stage formed under pressure.
Cells normally in animal hemisphere shown in'stipple. (Suggested by'a diagram
in Welh, Huxley, and Welh.)
Fig. 98. iJouble embryo arising from fusion of 2-cell stages of' Triton, alpestris
(above and below) and Triton taeniatus (right and left) when laid ov'er each other
crosswise. Note that a new cleavage is under way in -all blastomeres. {After
Mangold and Seidel.)
MONOVULAR TWINS AND MONSTERS. The extreme plasticity of the

vertebrate egg as seen by the fact that either two separate individuals
or duplicate monsters may be formed from the complete- or partial
Organization of the E m b r y o during Cleavage 157
gpa.ration of blastomeres suggests an explanation of identical twins
gnd the duplicate monsters which play so large a part in the study
of teratology. I t is generally accepted that identical, as distinguished
from fraternal, twins are the product of a single fertilized egg which
has divided completely during early embryology, whereas the duplicate
monsters, ranging from Siamese twins to monsters in which one indi-
vidual is but a parasite upon the body of the other, result from incom-
plete separation. These identical twins are always of the same sex.
Ordinary or fraternal twins (triplets, etc.) are supposed to be the
product of separate eggs which ovulated and were fertilized at about
the same time. Such twins are frequently of different sexes. In this
connection we might mention the fre'emartin, a sterile femal^ twinned
with a male, not infrequent among cattle, and supposed to reg^'t from
1 of 2 eggs which develop a common chorion and therefore a common
blood stream. I t is supposed that a male hormone circulating in the
common blood stream inhibits the normal development of the female
twin, so,resulting in the production Of the sterile freemartin (Lillie).
ORGANIZATION OF THE EMBRYO DURING GERM LAYER

FORMATION
The amphibian embryo is remarkably hardy, and during the early
stages of development will endure very severe operations. The work
of Harrison in the United States and of Spemann in Germany has
resulted in the_ perfection of a method of removing portions of an
embryo (microdissection) and grafting them into a new environment,
where they will continue development. This makes it possible to test
the effects' of various intrinsic factors involved in embryonic develop-
ment. Thus the effects of gastrulation may be determined by moving
known tissue materials' into new situations both before and after
gastrulation. The embryo from which the portion is removed is known
as the donor; the rqmoved portion is called the graft (transplant);
and, when the portion removed is transplanted into another embryo,
the second-embryo is' termed the host.
Figure 99 shows some of the methods which have been developed
in transplantation exjperiments. Thus the graft may be transplanted
into another-portion I of the same embryo (homoplastic transplanta-
tion) } It may be transplanted into another embryo of the same species
(heteroplastic transplantation). I t may even be transplanted into an
embryo of another species or genus (xenoplastic transplantation).
'^Soirie investigators use autoplastic = homoplastic; homoplastic = heteroplastic;
and heteroplastic=xenoplastic.'
Another method which has brought interesting results is ttansplant-
ing the removed portion into a nutrient medium and allowing it to
develop there under sterile conditions (explantation). This is also
Graft
Incision
Interplant
Fig. 99. • Diagrams to sliow different methods, of transplantation, etc. ' A, Homo-
plastic transplantation. B, Heteroplastic transplantation (both donor arid host of
same species). C, Xenoplastic transplantation (donor and _host of' different
species). D, Explantation (in vitro). E, Inte'rplantation. ' {Baêd on'a diagram
of Diirken.)
Iknown as cultivation "in vitro,", which means in glass. Another in-

genious technique is transplanting the graft into a cavity of ahotlier
embryo and allowing it to develop there. The example shown in
Fig. 99£J is of a bit of embryonic tissue transplanted into tlie eyeball
of a tadpole, which acts as a nutrient chamber. Hoadley and others
Organization during Germ Layer Formation 159
jjave developed a teehnique of grafting chick embryo tissue from a
donor to the chorio-allantois of a host. Such a technique is called
interplantation (implantation).
When considering the results of these experiments, we must realize
that they fall into three classes. The first, which is concerned with
the fate of a particular portion of the embryo when explanted or
interplanted, may be called isolation experiments. The second, which
is concerned with the fate of an embryo from which a particular por-
tion is removed, may be called defect experiments. The third, which
is concerned with the fate of a particular portion of an embryo which
has been transplanted into a host and also with the effects produced
by the transplant upon the host, may be called recombination ex-
periments.
Plasticity (Dependent Differentiation)

In'the amphibian egg, which is of the regulation type, it has been
demonstrated that the presumptive organ regions of the blastula (and
until about the middle,of gastrulation) are quite plastic, i.e., can be
transplanted into other localities and will give rise to organs appro-
priate to the new locality. Tissues which thus conform to their new %J
situation are said to develop neighborwise. Thus, material which is
presumptive epidermis can be transplanted into a region where it will
become neural f)late, mesoderm, or even endoderm. Presumptive meso-
derm is more refractory.. When transplanted it tends to invaginate,
but within the mesodermal area small groups of cells (jan be inter-
changed freely. . The presence of yolk apparently prevents the large
cells of endoderm from" conforming to the pattern of surrounding cells.
In the chick, however, the endodermal cells show a high degree of
plasticity.
Very instructive experiments are those in which material is trans-
ferred from a species |with heavy pigmentation [Triton taeniatus) to
one with light pigmentation [Triton cristatus). Here the graft pre-
serves its racial cha'raijter of pigmentation while "otherwise conforming
to the development-of the; host. Figure 100 illustrates such an example
of xenoplastic transplantation. The light-colored graft from T. cris-
tatus has developed into part of the neural tube of the host, where it
stands out by reason] of its light color. In the reciprocal transplant
(Fig. 101), the dark graft from T. taeniatus has given rise to the right
external gills of the host.
With the exceptioii of the chorda-mesodermal field district (the
gray crescept area, or marginal belt) and the endodermal field district,
in which the phenomenon of plasticity exists only within the area
— y
Pig. 100. Xenoplastic transplantation. Here T. cristatus (light) is the donor and
T. taeniatus (dark) is the host. A, After transplantation. B, The transplant de-
veloping in the neural plate (region of the brain). C, Section in later stage show-
ing transplant developing in fore-brain. ('After Spemann.)
ti^%!.^»'
Fig. 101. Xenoplastic transplantation betjveen Triton taeniatfs (dark), the donor,
and Triton cnstatus (light), the host, to show early plasticity. A, Imrftediately
after transplantation. B, The transplant developing in, the gill region. C, The
gills of the transplant relatively more advanced. D, Section throvigh .C in the gill
region. (After Spemann.)
itself, it may be said that the possibilities of any group of blastomeres
are greater than their presumptive fate. This is expressed in another
way by saying that differentiation potency is greater than differentia-
tion fate.
The Loss of Plasticity (Self-Differentiation)

After gastrulation is well under way, this plasticity seen in earlier
stages is lost. The various regions of the embryo have become deter-
mined and thenceforth will
trive rise only to the struc- Ear field Neural tube field
tures normally developing Eye field

from them. From now on
it is a real mosaic. Figure
102 shows an embryo in Hypophysis
which the various organ field
Nose field
fields are determined. If
Lens field
a bit of tissue is removed Hindlimb field
Balancer field
from the^ eye field ,and GUI Forelimb field
transferred to the flank of field
another embryo (Fig. 103);, Fig. 102. Diagram of an amphibian embryo,

it will' give rise only to showing organ fields as determined by trans-
plantation experiments (after Huxley and de
an eye, even in its new Beer).
and abnormal environment.
Tissues which, develop in this manner, independent of their new sur-
roundings, are said to develop self-wise.
Similar experiments have been carried on with the chick, and it has
been proved,-that the eye field, ear field, limb buds, and other regions
will develop and give rise only to the respective organs which they
would normally produce.
Very striking results have been obtained by implanting portions of
rat embryos on the chorio-allantois of the chick, and a considerable
f
amount of self-differentiation has been demonstrated.
T H E ' CHORDA-MESODERMAL FIELD. The area which first manifests
the property of • s.elf-(;lifTerentiation is the gray crescent region asso-
ciated with, the dorsal lip of the blastopore. This area always under-
goes involution to develop notochord and mesoderm and induces the
formation of a neural tube from the layer of ectoderm cells immedi-
ately overlying it. Ût what is more striking is the fact that, even
when transplanted into the ventral or lateral ectoderm of an embryo
of approximately the' same age, it undergoes involution, continuing to
develop notochord and somites and at the same time inducing the
forma'tion'of a neural tube (Fig. 104). In other words a secondary
embryo is organized in association with the implanted tis.sue. pQr
this reason the area was originally called.the "primary organizer"
(organizator, organizing center).
It was later shown that when material from the chorda-mesodennal
field had been dried, boiled, or narcotized, it could still evoke the for-
mation of a neural plate and folds in the ectoderm overlying it.
Evocation, then, differs from induction in that it can be brought about
Donor
Fig. 103. Self-differentiation in the'toad Bombinator. A, Donor in early neurula

stage showing region from which graft was taken. B, Host in Jartejieurula.stage.
C, Section through later embryo of host, showing graft forming'optic cup; in region
normally occupied by pronephros; (After Spemann.) ; i
by lifeless agents. Many such agents, 'bits of tissue from adult ani-
mals and a number of apparently unrelated chemicals, act as evocators.
We must distinguish, therefore, three properties in the chorda-meso-
dermal'field: First, its self-differentiating ability, that is to say, the
fact that this area is the first to have its f^-te determined;^.seCond, its
inductive ability, in that it can induce the tissue around i't to respond
to and become part of the pattern, which it is developing; third, the
fact that it contains substances which are sufficiently s.foble to .resist
physical and chemical treatments and yet evoke a response in nearby
areas. . ' •
The inductive influence of the chorda-mesoderm on the neijral plate
apparently continues for some time after the neural tube is formed.
rp)ie neural tube becomes differentiated along its long axis so that the
telencephalon is formed at the anterior end followed by the dien-
cephalon, mesencephalon, etc. The chorda-mesoderm continues to
x ( •
\
/
• • J
V •>
' . t.t, -.-..:onda
-.-..:onda J^\;^j"
"
Primary pronephric duct

Secondary pronephric duet
Primary neural Secondary gut
tube
Secondary
neural
tube
Primary ^^^"i'v , « V * /'/ Secondary

notochord '\-J * ^ ;f notochord
Primary gut ^^v^.
Fig. 104. Effect of transplai^tiag choYda-mesodermal field. A, Dorsal view of

host {Triton taeniatus) in neurula stage. B, Right side view at same stage,
showing secondary iieuval plate induced by dorsal lip region of the donor (Triton
cristatus) shown in, white.! C> Later stage, showing primary embryo in side view
and secondary embryo in dorsal view. D, Transverse section through C. (After
_,' • ' ' Spemanii and Mangold.)
play a part in this process either through a gradient action of some one
substance, or, more pijobably, through the inductive action of specific
\substances produced at various levels corresponding to the different
•regions of the neural tube.
It m,ust also be realized that the organizing stimulus originating in
the notochord is not specific merely for the differentiation of the neural
164 Experimental Embryology-
tube. Instead, as shown by the work of Yamada, it acts non,
specifically, tending to raise the level of differentiation of any tissue
near it to a more dorsal level. Thus, a ventral portion of lateral meso-
derm of Triton cultivated in vitro with notochord in an envelope of
ectoderm will produce pronephric tubules rather than blood which
would normally develop from it.
In later development, subfields (Fig. 102) are segregated in the larger
fields, until the property of plasticity has entirely disappeared and the
fates of the different parts of the embryo are strictly determined. The
mechanism of this process is still obscure, but experimental embry-
ologists are convinced that it is a progressive one. In general it appears
that when a particular structure is developing it gradually comes to
exert an inhibitory effect. Thus Weiss has shown that embryonic
tissue explants containing a structure A will grow successfully in ex-
tracts made from embryos from which the structure A has -been
removed. By contrast, if the culture medium contains an extract of A
then growth of this structure will be inhibited in the explant.
In other instances two main factors appear to be involved. One
factor islthe ability (competence) of a portion of the embryo to respond
to an induction, the other, the presence of an inductor. For example,
in some species of frogs (e.g., Rana fusca) the lens of the eye will not
form if the prospective primordium of the retina is removed in the
neurula stage. In another species {Rana esculenta) the lens fornis
even if the retinal primordium has been removed. The question arises
as to whether the failure of the lens to form in R. fusca was due to the
lack of an inductor or the lack of competence. It was, settled by graft-
ing over the developing optic vesicles the belly skin of the same species
and, in other embryos, the belly skin of a toad. The frog^'ski'n did not
form a lerfs but the toad skin did, thus showing that the-failure'was due
to lack of competence. • ' •
ENVIRONMENTAL FACTORS IN DEVELOPMENT

Many experiments have been carried on in the attempt to/deterrnine
the effects produced on the developing embryo by changes- in the en-
vironment. Xhese investigations have established norm-at' limits of
temperature, etc. Within these limits, although development'may be
altered as to rate, etc., it is nevertheless carried on to a success,ful out-
come. Beyond these limits the alterations are so profound as to pro-
duce monsters or cause death. Among the factors susceptible to
experimental control are gravity, heat, light, the chemical constitution
of the environment, and food.
Environmenta;! Factors in Development 10-
GBAVITY (AND CENTRIFUGAL FORCE). I t has been remarked (pace
250) that the original polarity of the egg is not due to any effect of
gravity. In telolecithal eggs, however, gravity may have some effect
on the course of development. Thus frog's eggs when forcefully in-
^'erted may give rise to duplicate monsters. The hen's egg if not
rotated at regular intervals fails to hatch. It has been shown (Dareste,
1877) that this is due to the failure of the yolk sac to complete its
development. It adheres to the allantois and cannot be retracted into
the body as in normal development.
The influence of gravity may be shown in an exaggerated manner
by prolonged centrifuging. I t was found by 0. Hertwig that, if the
frog's egg is centrifuged during cleavage, the yolk is so concentrated
in the vegetal hemisphere that the cleavage-planes fail to cut through
it and the end result is meroblastic cleav-
age suggestive of that seen in the chick
(Fig. 105).
HEAT. The rate of development is
directly affected by temperature. This,
is well shown in the development of the
frog's egg. In this the-range, or difference,
between the upper and lower limiting
temperatures, over which normal develop-
ment is possible is over 20°C. (Moore,
1939). Within this range, which in Rana Fig-105. Vertical section
pipiens extends from approximately 8°C. *^''°"S^' h\aBtu\<, of a frog's
, 00 o n J 1 / , egg after centrifugmg (after
to •28°C., development proceeds more Heriwig)
rapidly at higher temperatures and more
slowly at lower temperatures. The times assigned to the stages
(Shumway, 1940) used in this book are based on development at 18°C.
For the hen's egg, Kaestner determined the optimum temperature
for normal development to, be between 35° and 39°C.' (95°-102°F.).
The maximum temperaiture tolerated is 43°C., the minimum 28°C.
(20°-2I°C., EdWards).,
Eggs of either frog or, hen which have been exposed to extreme heat
or cold and. then returned to the optimum temperature often develop
abnormally. A' commoti type of monster is one in which neural plate
and notochord are splitj (spina bifida).
Very striking result^ have been obtained by subjecting the eggs
of the frog or the hen'to a temperature gradient, that is, controlling
the temperature so that one side is hotter or colder than the other.
If the .gradient runs along the polar axis, and the greater heat is
applied to the animal pole, the result is that the embryos and larvae
• have overlarge^heads; if the higher temperature is applied to the 'vegetal
pole, the head region is subnormal. Wlien the temperature gradient is
applied laterally, the development pf the heated side proceeds more
rapidly than that of the coo/ed side.
It may be concluded that, within the limits of toleration, develop-
ment is accelerated by increased temperatures and retarded by de-
creased temperatures.
LIGHT AND OTHER FORMS OF RADIATION. In spite of a considerable
number of experiments designed to determine the effects of definite
intensities and wavelengths of light upon the developing embryo, the
results are as yet too inchoate to be discussed in an elementary, text-
book.
Ultraviolet light, X-rays, and radium emanations in extreme dosage
cause the cessation of development. In smaller dosage, they bring
about anomalies (abnormalities in structure caused by disturbances
in development). It should be remembered that the work of Miiller
and others indicates that these agents accelerate the rate of mutation
of DrosopHila genes, and so induce genetic point mutations as well
as developmental anomalies.
CHEMICAL COMPOSITION. The chemical composition of the surround-
ing medium affects profoundly the nature of development. The em-
bryo cannot develop without oxygen, for it cannot live without respira-
tion. It has been pointed out by Morgan that frog's eggs in the very.
center of the egg mass often develop abnormally (spina bifida, etc.).
And it has long been known that the hen's egg ceases development if
the pores of the shell are closed by water glass, varnish, or-other agents.
Water, too, is an essential. The growth of the embryo depends
upon the absorption of water, and all embryos must unjleô their
development within a watery medium. Even the terrestrial enabtyo
• has its private pond in the amnion. A slowing in the rate of develqp-
ment, accompanied by abnormalities and a large percentage ^f: deaths,
results from incubating hen's eggs in a desiccator. The percentage of
water in the frog's egg increases steadily during the -first two' weeks
of development.
A very striking series of experiments was carried on by' .Herbst
on the development of the sea urchin in artificial sea water which
had been made up omitting one after another of the elements found
in normal sea water. Jenkinson, summarizing the evidence,, says:
"The experiments which we have been .considering are unique of
their kind, and it is impossible to exaggerate their importance. Por,
whatever may be the ultimate explanation of the facts, there can be
no doubt whatever that the most complete demonstration has been
Environmental Factors in Development 167
given of the absolute necessity of many of tlie elements occurring in
ordinary sea water, its normal environment, for the proper growth and
differentiation of the larva of the sea urchin. Nor is this all. Some
of the substances are necessary for one part or phase of development,
some for another, some from the very beginning, others only later on.
Thus potassium, magnesium, and a certain degree of alkalinity are
essential for fertilization, chlorine and sodium for segmentation, cal-
cium for the adequate cohesion of the blastomeres, potassium, calcium,
and the hydroxyl ion for securing the internal osmotic pressure neces-
sary for growth, while without the sulph-ion and magnesium the due
differentiation of the alimentary tract and the proper formation of
the skeleton cannot occur; the secretion of pigment depends on the
presence of some sulphate and alkalinity,- the skeleton requires cal-
cium carbonate, cilia will only beat in an alkaline medium contain-
ing potassium and magnesium, and muscles will only contract when
potassium and calcium are there."
The addition of chemicals to the medium has resulted in many
interesting disturbances in development. We can call attention here
to two only. In the sea urchin it was found that the addition of
lithium salts to sea water caused the'-embryo to undergo a very curious
form of gastrulation, in which the endoderm and mesoderm were
evaginated instead of being invaginated (Herbst). Such an embryo
is called an exogastrula. . •
Holtfreter (1933) induced exogastrulatibn in the egg of Triton by
removing the egg envelopes and-placing the developing egg in weak
Ringer's salt solution. In the cases where development continued for
some length of''time (Fig. 106), it was discovered that the embryo
developed in two parts, an ectodermal portion with no differentiation,
connected by a narrow isthmus to a mesendodermal portion in which
differentiation proceeded, but in an abnormal fashion. The embryo
is inside-out. The mesendodermal portion of the exoembryq develops
a typical notochord, soniites, kidney, gonad, a heart (empty), and a
digestive tube, in which ill the typical regions are indicated, including
visceral pouches. These results confirm those of transplantation and
explantation experiments discussed in an earlier section, and it is
particularly interesting to note that the ectoderm fails to develop a
neural tube in the absence of the chorda-mesoderm below it,
FOOD, HORMONES, AND' VITAMINS. The amount and kind of food
supplied to "the developing young naturally affect the subsequent
development. Thus, if frog tadpoles are fed on an exclusively vege-
tarian diet, the intestine becomes much longer than when an exclusively
meat diet is offered. Specific foods often result in equally definite
168 ' . Experimental Embryology
changes in the body. Thus Gudernatsch discovered that frog tadpoles
fed on thyroid tissue grew less rapidly but underwent metamorphosis
much more rapidly than the controls.
Later investigations indicate that the effects of thyroid are due to a
hormone formed by this gland (thyroxin), which is a definite factor in
bringing about amphibian metamorphosis (Fig. 107). The thyroid is
but one of several endocrine glands which have been shown to be
Epidermig
Rectum
Intestine
• Kidney tubule*
Coelom
Notochord
Trunk muscles
Pharynx
Head muscles
Mouth endfiderm
Fig. i06. Exogastrulation in Triton. A, B, Bxogastmla^Siowing.direction of dis-

placements during exogastrulation. Compare Fig. 56. C, Section of later exo-
embryo. (.Ajter Holtjreter, in Huxley and de Beer.) /• ^•
important factors in development either by feeding experimentSj, by

transplantation of glandular tissue, or by extirpatian of the glandJrom
a young embryo. ;, ' • "^
The pituitary gland, often called the master gland of the vertebrate
body, secretes a number of hormones. The follicle-stimulating hor-
mone and luteinizing hormone have already been mentioned '>tpage
137): In, niammals a lactogenic hormone controls the enlargenient of
the mammary glands. Other hormones secreted by the pituitary gland
are important in stimulating' the development and activity of such"
endocrine glands as the tjnyroid, the adrenal, and the gonads. Still
. another, the so-called growth-promoting hormone, stimulates the
growth of the embryo in later stages. It must- not be thought that this
last-named secretion is wholly responsible for growth, because this
Environmental Factors in Development 169
phenomenon commences before the appearance of the pituitary gland,
ancL in tadpoles, the extirpation of the gland does not inhibit further
growth.
The gonads form the so-called sex hormones, male sex hormone in
the testis, and female sex hormone in the ovary. These have most
important effects on the later development of the sex organs of the
individual. Lillie's theory as to the origin of the freemartin, a sterile
Fig.' 107. Metamorphosis in Ambystoma. A, Before metamorphosis, B, After

metamorphosis. {After Diirken.)
female intersex in cattle, has, been mentioned (page 157). Witschi

has created artificial Siamese twins in amphibia by cutting.off a por-
tion of the embryos in an'early stage and grafting the two cut surfaces
together. Individuals unitfed side by side are called parabionts; those
united end to .end are termed telobionts. If both members of the
pair are of the same sex,. development proceeds normally, but if it
turns out that one" was a genetic female and the other a genetic male,
the female is underdeveloped sexually, apparently due to the more
powerful effect of the male sex hormone. Several investigators have
170 • . Experimental Embryology
shown that sex hormones can be transmitted across the placental
barrier, but freemartins have not yet been successfully produced
through the direct action of purified male sex hormones.
The role of the vitamins in the metabolism of the embryo is too
little understood at the present time for us to do more than allude to
this subject. Vitamin E is often called the antisterility vitamin be-
cause its absence from the diet results in loss of the reproductive power.
Adamstone (1931) has showji that the chick embryo produced by hens
on a vitamin-E-free diet dies early in development, after extensive dis-
turbances in the blood vascular system. .
It has also been shown that other vitamins including several of the
B vitamins are necessary for development. Furthermore, Spratt has.
found by in vitro culture of chick embryos that glycogen is one of the
substances most essential for early development. The role of other
basic food substances is not known.
11
Digestive System
and Related Structures
The digestive tract of the vertebrate is a tubular structure derived
from the primitive gut or gastrocoel formed at the time of gastrulation
when segregation of the germ layers takes place. Its inner lining is
derived largely from endoderm, but its openings—mouth, anus, gill
clefts, etc.-:-a'rise from ectodermal pouches, and the whole tube is
Neural tube
ôtochord
Ppeoral
gut
Postanal
gut
Proctodaeum
-Hypophysis'
Stomodaeum
F i ^ A ^ T Diagram of a generalized vertebrate embryo to show endodermal

^ !' derivatives.
eiisheathed in splanchnic mesoderm. Thus, all three germ layers con-

^ tribute to the formation of the,' digestive system. At a very early
stage, three regions of the gut can be recognized based on-their relation
to the yolk mass (Fig. 73). iThese are: the fore-gut (Fig. 108), situ-
ated anterior to the yolk mass and extending as a blind pocket into
the'head; the mid-gut,-lying immediately above and dorsal to the yolk
mass; and the hind-gut, a blind, pocket extending posterior to the yolk
mass. In such forms as amphioxus and the frog in which the gastro-
coel originally communicate^ with the exterior by way of a blastopore
at the posterior end, this opening soon closes over. In all cases an
anterior and posterior opening to the exterior must later be developed.
The tube itseVf undergoes great specialization, thus producing the vari-
171
172 . Digestive System
ous organs of the digestive tract as well as other structures such as the
respiratory organs and certain endocrine glands.
THE FORE-GUT AND ITS DERIVATIVES
Development of the Mouth Cavity

The opening of the fore-gut to the exterior is established by develop-
ment of a mouth cavity. This is a comp'ound structure derived in part
from the stomodeum and in part from the fore-gut. The stomodeum
is an invagination of the ectoderm on the ventral side of the head.
The stomodeum grows inward to meet the ventral side of the fore-gut
but not quite at the anterior end. Thus, a small blind pocket of the
fore-gut, called the preoral gut, or Seessel's potket, extends forward
beyond the developing mouth cavity. The closing plate between
stomodeum and fore-gut composed of ectoderm and endoderm eventu-
ally ruptures, forming the oral cavity or mouth. The mouth opening -
is bounded by the maxillary and mandibular process of tha first vis-
ceral arch. These ultimately become the upper and lower jaws.
A number lof important structures are developed in association with
the stomodeum and mouth cavity, as follows:,*^
PITUITARY BODY (F^g. 108). This structure,takes its origin from' two
sources, viz., Rathke's pocket and the infuqdibulum. Rathke's pocket
or the hypophysis develops as ah evaginatiAa of the anterior surface
of the stomodeum. It grpws upward beneath the developing bnain and
fuses with an evagination from the floor of the diencephalon, the in-,
fundibiilum. Thus, both structures which contribute to the formation
of the pituitary body are ectodermal in origin. Rathke's pockpt pro-
duces the glandular anterior lobe, or pars anterior, of the pituitary •
body, and the Infundibulum give rise" to the pars nervosa or p6§teriot
lobe. The pituitary body soon loses its connection with the mouth
cavity but retains its connection with the fioor*of th^brain, and hence
is often called the hypophysis. *' >. < .'
TEETH (Fig. 109). Teeth develop inuch like thcfplacoid scales of
elasmobranch fish. • They arise on the dentfe,l ridge or lamina of' the
maxillary and mandibular processes. The dental ridges have theiorrn
of an arc-shaped ridge around the margin of the floor and roof of the
mouth cavity. They are formed of a core of mesoderm coveVed with
epithelium derived from ectoderm of the stomodeunj. At intervals
along the dental ridge, the tooth-primordia develop. Each of these
consists of two elements: a cup-like ectodermal enamel organ and a
conical dental papilla consisting of mesdderm. The enamell organ is
T h e Fore-Gut and its Derivatives 173
formed by invagination of tlie epithelium of the dental ridge (Fig.
109A), which, on making contact with the underlying mesodermal
papilla, becomes evaginated once more to form a double-walled cup
(Fig. 109B). The layer forming the inner lining of the cup becomes
the enamel organ (Fig. 109C), and its cells, the ameloblasts. secrete a
layer of enamel. The outermost cells (odontoblasts) of the mesodermal
papilla in contact with the developing enamel produce a layer of
Primary
Epithelial enamel organ
invagination
Secondary
mmm T-E^~enamel organ
Epithelium 7?v>-••-^j-'^^r-f-.:.fr''•"'^'''''''^.-C:'•••'r^'
of m o u t h , ' ^ ' ' '" ' " ' ' ""' •'" ' " ' • • • • '•••••'. '•
• ' ; ' ' • ! / ' ' ' - - ' -••-'
rr" Dental ridge
Enamel ',' y;"'/,, ;'.•;A'^JslkTS''"-'- •'-' -'-''-•'. •"•'."'.'-".'

Dentine '-.['L;•'•>;:i-f^ Enamel organ
fTtr-Pulp
\ F i g . 109. Diagrams to show origin of vertebrate tooth (lower jaw). A) Invagina-

tion of epithelium. S / F o r m a t i o n of primary and secondary cup-shaped enamel
organ. C, Formation of tooth.
dentine. In this manner the crown of the tooth is formed. Below the
crown, the odontoblasts-Produce dentine to form the root of the tooth.
The mesodermal core fUlihg the root and crown becomes the pulp of
the tooth, and,is supplied I with blood vessels and nerves. The root of
the tooth fits into' a bony'socket or alveolus of the jaw, formed when
ossification occurs in the mesoderm surrounding the root of the tooth.
In animals in which the milk dentition is replaced by a permanent set
of teeth, secondary enamel organs are budded off from the primary to
become the primordia of jthe permanent teeth (Fig. 109B).
TONGUE (Fig. 246).. The tongue arises froto two sets of paired, bud-
like prominences on the floor of the mouth cavity. These are the
anterior and posterior lingual primordia. The anterior primordia lie
opposite .t)ie first branchial arch and are composed of an outer ecto-
dermal layer with a core of mesoderm. The posterior primordia lie
174 Digestive System
opposite the second branchial arch and have an outer endoderma)
layer-cove'ring a core of mesoderm. As these structures enlarge, they
fuse together and the anterior end grows forward in the floor of the
mouth 'cavity, forming a strap-shaped structure. Its surface epithelium
is derived from ectoderm and endoderm, and the mesodermal core
forms the muscle which constitutes the main mass of the tongue. Some
deviations from this general plan of development are found in various
vertebrates.
;il:»it»J«l«g^
•Fig.' 110. Diagrams illustrating formation of a gland. A, Invaginationi of solid

cord of epithelial cells. B, Branching of cord. C, Cords hollow out to produce.
ducts. D, Ends of branches hollow out to produce acini.
SALIVARY GLANDS (Fig. 110). Salivary glands are derived largely

from ectoderm although they arise near the junction of ectoderm and'
endoderm. These glani^s follow a general plan of development which
i^'"applicable to many other glandular structures. The surface ecto-
/ (ierm of the mouth cavity evaginates into the underlying'mesederm,
' r'forming solid cords of cells which branch extensively,' ramifying
through the mesoderm. The cords of cells hollow out, thus' forming
tubular ducts.' The ends branch extensively and also hoUow oH^"
forming larger, sac-like alveoli or acini. The ectoderm lining- the
, alveoli thus becomes the secretory epithelium. In the lower; verte-
brates salivary glands are lacking, but in mammals where they .reach
their highest development there are three typdfe, as follows: •
d. The parotids, which arise near the angle of the mouth and' grow
backward into the underlying mesodermal tissue ta the region of
the ear.
b. The submaxillaries, which arise as a series of evaginations of
endoderm in the labial groove which lies between the dental ridge
and the lining of the mouth. These evaginations invade the meso-
derm beneath the developing lower jaw.
c. The sublingual glands, which arise as evaginations ofHhe endo-
jgym of the hnguo-labial groove which lies between the tongue and
.gjital ridge. The evaginations invade the territory beneath the
tongue.
PALATE. The palate forms a partition separating the mouth cavity
fjom the nasal passages. It develops from shelf-like lateral palatine
processes which grow toward the mid-line from the maxillae to meet
3 similar median palatine process which grows backward from the
median nasal processes. In early development, these primordia are
frequently kept apart by the developing tongue. After withdrawal
of the tongue they fuse, thus cutting off the nasal passage from the
niouth. The hard palate of the adult results from the development of
the palatine bones which arise in the mesodermal cores of the palatine
processes. .
pharynx and its Derivatives

Posterior to the mouth cavity is the pharynx. This region of the
fore-gut is generally marked in the early embryo by the development
of the visceral clefts or gill slits. These structures are formed from
two sources: a series of transverse groove-like invaginations of surface
ectoderm of the sides of the head fqld grow inward to meet a similar
series of lateral endodermal evaginations on the lateral walls of the
pharynx. When these grooves meet, a closing plate is formed. The-
gill slits, if present, result from the breaking,down of this closing plate.
Priniitively, fi visceral clefts or-gill slits are developed. Thus, between
succeeding gill slits' there remain pillars of tissue which form the
branchial or visceral • arches (p. 121). These are quite important
in embryonic development since they constitute the territories through
which the'aortic arches flow as the blood vascular system develops.
The pharyngeal region-is also important as the area in which several
of the endocrine glands develop.
THYROID GLAND (Fig. 111). The thyroid gland arises as a median
ventral evagination of the 'floor of the pharynx lying- opposite the
'second visceral groove. The structure bifurcates, thus forming the
' two main lobes of the gland, and continued division of each of these
i masses results in the formation of a large number of vesicle-like
structures. These constitute the secretory follicles, which are lined
with a characteristic cuboid,al epithelium. As the gland develops, the
original connection with the pharynx is lost, since the thyreoglossal
duct becomes occluded. In early development, the gland is very
intimately associated with the upper end of the ventral aorta. As the
heart retreat^ into the thoracic cavity, the thyroid is drawn deeper
into the region of the throat and the two lobes come to lie on either
176. Digestive System
side of the esophagus. The thyroid gland is important even in the
embryo as an endocrine gland controlling general metabolism, and
in amphibia it has been shown to exert a direct effect upon meta-
morphosis. . Experimental evidence shows that the onset of meta-
morphosis of the larvae of Amhystoma can be hastened by feeding
them thyroid extract.
PARATHYROID GLANDS (Fig. 111). These structures are also endo-
crine glands arising from epithelial tissue lining the third and fourth
visceral pouches. The tissue involved proliferates cords of cells into
Thymus
Thyroid
Ultimobranchial Ultimobranchial
Ultimobranchial
Fig. 111. Diagrams showing origin of epithelial,'bodies in A frog; B, chick;
and C, man Roman numerals refer to« visceral pouches.
the underlying mesenchyme of the adjacent brancjiial arch. Thus

.two.paired masses of tissue are formed. These become v5ry .intimately
associated with the developing thyroid gland, forming- small ^masses
of parathyroid tissue at the upper and lower ends of each lobe-of the
thyroid. They often become more or less completely embedded^ in
the thyroid tissue. The parathyroid gland produces the hormon§
parathormone, which is concerned with calcium metabolism and hende
is of considerable importance in connection with.the developroent of
skeletal structures in the embryo. , •' -
THYMUS GLANDS (Fig. 111). These bodies are also epithelial in
origin, arising from the lining of the visceral pouches in.mifch the.
same manner as the parathyroid. In the frog this tissue corned from
the dorsal side of the first and second pouches, in the chick from the
dorsal end of the third and fourth, and in the mammal from th'e ventral
end of the third and fourth. The epithelial tissues again proliferate
into the underlying mesenchyme, forming a reticulum in which a great
accumulation of lymphocytes, develops, thus producing a structure
greatly resembling the adenoid tissue of the tonsils.' Howey'er, some of
' ' ' \ ' • ' •
V
the epitheHal tissue has a different fate, becoming differentiated into
concentric masses of crescent-shaped cells. These structures are very
conspicuous in thymus tissue and constitute the so-called Hassall's
corpuscles. The function of the gland as an endocrine organ is un-
certain. It is known, however, that, when it is fed experimentally to
tadpoles, there is excessive growth and delayed metamorphosis. More-
over, in the higher vertebrates, e.g., man, it is well developed in infancy
but gradually undergoes involution during adolescence.
ULTIMO BRANCHIAL BODIES (Fig. 111). These structures are also
epithelial bodies apparently of glandular nature arising from the fifth
and sixth visceral pouches. However, both their fate and function
is uncertain.
General Structure of the Digestive Tube

In the early embryo, the gut is lined by endoderm and is covered by
a layer of splanchnic mesoderm. There is later an extensive invasion
of mesenchymal' cells between these two layers. The three tissues in
later development give rise to the layers characteristic of the adult
structure as follows:
Mucosa, the inner lining of the gut formed of endodermal epithelial
cells and supporting tissues of mesenchymal origin.
Submucosa, k broad layer of connective tissue of mesenchymal
origin. •
Muscularis, the circular 'and longitudinal muscular layers derived
from the invading mesenchyme.
Serosa, the outer covering of connective tissue and peritoneal epithe-
lium cjerived from the mesenchyme and splanchnic mesoderm, re-
spectively.
Although the digeistiye tube has the general structure described
above, special characteristics are developed in particular regions of
the tube. The.esophagus (Pig. 112), that is, the tube leading from the
pharynx to the stomach, has a stratified squamous .epithelium in con-
trast to the simple colurrinar epithelium characteristic of the remainder
of the tube. The stomach becomes a dilated portion of the digestive
tube characterized by great development' of its muscular walls. In
the duodenum, ileum, and jejenum, the epithelium develops many fine,
finger-like villi, thus increasing the absorptive surface tremendously.
Development of the Liver (Fig. 113)

The liver is the largest igland in the body. It develops as a ventral
evagination Qf the floor of the fore-gut at its distal end. Several inde-
pendent primordia may form. As a result, the liver usually consists
Visceral arches
(Hypophysis)
Esophagus
(Metanejphric
{Mesonephric duct (iiveriieulum (
Fig. 112. Endodermal derivatives in 10-mm. pig {jrom a wax reconstruction by

'• G.W. Hunter and L.T.Brown). ;• , '
of two main lobes and one or more smaller I6bes. The original eyagiha-
tion persists as a hollow saccular structure forming'the'gall bladder,
and its tubular connection with the gut becojnes the bile duct or
ductus choledochus. _The endodermal tissue of which" this evagination
is composed begins to proliferate extensively, forming irregular
anastomosing plates of hepatic tissue. The proliferating tissue thus
developing becomes intimately involved with, the vitelline veins, which,
at this level,' empty into the sinus venosus of the developing
heart. The vitelline veins are thus broken up by the invasion of the
developing liver tissue jnto an extensive network of capillary sinusoids
which course through the liver. In this manner the hepatic portal cir-
The Fore-Gut and its Derivatives 179
culation is established. The liver tissue meanwhile is organized in the
form of individual lobules with plates of hepatic cells radiating out
from the central vein, the central veins being tributaries of the hepatic
vein. The bile canaliculi develop between the rows of hepatic cells,
coursing outward toward the periphery of the lobules where they join
the hepatic ducts. These communicate with the gall bladder. The gall
bladder in turn communicates with the duodenum via the common
bile duct.
Fore-gut
Mid-gut
A . ' B
Fig. 113. Wax reconstruction of the liver primordia in a 48-hour chick embryo
(prepared by G.,T. Stanton). A, Anterior view. B, Posterior view. XIOO.
Development of, the Pancreas (Fig. 117)

The pancreas also, arises from the posterior .end of the fore-gut.
There are usually _ several primordia—one dorsal and one or two
ventral. These'develop as solid outgrowths, or cords of cells, into the
condensed mesenchyme of the dorsal mesentery supporting the gut.
Similar outgrowths develop into the mesoderm surrounding the ductus
choledochus. They continue to elongate and branch and finally the
tissue iorming the terminal,ends of the branches hollows out, in the
general manner characteristic of the formation of glandular tissue
(see page 174), thus forrfiing the pancreatic acini. The proximal por-
tions of the.branches become the pancreatic ducts. This tissue con-
stitutes the exocrine portion of the pancreas.
While these developments are going on, small masses of cells are set
aside in the developing pancreas to undergo quite a different develop-
ment, resulting in the formation of condensed masses of cells. Each of
these becomes highly vascularized by the development of a profuse
capillary bed. The structures so formed constitute the islets of Langqr-
hans and are the endocrine portion of the pancreatic tissue. They
secrete iftsulin, which is concerned with carbohydrate metabolism.
THE MID-GUT ^
All the regions of the digestive tract mentioned so far are derived
from the fore-gut. The intestine is derived in part from the fore-gut,
in part from the mid-gut, and in part from the hind-gut. It is im-
possible to indicate exactly which regions arise from these divisions of
the gut, as both the fore-gut and the hind-gut expand at the' expense
of the mid-gut during the consumption of the yolk. The intestine is
richly glandular throughout its length and is variously subdivided in.
the different vertebrates. Two main divisions may be noted: the small
intestine (ileum) and the large intestine (colon). The floor of the mid-
gut is either very thick, as in the arnphibia, or widely open, as in large-
yolked embryos. With the consumption of the yolk in many verte-
brates the yolk sac is drawn up into the body. It sometimes becomes
• a part of the intestinal floor.
THE HIND-GUT
, This portion of the digestive tube is' the prolongation. of the gut
tposterior' to the mid-gut. It empties into the cloaca but continues
beyond it as the postanal gut. The cloaca is derived in part from an
ectodermal invagination, the proctodeum, and from the associated
region of the hind-gut. ^ •
Diiferentiation of the Cloaca • •

The cloaca, as the name (Latin, doaca, sewer) implies is,a common
excretory chamber.' It receives not. only the intestine but also the
' excretory ducts from the kidneys, and the reproductive'ducts frorn the
gonads. In the amniotes it also produces a ventral ^divertiqulum,'the
allantois. In vertebrates, up to the mammals, it retains its role as
common excretory chamber. In mammals, however, the cloaca of t h e ,
embryo is partitioned by the development of a frontarl segturri, grow-
ing in from the sides toward-the mid-line. This divides the original
chamber into an anterior urogenital sinus and posterior recturh. These
chambers are separated from the exterior in the early embryo by a
common closing plate. Rupture of the portion of this plate closing the
urogenital sinus produces the urogenital opening, and rupture of the
portion covering'the rectum produces the anal opening in the'mammals.
I •: ' .• ..
TYPE VERTEBRATES
T h e Frog
STOMODEUM.- In the frog the stomodeal pit is at first a groove lying
. between the primordia of the eral suckers (Figs. 74, 75, 201, ^07). The
T y p e Vertebrates 181
groove deepens at its anterior end to open in stage 21 to become the
mouth (Fig. 212). I t remains round during larval life and is enclosed
by the mandibular ridges. Outside these, folds of ectoderm project as
the larval lips, on which horny larval teeth develop. These larval
structures are lost at metamorphosis, when the definitive jaws and teeth
are formed in the usual way. The primordium of the hypophysis
arises as a solid ingrowth from the ectoderm of the surface of the head
(Fig. 20,0), and later acquires a cavity and joins the infundibulum.
FoKE-GuT. When the mouth opens, a plug of cells forms in the
esophagus so that, while water can enter the mouth and pass out
through the gill clefts, no food can continue into the stomach and the
young larva continues to subsist on its yolk. The plug disappears in
stage 23. The origin of the tongue is, as usual, from an anterior ecto-
derrrial swelling and a posterior endodermal one (gland field). An
experiment (Holtfreter) indicates that the taste buds are of endodermal
origin. Six visceral pouches can be found. The first never loses its
closing plate,' which persists to give rise to the ear drum, while the
pouch itsdlf becomes the middle ear.' The sixth pouch is vestigial.
The others, II, III, IV, and V, arise in that order (Fig. 210) and by
the rupture of their closing plates become gill slits (Chapter 12).
The thyroid arises, just before hatching, as a solid diverticulum of
the pharynx;'it soon detaches itself and divides into 2 bodies which
later become vesicular. The thymus glands are. formed from epithelial
bodies (Fig. l l l A ) on the dorsal side of the second visceral pouches.
Epithelial bodies arise from the ventral side of the second visceral
pouches to become the carotid glands. Those of the third and fourth
pouches, it is claimed, persist and have been called parathyroids
(pseudqthyroid). The vestigial sixth pouches become the ultimo
branchial (suprapericarjdial) bodies (Fig, 111).
,^The esophagus is short, and the stomach a simple dilation, first
noticeable in stage 24. The liver arises as a backward ventral divertic-
ulum of the fore-gut, easily recognized at the time-the neural folds are
forming. I t is' not, however, until after the esophageal plug disappears
that the spongy complex of bile canaliculi and hepatic capillaries be-
comes evident. . Three pancreatic primordia appear in stage 23 and
fuse;, the dorsal duct disappears; the two ventral ducts fuse to become
the adult pancreatic duct (Fig. 114).
MID-GUT. The intestine of the tadpole, which is long and coiled
(about nine times the body length), becomes resorbed during meta-
morphosis until it is about one-third of its larval length (Fig. 115).
HIND-GUT. The cloacal region of the intestine gives rise to the
rectum'. The postanal gut is not connected to the neural tube by a
neurenteric canal after the fusion of the neural folds above the .blasto-
pore.-- There is, however, a pigmented streak at the site where a neuren-
teric canal might be expected (Fig. 200), and, in earlier editions of this
book, the general practice of considering this a neurenteric canal was
followed in the belief that the cavity had been, obliterated in the process
Oesophagus -.^
_ - G a l l bladder
Ductus
choledochus
!~ Pancreas •
Stomach
Duodenum.
Intestine'
, : (Pronephric
Cloaca— ducts)
Fig. 114. Endodermal derivatives of 11-mm. Rana pipiens emb^yo.^dorsal.view

{jrom a wax plate reconstruction representing a cast of the digestive tract prepared
by F. P. Eshlaman and V. E. Hanes), ) ,' ' '
•v "" ^
of preparing the specimen for observation. The urinary bladder of the'

frog arises from the ventral side of the cloaca" during metamorphosis.
The Chick ' ' ' , ' ' .

' . • • • ' ' ' .
STCTMODEUM. The mouth opens on the third'daji.of incubaition. (Fig.

236). The teeth are represented only by the tooth ridges,' which are
the first stage in the appearance of the enamel organs. Tjiese appear
on the sixth day of incubation and disappear shortly after the cornififca-
tion of the jaws. This results in the formation of the beak and the
egg tooth, the latter a horny projection on the upper jaw which is used
in breaking through the shell at the time of hatching, and soon after
disappears. The hypophyseal primordium arises as an evagination on
the second day (Fig. 231), loses its connection with the stomodeum on
the third, and unites with the infundibulum on the eighth.
Fig. 115. Digestive system in A, tadpole, and B, frog, to show actual shortening
I of the intestine after naetamorphosis (after Leuckart wall chart).
FORE-GUT. The primordia'of the tongue appear on the fourth day.

Fiye visceral pouches appear (Fig. 116), of which the first three open to
.the exteripr during the, third day of incubation (Fig. 235)'. The first
cleft closes during the fourth day, and the dorsal part of the pouch be-
comes the tubotympanic cavity. With the extension of the cervical
fiexure,, the remaining (pouches are crowded together and disappear.
The thyroid appears on the second day, separates from the pharynx
(Fig,'238) on the fourth, and on the seventh divides into two bodies
which migrate'backward to the junction of the common'carotid and
subclavian arteries. The thymus arises from the dorsal epithelial
bodies-of the third and fourth visceral pouches (Fig. I I I B ) while the
parathyroid rudiments arise from the ventral epithelial bodies of the
same pouches. The fifth pouch gives rise to the ultimo branchial bodies.
The esophagus is relatively long; and a. dilation, the crop, forms at
its posterior end. Tiie gastric region is divided into an anterior pro-
ventriculus, which contains the gastric glands, and a muscular'gizzard
at the posterior end. The liver primordium arises at the edge of the
anterior intestinal portal on the second day and, therefore, presepts the
aspect of an anterior ventral and two posterior lateral diverticula for a
short time (Fig. 113). Later in the same day the two lateral primordia
are brought together on the ventral side of the fore-gut as the anterior
intestinal portal moves back. The anterior (dorsal) and posterior
Visceral arches
Pharynxs^^ HI _3
iy„
V
^Thyroid
Stomach
Dorsal
pancreas
Yolk stalk
Cloaca."
Fig. 116. Endodermal derivatives in a 72-hour chick: • ~
(ventral) primordia persist as separate lobes, each with its ownJiepa'tic

duct. In the adult they come to lie side by side. The internal struc- •
tiire of the liver conforms to the usual pattern resulting ffom its rela-
tions with the vitelline veins. Three pancreatic diverticula arejornied,
the dorsal one on the third day, the ventral ones on the fourth. They
fuse in later development, and either two oir three oi the duCtg'persist,
those of the ventral pancreas coming to open inô th€^ common.bile duct.
• MID-GUT. The anterior portion of the mid-gut becomes the sihall
intestine, the large intestine arising from the posterior regi6n. - . >
It must be remembered that when the chick hatches the yolk has not •
been entirely consumed and that the yolk sac is drawn into the bodyof
the chick, still attached to the mid-gut. - When the yblk has been
entirely consumed, the shrunken yolk sac pinches off and degenerates.
HIND-GUT. About the middle of the second day, just posterior to the
primitive streak, ectoderm and endoderm join to form a small area
which is not invaded by mesoderm. As the tail fold forms, this is
carried around to the ventral side of the embryo, where it is known as
the cloacal (anal) plate. The rupture of this plate early in the fourth
day puts the hind-gut in direct communication with the developing
amniotic cavity. Anterior to the cloacal plate a broad evagination
gives rise to the allantois during the third day. No urinary bladder is
formed, but the cloaca is ultimately divided into three regions: an
anterior portion the coprodeum, into which the rectum enters; an inter-
mediate part, the urodeum, into which the urogenital ducts enter; and
the terminal proctodeum.
Man
STOMODEUM. The mouth opens during the second week of develop-
ment, and the. lips separate from the gums in the fifth. Two sets of
teeth are firmed, the first (deciduous) dentition consisting of 10 teeth
in each jaw, the second (permanent) dentition being composed of 16
teeth per jaw. The deciduous teeth dp not erupt through the gums
until after birth. The last are not shed until the individual is 11 years
old. The major salivary glands arise during the second month of
development and are believed to arise from the ectodermal portion of
the moiith. The hypophysis arises as a pouch (Fig. 246), becomes
attached to the'infundibulum, and loses its connection with the mouth
during the second month. The division of the primitive mouth into
nasal and oral chambers is described in Chapter 20.
FORE-GUT. The tongue arises from an ectodermal primordium which
becomes the body of the tongue and consists at first of a swelling on
the ventral side-of eachi mandibular arch and a median swelling
(tuberculum impar) b'etw.een them. To this an endodermal primor-
dium formed by swellings on the base of each hyomandibular arch is
added to form' the roo^. of the tongue. Between these two primordia
the thyroid gland arises as a ventral evagination from the pharynx.
After it is detached from the pharynx, the site of its origin is marked by
a^mall pit (foramen qecum). The primordia of the tongue unite dur-
' ing the sixth week. ,
Five pairs of visceijal pouches (Fig. 117) are formed by the end of
the first month. Noiie of these normally opens to the exterior. The
first pair forms the middle ear on each side, i.e., the auditory (Eusta-
chian) tube and tympanic cavity. I t is no longer believed that the
groovd (fossa) in which the palatine tonsil develops is the persistent
second pouch. Ventral epithelial bodies from the third pair of pouches
(Fig. IIIC) join to become the thymus gland, which becomes attached
to the pericardium and is dragged with it into the thorax. Those
from the fourth pair degenerate or join the thymus gland. Dorsal
epithelia bodies from the third and
Oral cavity fourth pair of pouches become the
Visceral parathyroid glands, which are
pouches
dragged with the thymus to the
Thyroid level of the thyroids, in which they
Pharynx enibed themselves. The vestigial
fifth pouches give rise to the ultimo
Trachea branchial bodies, which also becoine
Esophagus attached to the thyroid, either to
Lung buds become incorporated in this gland
or degenerate.
Stomach The esophagus, at first relatively
short, lengthens as the backward
Common
Dorsal 1 „ movement of the heart and lungs
I bile duct Ventral J " displaces the stomach. The latter
organ (Fig. 250) arises as a dila-
Yolk stalk
tion of the fore-gut posterior to
the esophagus. Continued growth,
mainly on the dorsal surface, pro-
Allantoic stalk duces the greater curvature, and a
Mesonephric
displacement of the whole organ so
Cloaca.
duct that the cephalic end is movedto the
Post anal gut left and the Caudal end.lo the right.
This is followed by a rotation of the
Fig. 117 Endodermal derivatives in a ^ ^ ^ ^ ^ ^ j ^ ^^ -^^ ^ axi§4hr-ough.
5-mm. humaii embryo, ventral view,
X25 (ajter Arey). 90° to the left. The liver arises
during the third week as a. central'
groove in the duodenum. The groove soon becpmes a sac, which grows
forward and ventrally into a mass of mesoderm which will become
the septum transv'ersum (page 197). The anterior wall becomes'the
glandular portion when it grows around the vitelline veins; the more
posterior part will become the gall bladder (Fig. 251). The. con-
nection between liver and duodenum persists as tlje common bile duct.
T^he pancreas appears slightly later, with either two or thrê pri-
mordia according to whether or not one of the ventral primprdia is
suppressed. The ventral pancreatic duct persists and opens into the
common bile duct. The ducts branch extensively, giving riê to hollow
acini, which secrete the pancreatic juice, and solid islands, which never
ve any cavities communicating with the ducts but discharge the
jjione insulin into the blood vessels supplying the gland.
]VliD-GuT. The intestine consists of portions contributed by all three
flivisions of the,gut, and is most conveniently divided into a cranial
nortion anterior to the yolk stalk and a posterior caudal portion. The
volk stalk is detached from the intestine during the fifth or sixth week,
and the rapid growth of the intestine throws it into a loop (Fig. 252)
which rotates (counterclockwise from the ventral side) and descends
into the umbilical cord (seventh week). In the caudal portion the
point of division between small and large intestines is marked by the
formation of a blind pouch, the cecum. The distal end of the cecum
does not grow as rapidly as the piroximal region and so remains a finger-
like projection known as the vermiform appendix. The small intes-
tine, growing more rapidly than the large, is thrown into a set of 6
primary coils, each of which develops secondary coils.
HIND-GUT. The cloaca becomes divided, by a frontal partition, into
a dorsal rectum and a ventral urogenital sinus (page 219). The cloa-
cal membrane"" is correspondingly divided into a rectal and a urogenital
plate, and the final openings are the anus and the urogenital orifice.
V
12
Respiratory Organs
As soon as cleavage begins in the fertilized egg there is a very rapid
increase in oxygen consumption and liberation of carbon dioxide,
but the early embryo, before the development of the blood vascular
system, carries on respiratory exchange over its entire surface. After
the development of blood vessels, respiratory exchange may take place
through any thin epithelium where the, blood corpuscles are brought
into contact with the oxygen-carrying medium. ^
In vertebiatfts s\icti as fish and amphibia whose development takes
place in ponds, rivers, and other natural waters, ectodermal outgrowths
on the visceral arches receive blood vessels' from the aortic arches and
become external gills (branchiae). As the blood stream passes through
the aortic arches immediately after leaving the heart, the blood is
oxygenated before being distributed to the body- I t is in connection
with the development of these external gills that the gill clefts are
formed, with the result that water admitted at the mouth and passing.
through the clefts creates a current in the vicinity of the external gills.
In vertebrates with cleidoic development, bii^s and reptiles, the* first
circulation is that of the yolk sac. This, however, is. remote from"
atmospheric oxygen, and the chick first acquires a' special- organ of
respiration when the_ allantois brings its blood vessels to the Chorion.
Mammals, with their intrauterine mode of development, soon develop
the placenta, which is the organ of fetal respiration. -: _•
The adult, too, may have one of many different respiratory-organs,
' whose epithelia may be either ectodermal or endodermal in origin.
Thus we find that among the amphibia respiration m a y t a k q ' place
in the skin as a whole (lungless salamanders); in specialized outgrowths
on the visceral arches, external gills (Necturus); or in the so-called"
hairs of the African frog, Astylosternus, ^ In this group are to be found
also examples of endodermal respiratory organs, the internal 'gills and
lungs. Internal gills ar^ otherwise found only among the, fish; the
lungs are the characteristij; respiratory organs of the amniotes. ' « '
188
Internal Gills 189
EXTERNAL GILLS
Among the amphibia, external gills (Figs. 74, 208, 210) may arise on
the three visceral arches posterior to the hyoid arch (arches III, IV,
and V). These develop as small .gill buds each consisting of an outer
ectodermal layer and mesodermal core. They elongate rapidly and
soon acquire a capillary loop from the adjacent aortic arch. The gill
buds branch several times, and smaller secondary capillary loops grow
into each branch. The complexity of the branchial outgrowth differs
markedly in different species, and can be reduced or augmented experi-
mentally by red.ucing or increasing the temperature at which develop-
ment is carried on. Except among Gymnophiona and Caudata, a fold
from the hyoid arch, known as the opercular fold, grows back to cover
the external-gills, thus enclosing them in an opercular chamber, which
may open by a pore on each side or by one only. After the formation
of the operculum the external gills atrophy and are resorbed, and a
completely new set of internal gills develops to replace them.
Efferent branchial
artery
External
gills
Internal
gills
i , • ] Afferent branchial-artery
Fig.' 118. .Diagram to show relations of external and internal gills in frog embryo
I {after Maurer).
INTERNAL GILLS
Internal gills (Figs'. 118, 214) are formed on the ventral surfaces of
the visceral arches and grow out info the visceral clefts as filaments or
thin sheets called demibranchs. These also consist of an outer layer
of ectoderrnal or endodermal origin, as the case may be, with a core of
mesoderm. They are formed by all fish and by the amphibia (excepting
190 Respiratory Organs
the Gymnophiona and the Caudata). It will be recalled that the first
visceral cleft does not have a permanent opening to the exterior except
in elasmobranchs and a few ganoids. Demibranchs naay arise in all
other clefts. The third, fourth, fifth, and sixth visceral arches niay
develop a demibranch on both anterior and posterior surfaces, the two
demibranchs of each arch constituting a gill. The first cleft, or spiracle,
sometimes forms a gill-like structure (pseudobranch). The origin of
the internal gills is disputed, some investigators claiming that they
arise from the endodermal portion of the cleft, others that they are
formed from ectoderm. In early embryonic life" the filaments of the
internal gills of some fish are elongated and have been called external
gills. Gills are not formed by the embryos of reptiles, birds, and mam-
mals, but filaments corresponding to those mentioned.above haye been
described in early embryos of reptiles and birds.
LUNGS
The typical respiratory organs of the vertebrates exclusive of fish
^re the lungs. These have often been compared with the swim bladder
of fish and the so-called lungs of the Dipnoi. However, the swim
bladder usually arises from the dorsal side of the fore-gut, in either
Visceral
pouch V
Visceral
Visceral groove
cleft V "V
Esophagus Visceral
pouch VI
Lung.bud
Fig. 119. Semidiagrammatic frontal section through pharynx of amphibian to.
show comparison of lung buds and visceral'pouches (ajler Makuschok).'
the esophageal or gastric region, whereas the lungs arise from;the sides
or floor of the pharynx. In the amphibia the lungs arise as a pair of
evaginations from the sides of the pharynx, posterior to the last pair
I of visceral pouches, which they resenable greatly (Fig. 119).- The por-
tion of the pharynx from which these .pouches* arise is cut off from the
esophagus above by a pair of 'lateral longitudinal grooves which meet
in the mid-line progressively from the rear forward. In this way the
ventral portion of the pharynx is converted into the trachea, opening
into the pharynx by the glottis and, at its posterior end, dividing into
the luhgbuds.. In the higher vertebrates, reptiles, birds, and mammals,
{he first structiire to appear is the laryngotracheal groove (Fig. 120).
This is a deep longitudinal groove on the floor of the pharynx. Its
posterior end soon begins to separate off ventrally from the dorsally
KW-
Fig. 120. Three stages in the development of lung buds and trachea in the turtle
Emys (ajter Hoohstettcr).
located esophagus,in the form of a blind tube which becomes the

trachea. The posterior free end of this tube bifurcates to form the
lung buds. The lung buds elongate thus forming the primary bronchi.
These subdivide repeatedly to form many branches, the secondary
bronchioles, tertiary bronchioles, etc., finally terminating in small air
sacs or alveoli.
TYPE VERTEBRATES
The Frog
EXTERNAL GILLS. Gill buds appear on the third and fourth visceral
arches in-stage 19 (Eig. 74). By stage 20, the bud on the third arch
has fornied its first branch and blood is circulating in the capillary loop.
In this stage a vestigial gill bud forms on the fifth visceral arch. The
gills on the other arches attain their greatest complexity in stage 22.
The opercular fold '(j'Fig. 75) is evident in the succeeding stage (23),
completely covers the external gills on the right side (24), and com-
pletes the opercular chamber in stage 25. There is an opercular open-
ing persistiftg. on the; left side, through which the water taken in at the
mouth escapes after passing through the visceral clefts.
INTERNAL GILLS. AS the external gills are covered by the opercular
192 Respiratory Organs
fold, a new.set of internal gills is forming on the veritral surfaces of the
visceral arches. These arise as rows of filaments, each row represent-
ing a demibranch. There are two rows (anterior and posterior) on
arches III, IV, and V, but only a single row on the anterior side of
arch VI. From the floor of the pharynx, a flap of tissue (velar plate)
grows over the visceral clefts on either side to cover them loosely and
prevent the escape of food (Fig. 214). A series of small projections
from the walls of the clefts serve as a strainer to supplement this pro-
tection. During metamorphosis the gill clefts and opercular chamber
are filled with rapidly growing cells, and this area is reworked to
become part of the body wall.
LTJNGS. The lungs of the frog arise as a pair of lateral evaginations
from the pharynx in stage 22, and the trachea is distinct- from the
esophagus in the following stage. During the period of raetamorphosis
the lung buds expand greatly and are divided by septa to form the
alveoli.
The Chick
Neither external nor internal gills are formed in the development of
the chick, unless such filaments as have been described by Boyden may
be considered an embryonic vestige.
T H E LUNGS. In the chick the laryngotracheal groove is the firs^' part
of the respiratory apparatus to appear, and is formed during the third
day of incubation. By the end of that day, the lung buda have ap-
peared tFig. 116). These push the splanchnic mesoderm*ahead of
them as they grow so that it forms their outer covering. The portion
of the coelom into which they grow is .not partitioned .off to form a,
definite pleural cavity. The 'original lung buds branch* exitehsively
during the first week of incubation, and during the'second some of
these branches grow out among the viscera and even into the hollow
bones, where they become "the accessory air sacs of the adult.
Man ' , ;
The lungs arise about the end of the fourth week 'from a'laryn-
gotracheal groove. The posterior ventral end'of the groove is cut off
from the dorsal 'esophagus by oblique lateral grooves wlîch pinch in
toward the mid-line and gradually advance forward,- thus separating
the trachea from the esophagus. At the free posteribr end of the
trachea bifurcation produces the lung bu'ds' which elongate, to form
the primary bronchi. On the right side an accessory lujjg bud, which
is known as the eparterial bronchus, is developed. The bronchial buds
continue to branch until about 17 generations of brcinchi. are formed.
Type Vertebrates 193
^fter birth, branching is renewed and, in all, 24 generations of divi-
sions are present. The dividing bronchi push out laterally into the
inesoderni surrounding the esophagus and trachea. The esophagus and
trachea, therefore, remain suspended in the mesoderm in the mid-line.
This septum of mesoderm will later become the mediastinum forming
the dividing wall between the right and left pleural cavities. The
origin of these cavities is discussed in Chapter 13. As the endodermal
bronchi push out into the mesoderm they are surrounded by a layer
of splanchnic mesoderm. This tissue, therefore, not only covers the
whole developing lobe of the lung and so forms the visceral pleural
lining, but it also covers the numerous branches of the bronchioles and
even lies between the endodermal air sacs or alveoli as an exceedingly
thin layer. The capillaries of the pulmonary circulation course through
this mesodermal tissue and so come into close contact with the
inspired air.
When the pulmonary arteries and veins develop they course through
the mesoderm associated with the tubular bronchioles and their
terminal'^capillary ranlifications surround the alveoli. Thus the blood
in the capillaries may be brought into close contact with the air con-
tained in the alveoli for purposes of respiratory exchange.
The anterior portion of the laryngotracheal groove gives rise to
larynx and trachea. The opening into the larynx, the glottis, is at
first a longitudinal slit. But, by the formation of the epiglottis from a
swelling at the base of the third and fourth visceral arches and from
the two arytenoid swellings at the bases of the fifth arch, the opening
is widened at the anterior end to assume the T-shape characteristic of
the adult glottis. The laryngeal cartilages arise from the fourth and
fifth visceral arches, and the vocal cords from folds on either side
of the larynx.
13
Coelom and Mesenteries

The body cavity or coelom of vertebrates arises by the splitting of
the lateral mesoderm into a somatic (parietal) layer next to.the ecto-
derm and a splanchnic (visceral) layer next to the endoderm. • Cavities
may appear in all three divisions of the mesoderm-; if they occur in
the myotomes, they are known as myocoels; if in the nephrotomes,
they are called nephrocoels;
Neural tube -,^^—^^ " ^ the cavi'ty of the lateral meso-
Axial. •
mesoderm
derm is the coelom or gplanch-
Notochord (myocoel) nocoel (Fig. 12l). In some
Aorta Intermediate forms the three cavities are
mesoderm confluent, but the connection
(nephrocoel)
is temporary and the myo-
Lateral
Gut mesoderm coels soon disappear.* In
(coelom) other forms the myocoels
make a transitory appearance
and are entirely separate
from the other cavities. How-
Fig. 121. Diagrammatic transverse section eêr, in many vertebrates iny-
of a generalized vertebrate to shoV the re- . , i' • •» mi
f ,. ^ 1 J .1 ocoels are never/ formed. The
gions of the mesoderm and cofelom. • -•- -• .
nephrocoels Will be.Considered
in connection with the urogenital organs. The coelom in ampl]ipxus,
in contrast to that of the vertebrates, has a metameric origin from
the ventral portions of the enterocoels,' These unite to form a' single
'chamber by the disappearance of the intervening anterior and pos-
terior walls of the enterocoelic pouches. In the amniotes the split
which constitutes 'the coelom continues out into the extraembryonic
mesoderm, thus giving rise to" the exocoel, or cavity of (the chorion.
The coelom does not extend anterior to the ivisceral arches'. Transitory
cavities have been found in the arches and, indeed, in the head itself,
and these have been interpreted as the remains of a'cephalic «coelom.
It will appear later that these are- more probably the rudiments of
cephalic myotomes. The coelom does not extend into thetail.
194 ^ • .
Coelom and Mesenteries 195
jn the head and tail regions the organs are loosely packed with a
tissue known as ^mesenchyme, instead of lying in a coelomic space.
n was formerly assumed that the mesenchyme originated wholly from
mesoderm, but it has been shown that in the amphibia, at least,
mesenchyme may originate in part from the neural crest (page 263).
goinatopleure and Splanclinoplevire

The somatopleure has already been defined as the outer layer of the
lateral mesoderm together with the ectoderm with which it becomes
associated. Between these two layers there is an invasion of mesen-
chyniatous cells from the dermatomes and myotomes which give rise
to the corium of the skin (see Chapter 18) and to its dermal muscula-
ture (see page 254). The somatic mesoderm lining the outer wall of
the coelom becomes the outer peritoneal lining. The splanchnopleure
is the inner layer of the lateral mesoderm plus the endoderm with which
it is associated. Again, between these two layers there occurs a migra-
tion of rnesenchyme cells which give rise to the splanchnic musculature
and blood vessels; the splanchnic mesoderm itself forms the inner
peritoneal lining of the coelom.
The Mesenteries
In all the 'Vertebrates, the coelom is divided for a time into right
and left halves .by sagittal partitions above and below the alimentary
canal,'known'as the dorsal mesentery and the _ventral meseritery,
respectively. These are formed by the convergence of the right and
left shefets of splanchnic mesoderm above and below the digestive tube
and the subsequent fusion of these sheets in the median line (Fig. 121).
The ventral mesentery disappears posterior to the liver, probably in
connection'" with the coiling of the intestine. The dorsal mesentery
(Fig. 122) persists as the support of the alimentary canal, and fre-
quently becomes subdivided into regions which are named from the
supported organ. Tljus the mesogastrium supports the stomach, the
mespduo'denuhi supports the duodenum, etc. In the formation of the
ventral mesentery, two organs, the heart and the liver, owing to their
ventral position, are; caught between the two converging sheets of
splanchnic mesodermi. I n these regions, therefore, the ventral mes-
entery is divided into an, upper and a lower half. The ventral mesentery
dorsal'to the heart becomes the dprsaf mesocardium, and that part
which is ventral to the heart is the ventral mesocardium (Fig. 1234).
Both eventually disappear, and the heart, as it increases in size and
complexity,, is supported by the large blood vessels which issue from it.
In'the region of the liver, the dorsal half of the mesentery becomes
196 Coelom and Mesenteries
Esophagus Spinal cord
Pericardial cavity Dorsal mesocar-

dium
Ventricle of heart
Ventral mesocardium Septum transversum

Liver
Ventral mesentery Stomach
B
(falciform ligament) Ventral mesentery
(lesser omentum)
Dorsal mescgastrium
Dorsal pancreas
Mesentery
Mesocolon •
Mesorectum
Fig. 122. Diagram of mesenteries in early iiuman embryo, from left side. ^^4, B,
and C indicate planes of sections shown in Fig. 121. {From Arey, after Prentiss.)
Neural tube
•4orla Nolochord.
Postcar- Aorta'
Dorsal mesentery,
Gut
Peritoneal
cavity
A
Fig. 123. Diagrams of mesenteries in early human jembryo as seen in transverse
sections. Compare Fig. 122." {From Arey, after Prentiss.) •
'- 1 \
\
Coelom and Mesenteries 197
the dorsal mesohepar (mesohepaticum), and the ventral portion is
the ventral mesohepar (Fig. 1235). The primordia of the pancreas
li€ originally in the dorsal and ventral mesenteries, respectively, but
«'ith the rotation of the stomach all are included in the dorsal mes-
entery. The peritoneal supports of the urogenital organs are con-
sidered in Chapter 14. The spleen (see page 233) arises as a
condensation of mesenchyme in the mesogastrium, close to the wall of
the alimentary canal.
Later Divisions of the Coelom

The coelom also becomes divided by a transverse partition into an
anterior pericardial cavity surrounding the heart and a posterior ab-
dominal cavity surrounding the viscera: This structure, the septum
transversum, is a transverse partition which grows out from the bridge
Pleural
cavity
Abdominal
'•cavity
Fig. 124.. Diagrams of the coelom and its divisions. A, Fish. B, Amphibia,
.reptiles, and birds. C, Mammals. {After Kingsley.)
of mesoderm surrounding the vitelline veins where they cross the

coelom en route from the body wall to the heart (Fig. 124A). The
cavities are connected during a large part of the embryonic period by
the pericardioperitoneal canals, which are formed on the ventral sur-
face of the gut where the septum transversum7 converging dorsally
' from the ventrolateral body wall, fails to make contact with the ven-
tral surface of the gut. In the mammals, additional septa develop
behind the lungs and separate the pleural cavities, which contain the
lungs, from the remainder of the abdominal cavity, which is now
known.as the jseritoneal cavity (Fig. 124(7).' The pleural cavities are
separated from each other in the median line by the mediastinum,
which is derived from the mesentery supporting the esophagus and
trachea. • The partition separating the lungs from the viscera receives
musculature from the myotomes and becomes the diaphragm.
198 Co'elom and Mesenteries
TYPE VERTEBRATES
The Frog
The lateral mesoderm splits into its somatic and splanchnic layers
in the tail-bud stage. The spht is most evident on the ventral side
in the region where the heart is forming. From the inner (dorsal) side
of the splanchnic layer at the point where the lateral mesoderm of the
right and left sides unites, a thin layer of cells is proliferated which will
later become the endocardium of the heart (page 234). The splanchnic
layer then grows up around these cells, forming a fold on either side
(Fig. 151).The folds unite dorsal to the developing heart, the inner
layer of each fold becoming the myocardium of the heart and the
outer layer forming the dorsal wall of the pericardial cavity. The line'
along which the two folds meet becomes the temporary dorsal meso-
cardium. The line where the somatic and splanfehnic mesoderm of
right and left sides first met is the origin of the ventral mesocardiunw'
In this instance it can be said to have arisen before the dorsal meso-
cardiuiji. It is also the first to disappear. • • .• •
In the region posterior to the heart the lateral mesoderm on either
side splits (Fig. 209) before uniting at the ventral side of the body. '
This gives rise to the abdominal cavity. The separation af the abdomi-
nal cavity from the pericardial cavity is accomplished by the ingrowth
of shelf-like folds (sometimes called lateral, mesocardia) from the
outer peritoneal layer. These continue inward medially toward the
common cardinal veins (page 232). They are in contact with-the
anterior surface of the mesodermal covering of the liver, from which a
layer is split off to .unite with the peritoneal folds mentioned above,
and so ft)rm the septum transversum. This is not completed until
metarnorphosis. The ventral mesentery disappears as f a s t ^ J l is ^
formed so that the coelom becomes continuous on the ventral side' as
soon as the two split sheets of lateral* mesoderm unite. The dorsal •
mesentery persists in its entirety.
The Chick
In the chick embryo the lateral mesoderm splits very early (Fig.
219). Consequently, as the subcephalic pocket and lateral Sulci'cut
off the anterior region of the chick from the blastoderm at the end of
the first day of incubation, there will be a U-shaped portion of the
coelomic cavity ventral to the fore-gut which is the primordium of the
pericardial cavity. In cross-section this appears as two dilated por-
tions of the coelom, which are known as the amniocardiac vesicles
(Fig. 219). On the inner or splanchnic wall of each in cloê contact
with the gut the heart develops (page 236), and the outer or somatic
wall gives rise to the amniotic folds. As the splanchnic layers are
brought together below the gut, the developing heart is caught between
them and so is temporarily suspended by a dorsal and a ventral meso-
Pericardial Pleuropericardial
cavity membrane
Pleural
cavity Pleuroperitoneal
membrane
Peritoneal Peritoneal
cavity canal
Element from
Pleural body wall
cavity
PleMToperitoneal
membrane
Pericardial
cavity
Septum
Pericardium transversum
1 B"* C
Fig. 135. Diagram to illustrate partitioning of the eoelom. A, Formation of peri-

cardial, pleural, and peritoneal cavities {ajter Arey). B, Development of pleural
cavities (ajter Arey),. _C, Elements contributing to development of diaphragm
(after Broman).
cardium. The venia-al mesocardium disappears immediately, the

dprsal one soon afterward. The septum transversum is formed be-
tween heart and liver. Two lateral folds of somatic mesoderm, the
lateral" mesocardi'a, extending inward to the vitelline veins, and two
closing folds extending from the ventral mesentery to the lateral
mesocardia combine to produce the septum.
Posterior to the septum transversum, the pancreas grows into the
dorsal mesentery (Fig. 240), and the liver into the ventral mesentery.
200 Coelom and Mesenteries
{
The ventral mesentery persists as the gastrohcpatic omentum between
liver and stomach, and as the falciform ligament between the liver and
the ventral body wall. The dorsal mesentery persists in its entirety;
the ventral mesentery disappears posterior to the duodenum.
Man
From the first, the U-shaped pericardial cavity in front of the
anterior intestinal portal is distinguishable from the abdo"hiinal cavity^
inasmuch as it never communicates directly with the extraembryonic
coelom as does the abdominal cavity. As in the chick, its posterior
boundary is coterminous with that of the fore-gut, but it is in com-
munication with the abdominal cavity by means of the parietal
recesses. The recesses are divided frontally by the common cardinal
veins into dorsal and ventral parietal recesses. With the growth of
the geptum transversum dorsally (Fig. 1254), the ventral recesses are
incorporated into the pericardial cavity. The dorsal recesses become f^.
the pleural cavities by the growth of a septum on each side from the
common .cardinal vein anterodorsally to the dorsal body wall arid
posteriorly to the free dorsal edge of the septum transversum. This "
constitutes the pleuropericardial septum (Fig. 125A). The septum
then continues posterodorsaiUy as the pleuroperitoneal septum (Fig.
12bA). Thufe the pleural cavity is separated completely from the
pericardial cavity. As the lungs expand ventrally they push the
pleuropericardial membrane ventrally, separating It-.from the lateral
body wall in the process, and thus enclose the heart in its owji sac, tlie
pericardial membrane (Fig. 1255). The pericardium is, therefore,
derived largely froih tlie pleuropericardial membKme. ' ~ ''
T H E DIAPHRAGM. In the mammal,the thoracic cavity or jiiejircj- '
pericardial cavity .is partitioned off from the visceral cavity ^by'the
diaphragm. This structure has a complicated origin, but in tire main
it is made up of the septum transversum, the pleuroperitoneal septa,,
tissue contributed by the dorsal mesentery, and derivatives of the
lateral body wall (Fig. 125C'). As it develops it undergoes** migration
from its original position in the cervical area to its final position. • At
the level of the fifth cervical somite it receives itsriervous innervati6n
(the phrenic nerve) as well as an invasion of muscle primordia. ^
14
The Urinogenital System

The urinogenital system of the vertebrate is in reality a combination
of two separate systems, namely, the excretory system, whose function
is to eliminate nitrogenous wastes; and the reproductive system, whpse
function is to produce and liberate germ cells. In most vertebrates
they are intimately associated both in embryonic development and in the
use of common ducts and openings for the discharge of their respective
products from the body. The nature of this association is clearly re-
vealed by ,a study of their develop-
ment. Both.sets of organs, arise in the > y Pronephros
intermediate mesoderm or mesomere of
the somites. Their ducts, along with
the intestine, open into the endoderraal
cloaca and are discharged through the
vent, or they may communicate sepa-
rately with the urogenital sinus to be Mesonephros
discharged through the urogenital
orifice. The actual openings in both
are lined with ectoderm.
EXCRETORY ORGANS
The ejj&cretory system of vertebrates Metanephros

is essentially a series of paired nephric Metanephric duct
tubules, developed ih'the intermediate
mesoderm, which remo^ê nitrogenous
wastes from" the blood ,an;d discharge
Fig. 126. Diagram to show rela-
them to the exterior by 2 longitudinal tioiiships of vertebrate excretory
ducts emptying into the cloaca. The systems.
•intermediate mesodeirm in the anterior
part of the body is divided into nephrotomes corresponding to the
somites'.
Three different types of kidneys are found among the vertebrates
(Fig. 126). The first is the pronephros, which arises in the anterior
201
202 T h e Urinogenital System
nephrotomes and is the functional kidney in the larval stages of the
fish and the amphibians. The second is the mesonephros, \^hich arises
from nephrotomes posterior to the pronephros and from the undivided
intermediate mesoderm (nephrogenic cord) behind them. It is the
functional kidney of adult anamniotes and embryonic or fetal am-
niotes. The third is the metanephros, which is the functional kidney
of adult amniotes.
Myocoel
Primary tubuJe
Primary
Coelom .ubule
Nephrostomal
canal
Nepbrostome
Nephrocoel
Primaiy tubule
Pronephric duct
Internal glomerulus
Nephrostomal canal
Nephrostome
External giomerulua
Fig. 127. Diagrams showing three stages in the development of the pronephric
tubule {ajter Felix). • i
The Pronephros
This organ is formed by all vertebrates, but is best developed in free-
swimming aquatic larvae like the tadpole (Fig. 137). It develops
typically as a series of independent tubules from the nephrocbels of
th'e more anterior nephrotomes. The nephrocoels elongate dorsally' to
form tubules, whose distal ends turn caudad and unite with each other
to form the pronephric duct, which grows backward toward the cloaca.
The ventral ends of the nephrocoels open into the coelom by means of
openings, the nephrostomes, lined with long cilia. Typically each
nephric tubule is associated with a capillary net from the dorsal aorta
(Fig. 127). The capillary net is called a glomerulus, which with its
Excretory Organs 203
nephric tubule forms the excretory unit known as a nephron. Two
types of glomeruli are formed. The external glomerulus is a knot of
capillaries pushing into the lumen of the nephrocoel and hence forming
a sort of primitive Bowman's capsule. The internal glomerulus is a
knot of capillaries contained within a Bowman's capsule formed by
invagination of the dilated prox-
imal end of a secretory tubule. Mesonephric duct
Both types are connected with
the dorsal aorta. The pronephros Primordium of.:-.
mesonephric tubule
exists as a functional unit only
during embryonic and larval life,
and it is generally believed that
it has no 'excretory function in
higher vertebrates. In alhverte-
brates it degenerates during the
development oi the mesonephros.
Mesial
side
The Mesonephros
The. mesonephros, like the

pronephros, is developed-by all
vertebrates, i t becomes the adult
kidney of the artamniotes, but
in the amniot'es it is functional
only during the, embryonic and
fetal period. Portions of the
mesonephros become associated
witii the reproductive organs of
the adult. Bowman's
In the lower vertebrates the capsule
Glomerulus
mesonephros develops in part
like the pronephros as a series of P
segmental nephrocoeleg, but only Fig. 128. Diagrams showing four stages
in the nephrOtomes irnmediately in development of mesonephric tubule
{from Arey, ajter Felix).
posterior to those containing the
pronephric tubules. Iârther back the intermediate mesoderm is in the
form of an unsegmentejd nephrogenic cord... From this material the pos-
terior mesonephric tubules develop but in a manner similar to that which
occurs in the higher vertebrates. Nephrocoels do not appear, but the
nephrogenic cord breaks up into a series of clumps of cells which are
the primordia of the mesonephric tubules. These clumps elongate first
of all to form a solid cord. Later the cord becomes S-shaped and
hollows out to'form a tubule "(Fig. 1.28). It joins the former pronephric
204 T h e TJrinogenital System
duct, which has grown back to the cloaca. After the degeneration of'
the pronephric tubules the duct is known as the mesonephric or
AVolffian duct. At the hollow proximal end of each mesonephric tubule
an invagination occurs, producing a double-walled cup or Bowman's
capsule. A glomerulus formed by a knot of capillaries connected to
the dorsal aorta develops in each of these. Nephrostomes are formed
only in the more anterior and earlier developed tubules of the lower
vertebrates, but these do not persist.
An important difference between the pronephros and the meso-
nephros lies in the fact that the number of nephric tubules in each
nephrotome is greater in the mesonephros. These arise by the con-
striction of the posterior median part of each mesonephric tubule into
• a small vesicle which gives rise to a secondary tubule; each of these
tubules acquires a glomerulus (and in lower vertebrates a nephro-
stome) at the proximal end. The connection of these secondary
tubules with the Wolffian duct, however, is attained by an evagination
from thp duct itself, which grows out as the collecting duct to meet the
developing secondary tubule. From these secondary tubules, tertiary
ones bud off and develop in like manner, acquiring connections with the
collecting duct through an evagination of this canal. As many as 8
tubules may be formed in a single segment by this process of budding.
This complexity is greatest at the posterior end of the mesonephros.
In the amniotes, the mesonephros (except for that portion associated
with the genital organs) disappears after the metanephros has been
formed.
The Metanephros ^
The metanephros is the functional kidney of adult amniote^' It is
probably equivalent to the posterior portion of the mesonephros of the
anamniotes, which it resembles greatly in its organogeny.
The region in .which the metanephros arises^ like that in which~ihe
earlier kidneys are found, is the intermediate mesoderm. However,
in the posterior region of the body it is never segmented into 'separate
nephrotomes and forms a mass of non-segmented nephrogenous tissue.
The first indication of formation of the metanephros is the appearance
of an evagination from the dOTsal_surface of the mesonephric duct-near
the point at which the latter enters the cloaca. This evagination grows
dorsally and then turns forward to become the metanephric duct, or
ureter, in much the same manner as the collecting ducts of the meso-
nephros arise. The metanephric duct then branches and sends out into
the nephrogenous tissue evaginations which increase in length and
branch repeatedly to form the collecting tubules of the metanephros.
Excretory Organs 205
Around the distal end of each tubule, a small mass of the nephrogenous
tissue condenses and acquires a lumen like the nephrocoels of the
pronephros arid mesonephros (Fig. 129, 1, 2). These structures
elongate to form the secretory nephric tubules which later fuse with the
Fig. 129. Diagrams to siiow .origin and development of metanephric tubules.

Collecting tubule in oentev, secretory tubules to right and left; the one on the right
relatively more advanced. {From Arey, ajter Huber.)
collecting tubules just described (Fig. 129, 3, 4). At the end of each
tubule a double-walled cup or Bowman's capsule develops for the
reception of a glomerulus, which is a capillary network from an arteriole
of the renal artery (Fig; 129, 5). The metanephric duct at first
empties into the cloaca by way of the mesoneph'ric duct, from which
it arose. In later development it acquires a direct connection of its
own to the urinary blaidder.
The manner-of development of the metanephros makes clear how the
gross structure of the kidney is established. Its general arrangement
into cortical and medullary portions is related to the fact that most of
the collecting tubules are arranged somewhat radially in the center and
so form the bulk of the medulla,-whereas the secretory portions and
206 The Urinogenital System
glomeruli are located near the periphery and so form the cortical area.'
The pelvis of the kidney represents the cavity produced at the terminal
/Kidney
><Bladdcr
Urethra
'Urachus
^Placcntar
^cotyledons-''
Fig. 130. Diagram to show relations of urinary bladder, urachus, and aliantois in,
fetal calf (from Windle).
Urachus \\/'Kidney,
'Bladder'
Urethra
Placenta
Fig. 131. Diagram to show relations of urinary bladder to urachus and. aliantois in
human fetus (from Windle).
end of the ureter at its first division, and the calyces are derived from
the first set of tributary channels opening into the pelvis. The renal
Reproductive Organs 207
'pyramids are the more-or-less conical- or pyramidrshaped clusters of
collecting tubules converging-toward the pelvis.
The Urinary Bladder
This structure takes its origin as a sac-like evagination from the
floor of the cloaca and is therefore lined with endoderm. The meso-
nephric ducts of the amphibia discharge their contents into the cloaca
directly above the opening of the bladder but have no direct con-
nection with it. In birds and inost reptiles which have no urinary
bladder, the portion of the mesonephric duct posterior to the point
where it joins the metanephric duct is drawn into the wall of the cloaca
so that each of these ducts opens into the cloaca separately,^ The
region of the cloaca into which the metanephric ducts empty is known
as the yrodeum. It is from the floor of this region of the cloaca that
the allantois originates in the early embryo.
In mammals the proximal part of the cloacal evagination which
gives rise to, the allantois is called the vGsico-urethral primordium.
From this, portion the urinary bladder is developed; the distal portion
becomes the allantois. Connecting the urinary bladder and allantois,
and running out into the. body stalk, is a constricted passage (Figs.
130, 131") known as the urachus. /The connection of the base of the
urinary bladder to the urinogenital sinus becomes the urethral During
the growth of the' bladder the terminal portion /of the mesonephric
duct is incorporated into, it so that both mesonephric and metanephric
ducts empty into it. As the bladder enlarges the metanephric ducts
retain their connection with it and the mesonephric ducts shift back-
ward so that they regain their connection with the cloaca and enter the,
clodca posterior to the mouth of the bladder. Meantime a frontal
wedge of mesoderm grows -across the cloaca dividing it into a dorsal
portion, the .rectum, and a ventral region, the urogenital sinus. The
history of this urogenital, sinus will be considered when the reproduc-
tive organs have been discussed.
REPRODUCTIVE ORGANS
The reproductive organs may be grouped into two classes: (1) the
primary structures, or gonads, in which the germ cells develop; and (2)
the accessory genital^ organs, whose original function is the discharge
of the germ cells from the body.
The Gonads
The gonads consist of the germ cells and the subordinate tissues,
blood vessels, nerves, connective tissue, etc., which make up a large
part of these glands. In Chapter 3 it is shown that the primordial
germ cells may first appear in the endoderm of the gut wall and thence
migrate by way of the splanchnic mesoderm, dorsal mesentery, and
peritoneum to their definitive position as a thickening on the veiitro-
mesial side of the mesonephroi. This thickening is called the genital
ridge (Fig. 132S). A considerable body of evidence has accumulated
indicating that germ cells may also arise Irom the epithelial cells of
the genital ridge itself.
The genital ridge is invaded by mesenchymal cells, and projects into
the coelomic cavity. The anterior and posterior ends of the ridge
degenerate, and the middle portion enlarges and is separated by a
Glomerulus
Wolffian
duct
MuUerian
duct
Interrenal
•onephric
tubule
Follicle
Fig. 132. Diagrams to show early development of the gonads in transverse sec-
tions. A, Testis. B, Genital ridge. C, Ovary. {Ajter Coming.)
longitudinal groove from the mesonephros so that it hangs in" the

coelom suspended by a fold of the peritoneum, known as-the mesor-
chium in the male or the mesovarium in the female. The definitive
germ cells have by this time become transformed into gonia Chapter ,
3), and the germ glands are known as gonads. • '
Within the gonads, the gbnia lêcome arranged in clustere-~in a '
characteristic manner, close to the germinal epithelium. Tubular out-
growths from the nephric tubules of the mesonephros grow in, toward
these groups of cells. The later history of ihe gonads differs in the
two sexes. _. " f
TESTIS. In the male, the clusters of spermatogonia become irregular
cords of cells. Later as the animal approaches sexual maturity the
cords develop a lumen and so form tubules which connect with the
. tubules growing in from the mesonephros (Fig. 132A). The testicular
portions of these canals are the seminiferous tubules, the nephric por-
tions, the efferent ductules of the testis. The walls of the seminiferous
tubules are composed of sperma^togonia and cells in various stages
of spermatogenesis, as well as Sertoli cells which act as nurse cells
for the developing sperm. Between the tubules lie partitions of
mesenchyme, which make up the stroma of the testis and contain the
interstitial cells. These are thought to be concerned with the forma-
tion of the male sex hormone. I t is because of the presence of these
cells that the testis is sometimes spoken of as the "interstitial gland."
I t is now well established that the testis secretes a "male" hormone.
Eventually, the tubules become-separated from the surrounding germi-
SwSJfSiS
-Tunica externa
•m
Mii -Tunica interna
Mim —Straiiim granuhsum
CumuUts aophortis Ovum
Fig. 133. Section of human ^ vesicular (Graafian) follicle {Irom Arey, ajier
Prenliss).
nal epithelium by the development of a mesenchymatous layer which

forms a white connective tissue investment called the tunica albuginea.
OVARY. In the female, the nests of oogonia become separate follicles
(Fig. 132C) which never attain connection with the mesonephric
tubules. These tubules consequently degenerate. A follicle consists
of a single oogonium surrounded by follicle cells', which may be com-
pared to the Sertoli cellsi of the male. In the mammalian ovary the
primai-y follicle is greatly enlarged to form a vesicular (Graafian)
follicle (Fig; 'ISS), which protrudes from the surface of the ovary.
The follicle cells multiply and secrete a follicular fluid which separates
the outer wall (stratum granulosum) from the egg and the layer of
follicle cells immediately surrounding it. The follicular cells form a
hillock, the cumulus odphorus, projecting into the cavity of the follicle
210 The Urinogenital System
and supporting the egg in the cavity of the follicle. When ovulation
takes place the wall of the follicle is ruptured, and the egg, still sur-
rounded by its investment of persistent follicle cells, now known as the
corona radiata (page 38), is washed out with follicular fluid. After,
ovulation and fertilization the follicle cells enlarge, multiply, and
secrete a yellow substance, the whole forming a corpus luteum (page
137). The existence of female hormones (page 137) formed in the
ovary is now definitely proved. The tunica albuginea of the ovary
develops much later than that of the testis but is also of mesenchymal
origin.
The Genital Ducts

The sperm formed in the seminiferous tubules of the testis are dis-
charged into the mesonephric tubules and thence make their way into
the mesonephric duct, which accordingly becomes the male genital -
duct. The ova, on the other hand, are discharged directly into the '
cavity of the coelom, whence they are received into a new tube, the
oviduct, by njeans of an opening, the ostium tubae abdominals. The '
mesonephric duct is often called the Wolffian duct; the oviduct is fre- '
quently called. the Miillerian duct. Both ducts appear in every
embryo (Fig. 1344), but the later histories of the two differ according
to the sex. The genital 'ducts of the teleost fish arise in a different
manner, which is beyond the scope of this book.
- T H E WOLFFIAN DUCT. In the male of the anamniotes (Fig. 1345),
the efferent ductules toward the posterior end of the series become .
occluded, leaving only a few at the anterior end still connected to the, _
seminiferous tubules of the-testis and still functional. These lose Iheir
renal corpuscles and shorten greatly. In the amniotes, where- t h ^
metanephros acts.as the functional kidney, this anterior group o'f'~
' efferent tubules becomes the epididymis; the more posterior, non--
functional vestige becomes the paradidymis. .The mesonephric d u c t ^ -
persists as the deferent duct. At the point where the deferent duct
enters the cloaca, th|^« develops a dilation, the seminal vesicle. '
In the female (Fig. 134C), the anterior portion of the mesonephros
persists as the vestigial epoophoron, and the posterior portion becomes
the paroophoron. Traces • of the Wolffian duct sometimes persist in 'v
marnmals as a blind outpocketing from the wall of the vagina known'
as Gartner's canal. . '
T H E MtJLLERiAN DUCT. This canal arises in the elasmobranchs by ,__
the constriction of the mesonephric duct into, 2 tubes, of which tfie
ventral becomes the Miillerian duct; Ihe dorsal tube persists as'the
mesonephric duct. The opening of the MuUerian duct into the coelom,
0
the ostium tubae abdominale, is a persistent nephrostome. In all other
vertebrates, this duct arises independently of, and after the formation
of, the Wolffian duct, a fact possibly correlated with the delayed
functioning of the oviduct as compared with the primary renal func-
tion of the Wolffian duct. In these vertebrates the Miillerian duct is
formed in the mesoderm lateral to the WolflBan duct and grows both
Qv— Appendix testis
Ductus
deferens
Seminal
vesicle
TJtriculus'
prostaticus
K g . •134. Diagrams showing origin and early development of genital d u o t i S ^S' ^> .
Early stage, showing mesoriephros, gonads (male on left, female on rigm), and
ducts. B, Later stage in male, showing in broken lines the structures whidn degen-
erate.' Cf Later stage in female. (After Felix.) A
forward and backward until the abdominal and cloacal openiH^S'-are

established. It i§ not formed until late in embryogenesis. I n the
female (Fig. 134C(), the posterior ends of the ducts are usually dilated
as paired uteri, and may fuse to form a single uterus. In the male
(Fig. 134JB) , the jMiillerian duct degenerates, but vestiges are to be
found even "in thej adult, such as the'"appendix testis situated anterior
to the testis on the dorsal abdominal wall and the utriculus prostaticus
of man, a blind pocket at the posterior end of the vas deferens. These
two structures represent the anterior and posterior ends of the female
duct, respectively.
The External Genitalia
The genital organs so far considered are common to all vertebrates
and are sometimes spoken of as the internal genitalia. External
genitalia are found only in those animals in which fertilization is '
internal. These organs serve the function of transmitting or receiving
the sperm at the time of copulation. Internal fertilization is a phe-
nomenon which has been observed in all classes of the vertebrates, but
it is characteristic of all amniotes.
Although the external genitalia differ in the sexes, they are embry-
ologically homologous. Two types are recognized, viz., duplex and
simplex. In the duplex type,
characteristic of the sauropsids,
sac-like extensions arise on each
side of the inner wall of the cloaca.
In the male these become the •
Labio-scrotal i . • x 'j-i j.
fold hemipenes or mtromittent organ;
Phallus in the female they remain ves- •
tigial.
In the simplex' type, charac-
teristic of mammals, a single
median ectodermal prominence
-n- ,„r T^- . 1 .1 •• arises anterior to the cloacal aper-
I'lg. 135. JJiagram to show the origin mi • • /i-i-
of the mammalian external genitalia t^re. This m the phallus (Fig.
{after Felix.) 135). In the male it enlarges
"•and grows forward, carrying with
it the lips of the urogenital sinus. These fuse on the Aêntral surface,
thus enclosing the urogenital sinus in the shaft of the penis as the
penile urethra; the phallus becomes the glans penis. In the feiAal^^^^
mammal, the phallus becomes the glans of the vestigial clitoris; the
margink of the Urogenital sinus remain open as the labia minora,
which guard the opening of the urogenital vestibule. At the base of the
phalli|i^ is a swelling, the genital tubercle, from which labioscrotal folds
arise on either side of the urogenital opening. In the male they fus^
to form the scrotum, an external sac into which the testes descend; in
the female they remain separate as the labia majora.
1 Adrenal Complex /
Closely associated with the kida*y,aly whether mesoneprfros or meta-|
pephros. is the ndrpppl glnnH This is in reality a complex of 2
endocrine glands which are distinct in the fish and arise from separate
primordia in all vertebrates (Fig. 136). The first component is the
interrenal (cortical) tissue, whi'ch oyiginates in the ititermediate mesp-
derm mesial to the region in whicli tlie mesonephros and genital ridge
ag£e§r. The second component is the suprarenal (medullary, phaeo-
chrome) tissue, which rises from ~
wandering; ectoderm cells. These
originated in the neural crest, were
associated with the cells forming
the sympathetic ganglia (Chapter
19), and finally migrate into a posi-
tion near the developing interrenal
cells. Both suprarenal and inter-
renal cells become arranged in cords
on the ventral surface of' the de-
veloping mesonephros and in close
ass6ciation with its blood vessels. Genital
ridge
In vertebrates which develop a met-
anephros the suprarenal and inter-
renal components become closely
associated to form a single adrenal
gland^ Each component, however, Fig. 136. Diagrams' to show the origin
produces its own hormone, epineph- of the suprarenal and interrenal com-
ponents of the adrenal gland (after
rin from the suprarenal component,, Corning).
cortin from,the interrenal.
.TYPE VERTEBRATES,
The Frog
• PRONEPiiRos.. The intermediate mesoderm of the developing frog
is atypical. In stage 16 the intermediate mesoderm has lost its attach-
ment to the lateral mesoderm, and, retaining its attachment to the axial
mesoderm, is growing out between the lateral mesoderm and the e'cfo-
derm. In the anterior region it is divided into nephrostomes corre,-*
spending to the somites to which they are_ still attached. Tê
longitudinal' bulge on either side of the embryo so produced is known
as the pronephric shelf. In later development the nephrotomes unite
to form a nephrogenic cord and lose their connection with the somites.
Later they acquire a new connection with the lateral mesoderm, which
makes the nephrogenic cord appear to arise from the somatic layer of
the lateral •mesoderm (stage 17). Cavities appear in the nephrogenic
cord' about the tinie the lateral mesoderm is split into somatic and
splanchnic layers. These cavities unite to form a pronephric duct;
pronephric tubules (Figs. 209, 210) develop in the region correspond-
ing to somites II, III, and IV. These acquire nephrostomes in stage 20.
The pronephric tubules elongate greatly and are contorted into coiled
structures that push into the cardinal veins. From the dorsal aorta a
vascular outgrowth, the glomerulus (Fig. 215), on either side extends
to the developing pronephros. The developing lungs projecting into the
coelom later form shelves which cut off the portions of the coelom into
which the nephrostomes open as the pronephric chambers. At stage 25
Nephrostome I
Opening
into cloaca
Fig. 137. Excretory system of ll-mni. liana pipiens embryo, frorn a wax plate
reconstruction, ventral view, X40 (prepared by Afarian^. James-and Phyllis T.
Mrazek). ,
the pronephros on either side of the body is large and conspicuous

(Figs: 137, 216). A projection from the roof of the cloaca arises to
meet the advancing pronephric ducts and seems to have moved forward
by stage 25 so that the pronephric ducts are actually recurved before
entering the cloaca. t^^_
MESONEPHROS. Mesonephric tubules appear in 'the nephrotomes
(somites VII-XII). These ha-ê nephrostomes in eatly larval life; but
,at tho time the pronephroi degenerate the portion 'of each mesonephric
tubule next to the nephrostome (peritoneal canal) breaks away from
the remainder of the tubule and fuses with the posterior cardinal
vein. The mesonephros is the functional kidney of the adult, and the
Wolffian duct, therefore, functions as the ureter.
URINARY BLADDER. This arises as a ventral evagination from the
floor oi the cloaca during metamorphosis. The mesonephric ducts
never acquire a direct connection to the bladder but open directly
above it.
T H E GONADS. The genital ridges arise soon after hatching. Sex
can be distinguished at the time when the embryo is about 30 mm.
Mesonephric tubules
Interrenal cells
Suprarenal cells
Postcaval vein
Efferent vein
Fig. 138. Section through mesonephros of 55-mm. frog tadpole {Rana pipiens) to
show interrenal and suprarenal cells, X660 (prepared by Mary H. Phillips).
in body length. The anterior portion of each genital ridge degenerates,

and becomes a fat h'^dj.. Seminiferous tubules are formed in the testis
and follicles in the Ovary. The mature follicle is not of the Graaffian
type. Hermaphrodites have been recorded. ~
T H E GONODUCTS. The Wolffian duct in the male acquires connection
with the testis by means of some of the mesonephric tubules (vasa
efferentia) and serves as the deferent duct as well as the ureter. A
seminal vesicle is formed. A rudimentary Miillerian duct also appears
in the male. " In the female the Wolffian duct functions solely as a
ureter whereas the, Miillerian duct becomes the oviduct. Bidder's
organ, a structure attached to the ovary, has been compared to the
epoophoron of mammals, because of its origin from mesonephric
tubules.
216 ' T h e Urinogenital System
ADRENALS. These arise from suprarenal and interrenal cells, which
accumulate around the blood vessels on the ventral side of the meso-
nephros (Fig. 138). The brown color of the suprarenal cells distin-
guishes this area as a yellow-brown streak on the mesonephros.
The Chick
PEONEPHROS. About 12 pronephric tubules.arise (somites V-XVI),
beginning on the second day of incubation. Nephrostomes are formed,
Somite
number
XXV
XXVI
XXVII
: XXVIII
XXIX
XXX
XXXI
•. XXXII
Metanephric xxxm
duct '
Fig. 139. Reconstruction of metanephric primordium tn 6-day chick embryo
(after Lillie, from Schreiner).
but glomeruli do not appear until the third and fourth days of incuba-
tion, at which time the pronephros is degenerating.- Jhe pronephrit
duct arises at the ninth somite. !
1
#
The development of the pronephros in the chick is very irregular; the
number of pronephric tubules varies in different individuals or on the
two sides of the same embryo; the tubules are often represented by solid
cords; the number and size of the nephrostomes vary; and the whole
appearance is that of a vestigial organ without a urinary function.
MESONEPHROS. Mesonephric tubules (Figs. 139, 234) arise from the
intermediate mesoderm between somites XII and XXX, the more
anterior of which develop nephrostomes. The main part of the meso-
nephros, however, arises between somites XX and XXX, where the
continued growth of the tubules causes the projection of this region
into the coelom as the Wolffian body. I t begins to degenerate on the
eleventh day.
METANEPHROS. An evagination from the mesonephric duct com-
parable to the collecting tubules of the mesbnephros grows out into
the nephrogenic region of the intermediate mesoderm during the fourth
day of incubation. This diverticulum gives rise to the ureter, which
branches niany times; to form a great number of collecting tubules.
Meantime in the nephrogenous tissue between somites XXV-XXXIII
a number of tiny vesicles appear. These elongate and finally become
the secretory tubules which unite with the collecting tubules. Each
secretory tubule is supplied with a glomerulus and a capillary network.
URINARY BLADDER. NO urinary bladder is formed. The cloaca per-
sists^ and three regions are recognizable (page 185), of which the
urodeum receives the urogenital ducts.
GONADS. The genital ridge arises with the mesonepliros as the uro-
genital ridge. • On the mesial side of this the anterior region gives rise
to the gonad. Sex is not distinguishable until the seventh day of
incubation. In the female, the right ovary develops only for a short
time and ultimately degenerates.
The ovarian follicles of the persistent left ovary enlarge greatly prior
to ovulation bi(t never assume the vesicular condition characteristic
of mammaljan Graafian follicles. ~
GoNODucTS. ThelWolffian duct (Fig. 139) becomes the deferent duct,
connected with the testis by vasa efferentia which form the epididymis.
The persisting mesonephric tubules of the posterior region of the
mesonephros form aiparadidymis. In the female a vestigial epoophoron
and paroophoron represent these bodies respectively. The Miillerian
ducts degenerate iuithe male without ever acquiring a cloacal exit. In
the female the right Miillerian duct disappears and the left becoines
the oviduct. It undergoes extensive localized specialization. The
shell gland, for example, is formed on the twelfth day of incubation,
but it does, not open into the cloaca until the hen is 6 months old.
EXTERNAL GENITALIA. Generally no external genitalia are formed,
although in some other birds such as the duck and ostrich a penis is
developed in the male.
ADRENAL GLANDS. This gland arises from distinct suprarenal and
interrenal components, which later become intermingled in a structure
known as the suprarenal capsule embedded in the anterior portion
of the kidney near the postcaval vein and gonad.
Man
PRONEPHROS. Between the third and fourth weeks of development
pronephric tubules arise in somites VII-XIII, develop nephrostomes
and glomeruli, but degenerate
©.—LCT4 oj somite 14
rapidly.
Degenerating meso-\
nephric tubules \ „^ MESONEPHROS. The first
mesonephric tubules rise in
the region posterior to the
Mesonephric duct
degenerating 'pronephros, that
is, . in somite .XIV. At the
height of their development
(Figs. 140, 250-252) they ex- _
Tubule
tend from somite I X to so-
mite XXVI. The intermedi-
ate mesoderm is unsegmented
posterior to somite X, and the
tubules arise from solid balls
of nephrogenic tissue which
later acquire cavities and ,
elongate to join the old pro-
nephric duct. There is no^
constant number of tubules "
Level of per somite region, but at the
somite-26 end of the first month there"
are about 30 tubules in each
mesonephros. The collecting
Ureter Metanephros portion of each tubule arises
Rectum from the original vesicle and
'not from the pronephric duct,
as seems to be the case in the '
Mesonephros in human embryos, chick. In the second month
embryo, X45 (after Shikin'ami). of development the more ,anr
B, 10-mm. embryo, X35 {after Felix). (From
terior tubules disappear while
Arey.)
new ones are being formed
at the posterior end. In this way, although about 80 pairs of tubules ^
are formed in all, only about 30 are present at any on^ tiiTie. '-A
glomerulus indents the distal end of each tubule to form a Bowman's
capsule. The mesonephros degenerates except for the structures taken
over by the reproductive organs early in the third month, when the
metanephros is capable of functioning.
METANEPHROS. The definitive kidney arises from a diverticulum of
the mesonephric duct (Figs. 244, 253), which gives rise to the ureter,
pelvis, calyces, arid collecting tubules. The secretary tubules arise
from condensations of non-segmented nephrogenous tissue. These
later become hollow, elongate, and join the collecting tubules. Each
has its glomerulus.
URINARY BLADDER. The bladder arises, from the floor of the cloaca
at the base of the rudimentary allantois with which it is connected
by the urachus (Fig. 131). The region of the cloaca from which the
bladder grows is cut off from the rectum by a urorectal septum, leaving
the mesonephric ducts connected to the enlarging bladder. These ducts
are incorporated into the bladder wall as far back as their junction
with the metanephric ducts. The metanephric ducts maintain their
openings- into the bladder (Fig. 141), but the mesonephric ducts are
carried back to enter into the urogenital sinus once more. The urinary
bladder opens into the urinogenital sinus by way of the urethra.
GONADS. The genital ridge arises on the mesial side of the meso-
nephros during the fifth, week. Sex is not distinguishable until after
the seventh week. Earlier the developing gonad' might be thought of
as being in an indifferent condition, for both the .cortical region which
will give rise to ovary and the medullary region which will give rise
to testis are present.
GoNODueTS. Each Wolffian duct functions as a deferent duct, ,and
both epididymis and paradidymis are formed, as well as a seminal
vesicle at" the distal end. Tn the female, epoophoron and paroophoron
ar,e .formed; and the terininal portion of the duct itself may persist as
Gartner's canal. The Miillerian ducts become the uterine tubes, which
unite at their posterior ends to form the uterus and vagina. The
vagina open's into the urinogenital sinus and is partially closed by a
semicircular fold of jits lining which forms the hymen, where it enters
the urogenital sinus.' In the male, vestiges of the anterior end of each
Miillerian duct persist as the appendix testis; the posterior end is
represented -by thei rudimentary utriculus prostaticus. The genital
ducts, i.e.. Wolffian or Miillerian ducts, empty into the urogenital sinus
posterior to the urethra. In the male the urogenital sirius is incor-
porated into the penis as the penile urethra.
GLANDS. In connection with the reproductive tract a number of
glands are developed in man as in most other mammals. In the male
paired saccular diverticula, the seminal vesicles, are produced from
the vasa deferentia near their openings into the urogenital sinus. An-
other pair of glandular structures, the prostate glands, arise as
evaginations of the wall of the sinus just at the base of the urinary
bladder. The bulbourethral (Cowper's) glands are produced as out-
Hind-gul
. Bind-gut I Mesonephric
AUantots 'rduct
Meta-
nephros
AUantots'
Cloaca' Cloaca
Cloaeal membrane
Tail-gut,
Mesonephric duct
bladder 1_ Ureter Bladder „ , Rectum
Coelom / , , , . ,
Mesonephric ducts
Allantois
—Rectum *
Urogenital / Pelvic Meta-
sinus \Phalhc.
nephros
Cloaeal^ —Cloaca
membrane
>
Fig. 141. Models showing. relation, of urogenital ducts to cloaca in human
embryos. A, 3.5 mm.; B, 4 mm., X50 {both ajter Pohlman). C, 8 mm., XSQ.
D, 11 mm., X25. {after Keibel). {From Arey.)
> i /
growths of the wall of the sinus. Both prostate and Cowper's glands
are endodermal in origin. In the female the vestibular glands of
Bartolin are developed in a manner similar to Cowper's glands and
open into the urogenital sinus. '
ExTEBNAL GENITALIA. These structures are of the typical mam-
malian form (page 212^. _. '
ADRENALS. This gland, often called the Suprarenal, arises from inter-
renal and suprarenal components, of which the interrenal forms the
cortex and the suprarenal the medullary portion. Both are included
in a single capsule, which in the second month is almost as large as
the metahephros and even at birth is a third the size of that organ.
HOMOLOGIES OP THE REPRODUCTIVE ORGANS

Male Indifferent Female
Testis Gonad Ovary
Epididymis Mesonephric tubules Epoophoron
Paradidymis Paroophoron
Ductus deferens Mesonephric (Wolffian) Gartner's canal
duct
Appendix testis Miillerian duct Uterus and tube
Prostatic utricle Vagina
Glans penis Phallus Glans clitoridis
Lips of urogenital aper- Labia minora
ture
Scrotum Labioserotal swellings Labia majora
15
Blood Vascular System

The vascular system is mesodermal in origin. It consists of several
distinct elements, namely: (1) the blood, composed of corpuscles
floating in a fluid matrix, the blood plasma; (2) the heart, a muscular
pulsating organ by means of which the blood is kept in circulation;
(3) a system of tubes or blood vessels by means of which the blood is
distributed to, and brought back from, various parts of the body of
the animal.
As an" adjunct of the blood vascular system it is also necessary to
consider the lymphatic system—a series of special channels by means
of which the- plasma which has escaped into the tissue spaces is'
I picked up and returned to the blood stream.
Blood island Ectoderm Somatic mesoderm Splanchnic mesoderm Blood vessel Blood cell.'-
Yolk Endothelium Entoderm fused to yolk

B
Fig. 142. Diagrams showing three stages in the development of a capillary from
a blood island based on transverse sections of the area vasoulosa in a 7-somite
chick (from Arey).
, ORIGIN AND DIFFERENTIATION OF BLOOD

The first indication of the development of the vascular system is the
appearance of cell aggregates called blood islands in the splanchnic
mesoderm, associated with the ventral surface of the yolk mass as in
222 «•• • 1
Origin and Differentiation of Blood 223
the frog, or in the extraembryonic mesoderm of the yolk sac in
telolecithal eggs (Fig. 142).
Shortly after the blood islands are formed they are converted into
hollow vesicles by the accumulation of fluid within them. This sepa-
rates an inner group of cells, the hemoblasts (Fig. 143) or primitive
Fig, 143. Stages in the development of human red blood corpuscles, a, Hemo-
blasts.. b, Megaloblasts (anamniote type), c, d, Normoblasts (sauropsid type).
e, Normoblasts in process of becoming j , erythrocytes. {From Arey, ajter
Prentiss.)
/
blood cells, 'from an outer layer which forms the endothelial lining
of the vesicle. By the anastomosis of neighboring vesicles a series of
irregular channels is formed in the splanchnic mesoderm. These
represent the beginnings of the extraembryonic vitelline vessels. In
addition to the blood islands, hemoblasts may also originate from cells
forming the walls of capillaries and from mesenchymal cells in regions
where the capillary network is developing.
The Blood Corpuscles

The erythrocytes, or red corpuscles, are distinguished by the pres-
ence of hemoglobin, which gives them their color. In anamniotes these
corpuscles have large vesicular nuclei with granular chromatin and a
distinct cell membrane. In the Sauropsida, the red corpuscles have
small compact nuclei. The mammalian erythrocyte is distinguished
by the absente of tlie nucleus in the adult, but, before the adult con-
dition is reached, a succession of types appear as follows: (1) the
anamniote-type or rhegaloblasts, which are large cells with a large
vesicular nucleus; i(2) the sauropsid type or normoblasts, which have
a smaller nucleus; (3) the mammalian erythrocyte, which is produced
224 Blood Vascular System
by the extrusion of the nuclei from the blood cells of the sauropsid
type (Fig. 143) and the development of hemoglobin.
The leucocytes, or white blood corpuscles, are of many different
types. It is sufficient here to recognize two kinds, viz., the granulocytes,,
which are classified on the basis of distinctive cytoplasmic granules,
and the lymphocytes, which lack granules. Although the matter can-
not be considered definitely settled, most embryologists consider that
all type& of corpuscles arise from hemoblasts and that the large
lymphocytes are nearest the ancestral type.
Hemoblasts become differentiated into the various types of blood
corpuscles in the following blood-forming centers: (1) the yolk sac;
(2) the embryonic capillaries;' (3) the liver, spleen, thymus, and
lymph glands; (4) the bone marrow. In the adult the lymph glands
give rise to lymphocytes, and the hf>ne marrow or myeloid tissue to
all types of corpuscles. -^
DEVELOPMENT OF BLOOD VESSELS

' As has been seen, primitive blood vessels of the vitelline circulation
are developed in the early embryo by the coalescence of blood islands
on the yolk sac. In addition, as the embryo becomes larger "and the
system becomes more complex," extension' of the primitive blood
channels takes place within the body of the embryo. This is accom-
plished by the development of an irregular and somewhat uncertain
network or pl'ekus of capillary channels which open up in the tissue
spaces of the; mesenchyme of the area being vascularized. These
become lined with endothelial cells developeid from the surrounding
mesenchyme. As the blood flow to such an area becomes more firmly
• established, the original plexus of capillaries is simplified by
elimination of many of the smaller vessels and the enlarging of a more
direct channel through the region. A very^good example of this situ-
ation is seen in the development of the main vessels df the limb bud,
e.g., the iliac artery. Although this explanation of the origin" of blood
vessels is generally accepted, ft has also been suggested that the ex-
tension of ,many channels is a result of the direct outgrowth of
primitive endothelial tissue.
i
Establishmient of the Basic Vascular Pattern of the Embryo
The first embryonic blood vessels (Fig. 144) are the vitelline
(omphalo-mesenteric) veins which appear at the ventrolateral margins
of the fore-gut. These vessels unite in the. region of the anterior
intestinal portal with the developing hearf, /torn the anterior ends of
Development of Blood Vessels 225
which the ventral aortae arise. These latter vessels course forward
ventrally to the anterior end of the fore-gut where they bend up
Vitelline artery
Vitelline
area vasculosa
Aortic arches
I-VI Caudal artery
Internal
carotid
artery
External Internal carotid

carotid
artery
Common cardinal vein
•Vitelline vein
Posterior cardinal vein
Vitelline artery
Fig. 144. Diagrams to show fundamental plan of embryonic circulation. A,

Early stage in. side view. B, Later stage in side view. C, Same from above,
I , aortic roots pulled apart.
I •
dorsally around the pharynx in the mandibular arch on each side as
the paired first aortic arch. They then continue backward dorsal to
the gut as the dorsal aortae. The primitive dorsal aortae, each of
which is later known as a radix of the aorta, fuse at a very early stage
about halfway back in the body to become the dorsal aorta. From
this vessel branches are sent to each myotome and to the vitelline •
circulation. The posterior ends of the vitelline veins fuse in small-
yolked forms, such as the frog, to form a subintestinal vein which con- •
tinues back to the tail. In large-yolked forms like the chick, the
vitelline veins are widely separated and brought into connection only
by the sinus terminalis, which makes a circuit of the outer margin of.
the area vasculosa. The vitelline veins are the ventral venous channels
and constitute the splanchnic veins. A dorsal set of somatic vessels
soon originates independently within the body of tke embryo. The
first of these to appear are the paired anterior cardinal or precardinal
veins draining the head. A similar pair, the posterior cardinal or
postcardinal veins, arise in association with the nephric region. These,
however, do not discharge their contents directly into the heart but
into the anterior cardinals. The portions of the original anterior
cardinals proximal to this juncture with the posterior cardinals are
now called the common cardinal veins or Cuvierian ducts
Origin and Development of the Heart

The heart takes its origin from the splanchnic layer of mesoderm •
ventral to the gut and associated with the region where the fore-gut
opens out into the mid-gut by way of the anterior intestinal portal or
its equivalent. The mesoderm^ involved may not be originally present
in this position (as in man) but soon attains it by the shifting which
accompanies remodeling of the developing embryo (Fig. 155). ,Thus
the endodermal wall of the anterior intestinal portal is paralleled on
each side by a layer of splanchnic mesoderm. This sheet of tissue _
bulges out on each side into the adjacent (and definitive) pericardial
region of the coelom. At the*same time, "a-group of mesenchymal cells^
separate off the splanchnic layer, wander into the cavity formed by.
the bulge, and there organize into a delicate tube on each side. These
tubes are therefore situated between the endoderm and the. layer of
splanchnic mesoderm. They grow forward side by side into the head /
beneath the gut, and the splanchnic mesoderm, now converging to ' '
form.the ventral mesentery beneath the gut, comes together around,
them to form:
a, The dorsal mesocardium.

b, A heavier outer layer of splanchnic mesoderm which is the primor-
dium of the epimyocardium.
c, The ventral .mesocardium.
\.
Development oi Blood Vessels 227
LATER DEVELOPMENT OF THE HEART. Although the heart is primi-
tively a paired organ, the two primordia soon fuse into a single median
tube by the breakdown of the wall between them. Anteriorly, they
continue forward as paired vessels, the ventral aortae. Posteriorly,
they connect with the vitelline veins, and later, with the common
cardinal veins as well. Around the endocardial tubes there develops
a coat of muscle fibers which becomes the myocardium. Outside this
is a covering of splanchnic mesoderm forming the epicardium, which
is continuous with the lining of the part of the coelom surrounding the
K^
Fig. 145. Diagrams to show early stages in development of vertebrate heart.

4, Paired .heart tubes. B, Same, fused. C, Primary flexure. Z), Later "S" stage.
, E, After a,nterodorsal displacement of atrium.
heart.- This space will later be cut off by the septum transversum to
form the pericardial cavity. The dorsal and ventral mesocardia sus-
pend the heart in this cavity for a time but soon disappear.
The' later history of the heart is one of growth and subdivision into
special chambers. Because the local growth of the heart is limited,
by the anterior and posterior walls of the pericardial cavity, and by
the^ mesocardia which suspend it, any extension in length must be
accompanied by coiling. Experiments have shown, however, that the
coiling of the heart jis due to intrinsic causes and is not conditioned
by the space at its' disposal. The primary flexure of the heart is
toward the right, thus qhanging the shape of the organ from a straight
tube to a C-shaped one. Further growth results in the twisting of the
heart into the shape' of an S. Still later, the original posterior loop
of the S is pushed iorwatd and dorsad so that it comes to lie dorsal
to the morphologically anterior end (Fig. 145).
The original chambers of the heart are produced by local dilations,
of whiqji the most posterior is the sinus venosus; next to this is the
228 * Blood Vascular System
atrium; in front of this, the ventricle; and finally, most anteriorly, the •
bulbus arteriosus. The sinus is the chamber into which the primitive
veins enter; the atrium is a thin-walled distensible chamber; the
ventricle is a thick-walled, muscular, pulsating pump; and the bulbus
is the chamber from which the blood enters the JDrimitive arteries.
These chambers undergo different changes in the various types of
vertebrates. In fish there is little modification from the original
tubular embryonic plan. In higher vertebrates, however, the most
important modification is a progressive separation of the atrium and
ventricle into right and left halves. The right side receives venous
blood from all parts of the body and transmits it to the lungs for
respiratory exchange. From the lungs the blood is returned to the left
side of the heart and thence conveyed to all parts of the body. This
differentiation reaches its culmination in the birds and mammals.
The partitioning of the chambers of the heart is accomplished by the
•development of a number of septa. The bulbus is divided into the
systemic and pulmonary trunks by the median septum aorticopul-
monale. The ventricle is partitioned into right and left sides' by the
inter\'entricular septum in the birds and mammals. As for the atrium,
a single septum develops in the birds, and two in the, mammals. In
both cases the partition is not completely closed during embryonic life
and a channel, the foramen ovale, persists until hatching or birth.
The Arteries (Fig. 146)

The ventral aortae.ultimately fuse into a single hiedian tube sending^
bra,nches into each of the visceral arches. These vessels, which unite
with the dorsal aortae, are usually 6 in number and are known a^the
aortic arches. Anterior to these the ventral aorta* continue forward
as the external carotid arteries. Similar forward extensions of/the^ .
dorsal aortae constitute the internal carotid arteries. These continue
forward, forming a capillas^ plexus over the lateral surfaces of the—-
fore-brain, and finally fuse beneath the mesencephalon to form the •
basilar artery. This vessel, as indicated below, divides and anasta- •
moses with the vertebrals. In the region of the aortic arches the dorsal
aortae remain separate as the aortic roots (radices aortae). Poste-;
riorly, as has been mentioned, the paired 'radices aortae fuse to formv
the median dorsal aorta. ' I
T H E AORTIC ARCHES. In larvae breathing by means of external
gills, a loop from each aortic arch (see chart, p. 121) grows out into
the gill developing on the visceral arch with which it is associated.
These loops are occluded when the external gills disappear.
In forms with internal gills, each aortip arch breaks up inte capil-
laries in the demibranch and becomes divided into a ventral afferent
branchial artery and a dorsal efferent branchial artery.
In vertebrates with a pulmonary respiration, aortic arches I and II,
in the mandibular and hyoid arches, respectively, disappear. Arch I I I ,
Spinal
Mesenteric
\
Fig. 146. Diagrams to show principal arteries; A, I n side view, B, Cross-section

through mesenteric.
/
Internal External
carotid carotid
Subclavian
RIGHT LEFT
Fig. 147. Diagrams of aortic arches. A, Hypothetical primitive type. B, In

frog. C, In chick. D, In man. (After Kingsley.)
^ i
in the first branclîial arch, persists as the connection between, the
internal and external carotid arteries; the dorsal aorta between arches
I I I and IV disappears. Arch IV becomes the paired systemic arch
(Fig. 1475). In birds (Fig. 147C), arch IV on the left side disappears
along with the remaining posterior portion of the left radix of the
230 '" Blood Vascular System
aorta. In mammals (Fig. 147Z)), that on the right degenerates along '
with the remainder of the right radix of the aorta. Arch V is greatly
reduced and frequently disappears or has, at most, a vestigial and
transitory existence. From arch VI, small vessels, the pulmonary
arteries, grow back to the lungs. The distal portion of the arch VI
between the new pulmonary arteries and the persisting radix of the
aorta is reduced in caliber and is known as the ductus arteriosus. It
becomes occluded and degenerates after birth or hatching in all the
amniotes except some few reptiles.
INTERSEGMENTAL ARTERIES. From the dorsal aortae a series of small
paired intersegmental arteries are given off between the myotomes
(Fig. 146B). Many of these persist as the intervertebral arteries.
The more anterior ones become united on either side by a dorsal
longitudinal vertebral artery. These vertebrals fuse anteriorly with
the basilar artery, which divides behind the pituitary body. The two
vessels so formed unite with the internal carotid on either side. In
the region where the anterior limb buds are developing, intersegmental
arteries grow out into them, giving rise to the subclavian 'arteries.
Similarly, m the region of the pelvic limb buds, intersegmental arteries
give rise to the iliac arteries. In the amniota, the allantoic arteries
grow out from the iliac arteries into the walls of the allantois. These
become so important that for some time it appears as if the iliac
arteries were derived from the allantoic instead of the reverse. The
allantoic arteries, which degenerate at the time of birth, are known
as the umbilical arteries in mammals, as they traverse the umbilical
cord and supply the placenta.
Other important intersegmental arteries become the renal arteries
of the kidneys and the genital arteries of the gonads. ; /
MESENTERIC ARTERIES. F-rom the dorsal aorta, a number of vejikal .
branches, originally paired, but soon fused to become median vessels, .
pass down the dorsal mesentery. They unite with the capillaries-
of the yolk sac, which they supply with blood. Later, some of them
develop branches over the alimentary canal which persist after the' doss
of the yolk sac as the coeliac and mesenteric arteries.
The Veins _ ^
As indicated previously, there'are two primitive venous system's
laid down in the early embryo. In general it ^nay be said that the
cardinal system is modified to-become (or is replaced by) the caval
veins. The vitelline veins are reorganized to become the hepatic-
portal circulation. The allantoic veins in birds or umbilicals in mam-
mals, disappear at hatching or birth, respectively. In addition there
also develop the pulmonary veins draining the lungs. The later historj'
of the vitelline and cardinal veins is one of transformation from orig-
inally paired vessels to more nearly axial ones. Eventually the sys-
tems become so related to the arteries that there is an accompanying
vein for every artery.
HEPATIC-PORTAL CIRCULATION. The vitelline (omphalo-raesenteric)
veins are surrounded by the developing liver (Fig. 148), and within this
organ the original channels are broken up into an intricate capillary
Allantoic
LEFT
Portal
Fig. 148. Diagrams to show three stages in the development of the hepatic-portal
, venous system in man (after Hochstetter).
network. The anterior portions of the veins extending from the liver
to the heart become the hepatic veins. Posterior to the liver they are
thereafter known'as the portal veins. The manner in which the orig-
inally paired .system becomes an axial one differs in the different groups
of vertebrates and is discussed in later paragraphs.
CAVAL CIRCULATION. The primitive cardinal veins are paired, and •
carry the blood from the head past the pronephric region into the sinus
venqsus of the heart. After the appearance of the posterior cardinals
which join them at the anterior surface of the pronephros, the system
has the form of a letter H (Fig. 149.4). The upper limbs of the H
are now known as the anterior cardinals. The cross-bar is represented
by the common cardinals (Cuvierian ducts), and the lower limbs are
the posterior cardinals. The anterior cardinals persist as the internal
jugular veins of the adult. The commoh cardinals unite, or one may
degenerate, so that a,single vessel, known as the precaval vein (anterior
vena cava or pre cava), from the anterior portion of the embryo enters
the heart at the sinus venosus. The posterior cardinals lose their con-
nection with the common cardinals and enter the heart through a new
vessel, known as the postcaval vein (posterior vena cava or post cava) ,-
originating from the hepatics and subcardinals. The details, which
differ in the different classes, are described in later paragraphs. Mean-
time, it may be recalled that the cardinal veins of the embryo are
associated with the excretory organs, from which they return blood to
Anterior,— •
cardinal
C(_j— Coronary
sinus -
Fig. 149. Generalized diagram to sliow relationships of cardinal and caval veins.
the heart. In some cases the posterior portions of these veins convey
blood from the posterior region of the body to the mesonephros, m
which case we may speak of a renal-portal circulation.
T H E PULMONARY VEINS. These veins ,enter the left atriunl and are
new vessels which arise in situ and grow backward from the heart to
the developing lungs. / ' "^ .
T H E LYMPHATIC SYSTEM
This system serves to return to the veins the blood plasma "yvhicb
has escaped from the capillaries (Fig. 150). It contains white blood
corpuscles of the ameboid itype (lymphocytes), which have the power
of making their way through the capillary walls. The lymphatics
apparently originate aa intercellular spaces in mesenchyme, which later
become confluent and acquire a limiting endothelium. Like the blood
vessels, the lymphatic capillaries anastomose and form larger vessels
which drain into the veins. The walls of these Central vessels are often
muscular, and localized areas known as lymph hearts are found. So,
too, there are localized distensible regiqjis called lymph sacs. Sbme of
Superficial lymphatics
Jugular lymph sac
Subclavian lymph sac
Lymph gland
Deep lymphatics
Thoracic duct
Retroperitoneal lymph sac
Cisterna chyli
Posterior lymph sac

Superficial lymphatics Lymph gland /
Fig. 150. Reconstruction Of primitive lymphatic v'essels in- human fetus of 2

months (jroiii Arey, after Sabin).
these becortie lymph glands. The spleen, already alluded to in the

section on mesenteries (page 197), is a hemolymph gland in which both
lymphocytes and erythrocytes are proliferated during embryonic life.
TYPE VERTEBRATES
The frog —
HEART. The heart of the frog (Fig. 151) originates in stage 17 as a
loose clump of cells proliferated from the dorsal side of the splanchnic
layer of mesoderm at the point where the right and left sheets of
lateral mesoderm come together. These cells organize themselves in
the following stage into 2 small vesicles, which fuse shortly thereafter
to form the endocardial lining of the heart. Meantime the splanchnic
layer itself has grown, up around the heart as a fold on either side, the
inner layer of the fold forming the epimyocardial wall of the heart, the
outer giving rise to the outer lining of the pericardial chamber (page
198). Muscle cells appear in the myocardium, and the heart (Fig. 206)
commences to beat in stage 19. The heart is at first a simple tube, but
soon four regions are distinguishable. Commencing at the posterior
end, we find first the sinus venosus, into which the meatus, formed by
the fusion of the vitelline veins, enters. Then comes the thin-walle.d
atrium (Fig, 212), continued'by the muscular ventricle, which in turn
opens into the bulbus arteriosus. This divides to give rise to the ventral
Splanchnic
layer
Endocardial
primordium
Pericardial cavity'
Somatic layer
Sucker
Atrium
Ventricle
Dorsal
mesocardium
Epimyocardium
Eildo'cardium
Outer pericardial
lining
D
Fig. 151. Transverse sections to show origin of the heart'in frog embryos (Rfma
pipiens). A, Stage 17, B, stage 18, C, stage 19, D, stage 21. X35. '' -
aortae. The septum dividing the atrium into left and right atria,
which receive blood froiii the lungs and the rest of the body respectively,
is not formed until after hatching (stage 21). . ,
ARTERIES. The origin of the aortic arches is difficult to distinguish
in sectioned material, and these are first clearly indicated in stage 20
at a time when the circulation of the blood can be seen in the first
gill bud (on the third visceral arch). Studies made with the aid .of
injected specimens indicate that the aortic arches arise as spaces in
the visceral arches. These spaces form ventral twigs (afferent
branchial arteries) of the ventral aortae "and dorsal twigs (efferent
branchial arteries) of the dorsal aortae, respectively. In the gill buds
these twigs unite to form capillary loops. Some writers hav^ de-
scribed a hyomandibular artery anterior to the afferent and efferent
arteries of tlie third arch which courses through the second arch and
supplies the first, but its homologies are still uncertain. Aortic loops
arise in the third, fourth, fifth, and sixth visceral arches. After the
ARTERIES
VEINS
Commissural
Anterior
cerebral Anterior
External "cardinal
carotid
Basilar fe^Si«i^"y"'7
Afferent t ~
branchiate ~-~'
Inferior
jugular
Efferent _ - -
branchials ^^
Common
cardinal
Cutaneous—' — Postcaval
Pulmonary - — Pulmonary
Glomus •^J}J/jJL Pronephric
'/;^S,^^^ sinus
Radix aorta
Dorsal aorta Posterior cardinal
Fig. 152. Plan of circulation in 11-mm. Rana pipiens embryo, dorsal view (from
a graphic reconstruction).
appearance of the internal gills (Fig. 118), the ventral limb of each'
loop becomes the afferent branchial artery of its gill; the dorsal limb
becemes the efferent hranchial. With the loss oj^branchial respiration,
arch I I I becomes the proximal portion of the carotid arteries, arch IV
the systemic arch which persists on both sides, and arch V disappears;
from arch VI arise vessels which carry blood to both the lungs (pul-
monary arteries, Eig. 152) and skin (cutaneous arteries).
VEINS. The, viteljine veins anterior to the liver fuse to become the
hepatic vein; posterior to the liver, the right vitelline vein disappears,
the left becomes the hepatic-portal vein. The anterior cardinal veins
become the internal jugular veins; the common cardinals become the
precaval veins. The posterior cardinal veins fuse between the meso-
nephroi, and a new vein grows back from the hepatic vein to the right
posterior cardinal, to form the postcaval vein. The posterior cardinals,
anterior to their junction with the postcaval, degenerate. Posterior
to this junction they persist as the renal-portal veins, carrying blood
from the iliac veins to the kidneys.
The Chick
HEART. The chick's heart (Fig. 153) develops very much like the
frog's, except that the paired primordia of the endocardium (Fig.
220), originate at a time while they are still separated by the open
fore-gut (24 hours of incubation). Loose masses of cells migrate
from the splanchnic layer of mesoderm on the side next the endoderm
as in the frog (26-27 hours), form separate vesicles which are brought
33 Hour 48 Hour 72 Hour

Fig. 153. Stages in the development of the heart of the chick, as shown in wax
reconstructions from the ventral side. .
together on the ventral side of 'the fore-gut as th^ anterior intestinal

portal moveslback (27-28 hours), and finally fuse at'29 hours. ^The
epimyocardium is also formed as in the frog. The heart tube fdrmed
in this manner bends to the right at 33 hours (Fig. 223), begins to
beat at 44 hours, and has formed a right-handed coil at the end of
the second day (Fig. 235). • ' • >
The right and left halves of the heart are completely separated by
three septa: the septum aorticopulmonale, which divides the bulbus
into a chamber on the right* leading to the pulmonary arteries and
one to the left leading to the dorsal aorta; the interventricular sep-
tum, which divides the ventricle; and the interatrial septum, which
divides the atrium into two atria. This separation is completed at
the end of the first week of incubation. TtTe sinus venosus is incor-
porated in the right atrium.
ARTERIES. Six aortic arches are formed (Fig. 238): I and I I di'sap-
pear on the third and fourth days of Incubation; I I I forms the proximal
portion of the internal carotid artery; IV disappears on the left side
but persists as the systemic arch on the right; V disappears; the pul-
monary arteries arise from VI, but the distal portion of the right arch
remains as the ductus arteriosus until the chick hatches (Fig. 147C).
Aortic arch I
Anterior cardinal vein
Internal carotid
Dorsal aorta artery
External
carotid
artery
Bulbus
Ventricle
Meatus
\ venosus Vitelline vein
Posterior
cardinal vein
Vitelline artery
Caudal artery Iliac artery
Fig. 154. Main blood vessels in the 72-hour chick.
The arteries of the head, internal and external carotids, arise as

prolongations of the aortic roots and ventral aortae, respectively. The
arteries of the body arifee from intersegmental_branches of the dorsal
aorta." Up to the time of hatching the largest of these are the paired
vitelline arteries, which return blood to the area vasculosa (Fig. 154).
VEINS. The vitelline veins unite behind the sinus venosus to form
the meatus venosus, which later becomes the hepatic vein. The por-
tion of the meatus jvenosus surrounded by the liver breaks up into a
capillary network within that organ. For a time the vitellines pos-
terior to the liver serve as hepatic-portal veins. On the fifth day of
incubation a small vessel arises in the dorsal mesentery and joins the
vitellines, now united, by several anastomoses. This vessel, the mesen-
teric vein, becomes the portal vein of the young chick, and the vitelline
veins atrophy after hatching. The allantoic veins grow backward •
from the common cardinals to join the capillaries of the allantois;
the right allantoic degenerates on the fourth day, and the left acquires,
a new connection with the meatus venosus, by way of the left hepatic
vein. The allantoic vein degenerates at hatching. Two precaval veins
are formed from the proximal portions of the anterior cardinals and
common cardinals. The posterior cardinals at first return the blood
from the mesonephroi to the heart. At the end of the third day of
incubation a pair of veins, on the ventral sides of the mesonephroi,
appear to supplement them. These are the subcardinal veins. The
postcaval vein' arises from (1) a branch of the meatus venosus which
grows back lo meet the right subcardinal vein, (2) the fusecl subcar-
dinals which carry blood from the mesonephros, and (3) the renal
veins which develop in connection with the metanephros. The anterior
sections of the posterior cardinals disappear; the posterior sections,
the renalportal veins, carry blood to the mesonephros. After its degen-
eration, they join the common iliac veins, which pass directly, to the
postcaval vein.
Man
HEART. The first primordium of the heart is a thickening of the
splanchnic layer of mesoderm in front of the head fold. As the head
fold and subcephalic pocket enlarge,-this plate is carried underneath
the fore-gut and lies on the dorsal side of the developing coelomic
split (Fig. 155). Two converging tubes are formed from the cardio-_
genie thickening, and these later fuse, commencing at the anterior
end. No ventral mesentery is formed. ThCiheart loops to the right and
forms a half coil so that the atrial limb lies dorsal to the ventricular
limb. The subsequent partitioning of the heart into right and/left" .
halves is complicated, for 2 atrial septa are formed. The ventricle
is separated by an intisrventricular septum, and the bulbus •is divided- -,
by 2 septa which unite to form a septum aorticopulmonale. The
sinus venosus is incorporated in the right atrium, although the middle
portion can be distinguished as the coronary sinus.
ABTERIES. The aortic arches are formed and have the same history /
as those of the chick, with the exception that it is the left fourths
aortic arCh which becomes the systemic arch (Fig. 147D). The arteries
of 'the body arise from dorsal, lateral, and ventral intersegmental
branches of the dorsal aorta.
VEINS. The umbilical veins are the first 1^ appear, and after them
the vitelline veins (Fig. 156). Both are enveloped by the enlarging
liver. '
The anterior portion of the right •vitelhne vein becomes the hepatic
vein; the hepatic-portal arises from the posterior portion of the
vitelline veins anterior to their junction with the mesenteric vein.
Of the umbilical veins, only the left persists, with a direct connection
Anterior intestinal portal

C
Fig. 155. Origin and development of the Heart in human embryos. A, Diagram
of sagittal section before somite formation. B, Same, at 7-somite stage. (Both
after Arey.) C, .Ventral vie;w at 6-somite stage. D, Saine, at 11-somite stage.
{Both after Davis.) E, Ventral view at 12-mm.^stage {after Wirtinger).
Dorsal aorta
Posterior cardinal vein
Common cardinal vein
Umbilical vein
Aortic arch I
Umbilical artery
Anterior
cardinal vein
Internal
Villi carotid
artery
chorion
Vitelline vein
Fig. 156. Circulation, in human embryo at end of the first month {diagram after
Patten and Davis, modified).
through the liver by means of the ductus venosus (Fig. 254). At birth
this duct closes and the umbilical vein disappears.
Anterior cardinal
Sinus venosus
Subclavian'
Common cardinal
Left umbilical
Left vitelline
-Posterior cardinal-
- Subcardinal
Hepatic segment
Subcardinal segment
Renal segment
Supracardinal segment
Right innominate
Anterior cardinal,
• Common cardinal Left innominate
• Hepatic extension Oblique
Precaval
-Subcardinal •
Postcaval
- Supracardinal
• Postcardinal
• Hemiazygous
Azygous'
• Renal collar
Spermatic
Common iliac
B
Fig. 157. Origin of caval veinS|in human development. A, 6 veeeks, B, 7 weeks,
' C, 8 vpeeks, D. adult. {After McClum andf Butler.)
The anterior cardinals are united by an anaômosis (left innominate

vein), and the left common cardinal disappears with the exception
of the oblique vein which returns blood from the wall of the heart to 'the
Changes in Circulation a t Birth or Hatching 241
coronary sinus. The right common cardinal, together with that portion
of the anterior cardinal as far as the branching of the left innominate,
becomes the precaval vein. The precaval later acquires the azygous
and hemiazygous veins, which originate from posterior cardinals and
supracardinals as described below. The postcaval vein has a more
complicated history, and the details are still in dispute. After the
postcardinals the next veins to appear are the paired subcardinals,
ventral and .mesial to the postcardinals on the lower surface of the
mesonephros. After them the supracardinals make their appearance.
These are dorsal and mesial to the postcardinals, and, as can be seen
from Fig. 157, replace them to a considerable degree. A study of this
figure will indicate how the postcava of the adult comes to consist of
(1) a new vein'derived from the hepatic, (2) a portion of the right sub-
cardinal, (3) a connection between the right subcardinal and right
supracardinal, (4) the right supracardinal, and (5) an anastomosis
between the posterior ends of the postcardinals.
CHANGES IN CIRCULATION AT BIRTH OR HATCHING

I t is obvious that, at the time of • birth or hatching, new demands
will be made' upon the circulatory system, since the new organism
is about to eet out on an independent existence. These requirements
are met-by the inauguration of a series of changes related mainly to
full functioning of the- digestive system and organs of respiration.
Since the lungs become functional at this time, the pulmonary arteries
and veins must take up their full activity. This necessitates certain
other changes, namely, the occlusion of the ductus arteriosus and the
closure, of the foramen ovale in the heart so that the blood must make
a complete circuit of both'right and left sides of the heart. Further-
more, since the allantoisior placenta (as the case may be) is no longer
functional; the allantoic or umbilical circulation must be cut off.
This entails the occlusion of the ductus venosus_through the liver. In
thfe birds- and reptiles, moreover, the importance of the vitelline veins,
as Such, begins to dwindle.
16
The Skeleton
The skeleton of vjsrtebrates consists of a system of supporting and
protecting elements developed from mesenchyme. These may arise
in either of two ways: Often the skeletal elements are first laid down
by the deposit of a cartilaginous matrix in the mesenchyme. This
process, which is known as chondrification, is brought about through
the activity of specialized cells called chondroblasts. Later the car-
Notochord
Blood
vessels
Ventral
muscle
Dermis
Fig. 158. Diagram to show the skeleton-forming regions as seen in the tail region
of a vertebrate (after Kingsley). '
tilage is replaced by bone through the activity of osteoblasts. These

cells become imprisoned in the' matrix and so become the osteocytes.
Bones formed in this manner by indirect ossification are called car-'
tilage bones. By contrast other bones are formed by direct ossifica-
tion of the mesenchyme, omitting the cartilage stage. Such bones are
known as membrane bones. Both cartilage and bone are typically
surrounded by a membrane derived from mesenchyme, which is called
242 '
The Axial Skeleton 243
the perichondrium or periosteum, as the case may be. The separate
elements of the skeleton are connected with each other by ligaments,
by cartilage, or in a bony union.
The principal groups of skeletal elements (Fig. 158) are:
1. Dermal—consisting of bones formed in the dermis of the skin.
2. Axial elements
a. Bones formed in the median sagittal planes between myotomes on the
right and left sides of the body, e.g., sternum.
b. Bones formed in the frontal planes between dorsal and ventral muscle
masses, e.g., ribs.
c. Bones formed in the transverse planes between the myotomes, e.g.,
ribs.
d. Bones formed around the notochord, neural tube, and axial blood ves-
sels, e.g., the vertebrae.
3. Visceral elements—bony structures formed in visceral arches.
4. Appendicular skeleton—bones of the paired appendages.
THE DERMAL SKELETON

Among living vertebrates the most primitive examples of .derm bones
are the placoid scales (Fig. 159) of the cartilage fish, which are formed
in exactly the same way as teeth,
through the .activity of an ecto-
dermal enamel org&n and the
deposit of dentine by môdermal
odontoblasts (Chapter 11). In
the dermal skeleton two types of
bones are distinguished. The in-
vesting bones or dermal plates
serve to envelop regions of the Fig- 159. Section of developing placoid
head and trunk. The substituting scale {Squalm acanthias) to show origin
, fj. u I 1 of primitive dermal bone. Compare
bones oiten become so closely ^ Fig. 109. (After Kingsley.)
allied with the cartilaginous bones
as to become-fused T;\!ith them or even to replace them in ontogeny.
Many of the cranial bones -are of this type. They may be distinguished
by the fact that they do not pass through a cartilaginous stage in
development.
THE AXIAL SKELETON

The prinîtive axial skeleton is the notochord, whose origin is dis-
cussed in Chapter 7. Around this a connective tissue sheath is formed
by mesenchymal cells. Later the skull and vertebral column are
formed.
244 T h e Skeleton
The Vertebrae
The mesenchyme from each half sclerotome forms 4 condensed
blocks, the arcualia (Fig. 160), 2 dorsal to the notochord and 2 ventral;
These form the arches and centra of
Ectoderm
Dermatome
the vertebrae, as well as the pri-
Myotome mordia of the ribs. The posterior
arcualia of each somite unite with
th6 anterior arcualia of the succeed-
ing somite to form the definitive
^ ^ ^ ^ ^ ^ ^ ^ ^ ^ ^ ^ N o t o c h o r d vertebra, which thus comes to lie
• at the point of separation between
Fig. 160. Section through sclerotome , , T7>- i j. i i.
,,. , /c , N 4_ , ,• two myotomes, timht elements are
01 lizard (ocleporus) to show arcuaka .
{alter Kingsley). ^'^'^® concerned with a smgle verte-
bra: right and left dorsal arcualia
from the anterior half sclerotome, right and left dorsal arcualia
frdmlEhe posterior half sclerotome, plus the four corresponding ventral
elements.
In,/the prevertebral masses so formed, centers of chondrification
appear, one on each side of the spinal cord and one or more below the •
Fig. 161. Section to show ossification centers in human vertebra and ribs {ajtct^^^
K oilman.).
pord. These form, respectively, the neural arch^ and the centrum of
the vertebra (Fig, 161). In the vertebrae of the tail region, two addi-'
tional centers of chondrification arise below the centrum to torm a,
haemal 'arch enclosing> th'e caudal prolongation of the dorsal aorta.
With the chondrification of the vertebrae the notochord disappears in
all but the most primitive vertebrates, persisting only as the nuclei
pulposi of the intervertebral discs between the vertebrae. Finally the
vertebrae become ossified, and characteristic spines and other proc-
esses are developed.
The Ribs
Except in the caudal region, lateral processes arise from the vertebral
primordia and grow out into the myosepta. They later become carti-
laginous, and finally true bone. These are
the ribs, of which there are two types, dor- ^ ^ cfjj;; i?SSÂ#' ; Clavicle
sal and ventral, distinguished according to %•••., ^ "g .:,... .-.
the part of the vertebra from which they M^wu^f M i M,
originate. ;^,:,. ^ | \*&
The Sternum
" Mesosterna -
The sternum, or breast bone, arises in
the amphibians from the coalescence of
two longitudinal bars of cartilage, which
later articulate with the coracoids of the
pectoral girdle, but do not come in contact
with the ribs. In the amniota, the ster- Pig. 162. Diagram to show
num arises from the fusion of the ventral origin of mammalian sternum
{ajter Kingsley).
ends of the anterior rib rudiments! In
this way 2 longitudinal bars arise, from which the unpaired sternum is
formed-by fusion along the mesial line (Fig. 162).
The Skull '

The skull is-a complex of skeletal elements, arising from the chon-
drocranium, or primitive cranium of cartilage bones, which is derived
in part from the protective covering of the brain and sense organs
Sphenolateral Otic capsule
Occipital
vertebrae
Visceral arches
Fig. 163. Diagram showing components of ohondrocranium {Squalus acanthias)
I (after Kingsley).
(neurocranium), and ;in part from the supporting elements of the

visceral arches (splanchnocranium). This is supplemented by numer-
ous investing and substituting bones from the original dermal skeleton
(dermocranium).
NEUROCRANIUM. The neurocranium arises from the head mesen-
246 T h e Skeleton
chyme. In this mass, which completely invests the brain and sense
organs, definite centers of chondrification appear. These masses unite
to form the chondrocranium of the cartilage fish (Fig. 163). If the
notochord is used as a point of orientation, on either side of it a para-
chordal bar is found. In front of each of these is a separate rod; these
are the trabeculae. Between the two parachordals and around the
notochord, the basilar plate arises as the support of the epichordal
brain. The trabeculae also fuse in front to form the ethmoid plate,
which supports the prechordal brain, but they remain separate at their
posterior ends to form an opening through which the pituitary projects
Premaxilla
Womer,
Ethmoid Maxilla
Palatine
Orbitosphenoid- ^'^
Parasphenoid
Pterygoid
AJisphenoid
Jugal
Prootic
Squamosal
Quadrate
Opisthotic
Supratemporal Exoccipital
Basioccipital
Fig. 164. Diagram showing components of vertebrate skull, generalized, ventral

view. • Chondrocranium stippled, dermal elements in outline. (After Kingsley.)
downward. In front of the ethmoid plate the trabeculae -grow forward

as the cornua. Dorsal to each trabecula, another longitudinal bar,
the sphenolateral, arises. Between these two bars the cranial nerves-
make their way to the exterior. /
Around each of the major sense organs a cartilaginous capsule
develops. The olfactory capsules unite with the ,cornua, ethmoid, and
sphenolaterals. The optic capsule rarely develops fully, usually per-'
sisting in the connective tissue stage as the sclera'of the eyeball. Thfe,'
otic capsule, however, becomes" completely chondrified and unites with
the parachordals and the sphenolaterals. Between the two otic capsules
and sphenolaterals arises a- dorsal plate which forms a roof for the
brain. In the amniotes,"one or more neck vertebrae are consolidated
with the occipitalêgion.-
T H E SPLANCHNOCEANIUM. • The digestive canal in the head region
consists of the mouth, oral cavity, and pharynx. The walls of the
pharynx are perforated by the visceral clefts, which are separated
from each other by the visceral arches. These arches are composed
mainly of mesenchyme in which chondrification produces a series of
cartilaginous bars or arches supporting the wall of the pharynx. These
Fig. 165. Dorsal view of skull diagrammed in Fig. 164.
visceral arches are the mandibular, hyoid, and 4 (or more) branchial
arches. .The niandibular arch divides into dorsal and ventral portions,
of which the. dorsal portion becomes the pterygoquadrate cartilage
(upper jaw of cartilage fish); the ven-
tral portion becomes the meckelian car- PremaxiUa
tilage (lower.-jaw). The hyoid arch Nasal
divides into a dorsal hyomandibular Lachrymal
Maxilla - ^
cartilage and a ventral hyoid cartilage Sclerotics
which is'^ usually divided into several Jugal
Frontal
centers of- chondrification. The hyo-
mandibular acts as a .suspensory ele- Postorbital Postfrontal
ment for the jaws in the fish. It is Squamosal Parietal

Supra temporal
hbmologized with a, bone of the middle Quadratojugai Interoccipital
ear, the columella, in amphibians, and Dermoccipital
the stapes of mammals (see page 289). Fig. 166. Lateral view of skull
The hyoid becomes the support of the diagrammed in Figs. 164, 165.
tongue. The .branchial arches are usu-
ally divided into four parts and act as gill supports in the anamniota.
They disappear or become pharyngeal and laryngeal cartilages in
amniota.
FORMATION OF THE SKULL. In the formation of the skull two phases
are involved, namely, the ossification of the chondrocranium and the
248 T h e Skeleton
addition of bones of the dermocranium to supplement the elements
formed from the chondrocranium. These derm bones may invest and
to some extent supplant those of the chondrocranium. The main .
bony elements of the skull derived from the chondrocranium (Figs.
164, 165, 166) together with those of the dermocranium (Figs. 164,
165, 166) are listed in table 8 on page 251.
T h e Appendicular Skeleton
The simplest forms of appendages, the unpaired and paired fins of
fish, contain a skeleton consisting of parallel cartilaginous or ossified
rods, which are made up of the proximal basalia, embedded in the
dorsal muscle masses of the body; and the distal radialia, extending
outward into the free appendages. In tetrapods the appendages are
paired jointed legs. In these the skeleton is divided into a basal girdle
and a free appendicular skeleton (Fig. 167).
T H E GIRDLES. The girdles are in the form of inverted arches, of
which the pectoral girdle is united to the axial skeleton in fish and
free in the tetrapods; the pelvic girdle, usually free in fish, is united •
to the axial skeleton in the tetrapods. Each arch typically consists
of three portions. The dorsal one in the pectoral girdle is the scapula;
in the pelvic girdle it is called the ilium. The two ventral elements
of the pectoral girdle are theprecoracoid (anterior) and the coracoid
(posterior); the corresponding elements of the pelvic girdle are the
pubis and ischium. The clavicle, originally a derm bone, is associated
with the peqtoral girdle.'
HOMOLOGIES OF APPENDICULAR SKELETON
Pectoral Xjfeneral Pelvic

Girdle ;
Scapula Ilium
Procoracoid Pubis
Coracoid Ischium
Free a;ppendage
Humerus Femur
Radius Tibia
Ulna Fibula
1
Carpals Tarsals
Metacarpals • Metatarsals
Phalanges (I-V) Phalanges (I-V)
T H E FREE APPENDAGES. The pectoral and pelvic appendages are very

similar. Each has three segments: proximal, intermediate, and difetal.
The proximal segment of the pectoral appendage contains 1 bone, the
humerus; the corresponding bone of the pelvic limb is called the femur.
pThe intermediate portion of the pectoral limb possesses 2 bones,
the radius and the ulna; the corresponding bones of the pelvic appen-
dage are the tibia and fibula. The distal
segment is divided into three regions of which " 3"
the proximal portion contains 9 or 10 bones, s | •i
the carpals of the pectoral appendage, the
tarsals of the pelvic. The intermediate por-
tion contains 5 metacarpals or metatarsals,
respectively. The distal portion contains
the free phalanges of the fingers or toes.
ORIGIN OF THE APPENDICULAR SKELETON.
Air the bones of the appendicular skeleton,
with the exception of the clavicle, are formed
from a mesenchymal blastema in the limb
buds by the appearance of centers of chondri- Humerus
fication.N The origin- of this blastema was
formerly thought to be from the sclerotomes,
but the weight of evidence seems to .indicate Fibula
- Ulna
an origin from the somatic layer of mesoderm Tibia
Radius
in the deveiloping limb bud. Tarsals Carpals
Metatarsals >7|7Sn^ Metacarpals
TYPE VERTEBRATES ^m\

// Phalanges
«?%
7 ^. 0
The Frog^
Nine vertebrae are fomied, of which the pig. 167. Diagram of ap-
first is known as the cervical vertebra, or pendicular skeleton, tetra-
atlas,' the succeeding 7 are the abdominal P°d type, showing homolo-
vertebrae, and the last is called the sacral ^^' °^ pectoral elements
, , ., . , ,',•,,,,, , . • II above and to leit; pelvic
vertebra as it is to this .that the pelvic girdle ^1^^^^^^ ^^^^^^ ^^^ ^^ ^.^^^_
is attached. No caudaVvertebrae are formed, {Ajter Kingsley.)
but 3 strips of cartilage enclose the notochord
and form the primordium of the adult urostyle. Dorsal ribs are differ-
entiated, but these Iremain rudimentary and fuse with the transverse
processes of the vertebrae. The sternum arises from the fusion of 2
longitudinal- bars of cartilage which never attain connection with the
ribs. I t persists anterior and posterior to the pectoral girdle.
The cartilage bones' of the skull are the exoccipitals, prootics, stapes,
ethmoids, and the pterygoquadrate (in part), articulare, mentomecke-
1 The details of the skeleton in this and succeeding paragraphs are for reference
only.
250 T h e Skeleton
lian, hyoid, and branchials. The derm bones are the frontoparietal,
nasals, premaxillae, maxillae, quadratojugals, squamosals, parasphe-
noid, palatines, vomers, and dentaries. o
In the pectoral girdle develop the scapula, coracoid, and precoracoid,
the last of which is replaced by the clavicle. In the pehac girdle
only the ilium and ischium ossify. Only 4 digits are present in the
hand, the thumb (pollex) being absent.
The Chick
There are 16 cervical vertebrae, of which the first is the atlas, and
the second, which has appropriated the centrum of the first, is the
axis; 5 thoracic vertebrae; about 6 lumbar vertebrae; 2 sacrals; and
about 15 caudals. The last thoracic, all lumbars, and sacrals and 5
caudals are fused to the pelvic girdle. The last four caudals are fused
in a pygostyle. Dorsal ribs are formed by the cervical and the tho-
racic vertebrae. The sternum arises from 2 longitudinal bars of car-
tilage which unite in the median line. I t is distinguished by the
development of a large keel (carina) for the attachment of the pectoral'
muscles. ' ^
The cartilage bones of the skull.are the basioccipita'l, exoccipitals,
and supraoccipitals; prootics, epiotics, and opisthotics; basisphenoid,
orbitosphenoids, and alisphenoids; the ethmoid; quadrate, articular,
meckelian cartilage; stapes, hyoid, and branchials. The derm bones
are the frontals, parietals, nasals, lachrymals, premaxillae, maxillae,
jugals, quadratojugals, squamosals, pterygoids, palatines, parasphe-'
noids, vomer, angular, supra-angular, opercular, and dentary.
The pectoral girdle, develops a scapula and coracoid, together with
.a dermal clavicle. Ilium, ischium, and pubis ossify separately in
the pelvic girdle. Five digits are preformed in the pectoral appendagey .
of these the first and .fifth fail to develop further. Five also appear ,
in the embryonic skeleton of the pelvic appendage; the fifth sooit --
disappears, and the first is extremely short and develops no phalanges.
Man
Seven cervical vertebrae, including the axis and atlas, 12 thoracic,^
5 lumba^, 5 sacral, and 4 caudal vertebrae are formed. Of these, the;-
sacral vertebrae are united to the pelvis, and the caudal vertebrae
are frequently fused to form the coccyx. Primordia of ribs are formed
by all vertebrae except those following the first caudal. Only the
thoracic segments, however, develop complete ribs. The sternum
arises from 2 longitudinal primordia with which the first 8 or 9/ribs
acquire cartilaginous connections. . '
TABLE or C H I E F ELEMENTS OF THE SKULI,
A. Elements of chondro- Bj^. Bones of skull derived from chondro-

cranium cranium
1. Parachordals Sphenoids (basi-, pre-, ah-, orbito-)
2. Trabeculae Ethmoids
3. Sense capsules
Nasal Ectethmoids, turbinates
Optic Sclerotic
Otic Otics (pro-, opisth-, epi-)
Petrosal
4. Sphenolateral Lacrymal, infraorbital
5. Occipital Occipital (basi-, supra-, ex-)
6. Mandibular
a. Pterygoquadrate Pterygoid, quadrate (incus of ear)
b. Meckelian Articdare (malleus of ear)
7. Hyoid
a. Hyomandibular Hyomandibular (columella or stapes
of ear)
6. Hyoid Hyoid (of tongue)
8. Branchial arches Thyroid, cricoid (other throat car-
tilages)
B„. Dermocranium
a. Dorsal' elements Lateral elements Ventral elements
Nasal Premaxillae Parasphenoid
Frontal Maxillae • Palatine
Parietal Zygomatic Vomer
•'Orbital • Jugal, quadratojugal
Temporal Squamosal
d. Lower jaw: dentaryj splenial, coronoid, angulare
T h e cartilage bones of'the skull are the occipital (in p a r t ) , sphenoid,

ethmoid, turbinates, temporals (in p a r t ) , stapes, malleus, incus, and
hyoid. T h e malleus; ancl incus are the representatives of t h e articular
and q u a d r a t e . T h e .derm bones are t h e occipital (in p a r t ) , temporals
(in p a r t ) , frontal, parietals, lachrymals, nasals, vomer, maxillae, zygo-
matics/ palatines, and mandible, t h e last-named bone representing t h e
fused dentaries. I t is apparent t h a t m a n y of the bones of the h u m a n
skull are the result! of the fusion of separate centers of ossification
which represent skull elements of the lower vertebrates. T h e second
and third visceral arches contribute to the formation of the hyoid, t h e
others to t h e laryngeal cartilage.
T h e pectoral girdle consists of the scapula, with which is fused
the coracoid. There is no precoracoid, b u t a dermal clavicle is
252 ' T h e Skeleton
present. The centers of ossification that represent the pubis, ischium,
and iUum fuse to form an innominate bone. The free appendages
terminate in 5 digits. In conclusion, it should be mentioned that the
adult condition of the human skeleton is not attained until the age
of 25.
17
Muscles
The musculature of the vertebrate is derived from mesenchyme the
greater part of which originates from the myotomes (Fig. 168). This
gives rise to the skeletal musculature, composed of striated muscle
Sclerotome
Dermatome
Neural tube
Myotome
Dorsal
appendicular
muscle mass
Ventral
appendicular
Gut muscle mass
Splanchnic
mesoderm
Somatic
mesoderm
Fig. 168. Diagram of transverse section through vertebrate embryo in region of
limb bud, to show origin of appendicular muscles (ajter Corning).
cells and controlled by the central nervous system. A portion, how-

ever, originates from splanchnic mesoderm and gives rise to non-
striated or smooth muscle cells found in the skin^ in the wall of the
alimentary- canal, in the blood vessels, and in the urogenital organs.
These are controlled by the sympathetic nervous system (page 275)
and make up the visceral musculature. Several exceptions to these
general statements should be noted. The muscle cells of the heart are
striated; the muscles derived from the visceral arches are both striated
and controlled by the.central nervous system, although derived from
head mesenchyme. Itjwill be noted later that the muscles of the iris of
the eye (page 287) and of the sweat glands (page 260) are appar-
ently ectodermal in origin.
253
254 Muscles
Histogenesis of Muscle
Histogenesis of Striated Muscle
The histogenesis of striated muscle is not completely settled. I t •
would appear, however, that the mesodermal cells which are to form
this type of muscle become differentiated into myoblasts oriented with
their long axes in the same direction. In the cytoplasm of these
cells a series of very fine myofibrillae are developed, running the length
of the cell. At the same time the nuclei of the cells increase greatly
in number, probably by mitosis, and take up a peripheral position.
The myofibrillae undergo further differentiation resulting in the devel-
opment of the characteristic cross striations. In this way muscle
fibers are developed, and these become associated in groups by the
development of a connective tissue reticulum interspersed within and
surrounding the muscle bundles.
Histogenesis of Visceral Muscle

The histogenesis of visceral muscle involves the organization of
muscle fibers from the mesenchyjne which invades the wall of the'
embryonic gut between the endoderm and the splanchnic mesoderm.
These cells become spindle shaped and arranged in suclf a manner that
the widest portion of one cell lies opposite the taper^pg ends of its
neighbors. Thus sheets and bands of muscle cells are developed from
the primitive myoblasts. In these cells delicate contractile myo-
fibrillae are formed. The muscle cells are boimd together by con-
nective tissue fibers which are interwoven among the individual cells,
thus Organizing the tissue into layers,, etc.
Histogenesis of Cardiac Muscle

Cardiac muscle develops as a- reticulum formed from splanchilic
mesoderm cells. It is believed by many workers that the reticular
arrangement is retained and that it accounts for the branched nature- -
of the cardiac muscle, fibers. Some doubt about this exists, however.
In any event, delicate contractile myofibrillae are differentiated' in
the cytoplasm of these- cells, and they apparently 'extend for consider-
able distances following the branching processes of the' syncytium.'
Like skeletal muscle, howeyer, many nuclei are formed in the. fibers'-,
and characteristic cross striations are later developed.-
Skeletal Musculature , '

Dermal Musculature
Attached to tê skin are striated muscles which are derived from
skeletal musculature (see below) but have lost their attachment to
the skeleton. The dermal' musculature is best developed in the arnni-
Muscles 255
otes. The muscles of expression in man are dermal muscles supplied
by the seventh cranial nerve (see Chapter 19).
Axial Musculature
In this section are included all the muscles arising from the myo-
tomes and attached to parts of the axial skeleton, which they move.
They are originally metameric, but their later history is obscured by
subsequent migration, fusion, splitting, budding, and degeneration.
The intercostals, between the ribs, however, preserve their original
metamerism, which in the others may be traced to some extent by the
innervation, since the connection between a spinal nerve and the
muscle mass it supplies is
established early in organo-
geny and remains constant.
Thus it can be shown that
the musculature of the dia-
phragm, supplied by the
phrenic nerve, arises from a
cervical myotome.
Cranial Muscles
The muscles associated
with the skull are derived
from'different sources. .The F'S 169. Head of embryo dogfish (Squalus
muscles of the eyeball arise acanthias), showing preotic somites {A, B, C)
and cranial nerves (V, VII, I X , X ) (after
from the three preotic myor Kingsley).
tomes (Figr 169). The first
of 'these forms all the muscles of the eyeball except the superior oblique,
which is derived from the second myotome, and the lateral rectus, de-
rived from • the third head myotome. These are innervated by the
third, fourth, and sixth cranial nerves, respectively. The tongue mus-
culature is derived frorh the myotomes associated with the occipital
vertebrae and supplied by the twelfth cranial nerve. The muscles of
mastication, the facial muscle, and the laryngeal muscles, together with
those of the ear bones, arise from the visceral arches (Fig. 170), and
are supplied by cranial nerves V, VII, IX, X, and XI (see Chapter 19).
These muscles can probably be traced back to head mesenchyme rather
than splanchnic mesoderm as formerly assumed.
Appendicular Muscles
The preponderance of evidence indicates that in birds and mammals
as well as amphibia (Chen, 1935) the limb muscles develop in situ.
The limb bud develops as an undifferentiated mass of mesenchyme
256 Muscles
surrounded by ectoderm. In this blastemal mass, muscles and bones
are laid down, tiie differenti'ation proceeding from the proximal toward
the distal end. The pectoral muscles differentiate before those of the
Vagus GJossopharyngeal / Facial

Trigeminal
Fig. 170. Diagram to show hypothetical relataonship of branchiomeric muscles to

visceral arches and cranial nerves (after Wilder).
Dorso-medial
Scapula muscle prirnordia
Prooorocoid
Coroeoid
Ventro - lateral
muscle prirnordia /
Pig. 171. Reconstruction of the pectoral muscle masses in .a 17-mm. Nectunis . N'
{prepared by H. F. DeBruine). ^ --
pelvic appendage. The appendicular muscles are found in antagcaiis- / ,

tic groups: protractors, which move the limb forward; and retractors,
which have the apposite effect; levators, which raise'the limb; and'
depressors, which contract in the opposite direction. Like the axial
mjisclesj these have beconie highly modified and specialized among the
tetrapods (Fig. 171).
Visceral Muscles
In this category are included the muscles lining the alimentary tract,
lungs, vascular organs, and urogenital system. All arise in the
Muscles • 257
splanchnic mesoderm which^ surrounds the endothelial lining of the
organs concerned.
Heart
The muscle of the heart arises as a network of smooth muscle
fibers which later become striated. The fibers early become connected
by protoplasmic processes to form a syncytium. It is interesting in
this connection that the smooth muscle cells of the bladder of the dog
have been transformed into what are apparently striated muscles when
this organ is made to pulsate rhythmically by continued irrigation.
NOTE. The study of comparative myogeny has not arrived at the

stage -where it would be profitable to summarize our information about
the development of the muscles in frog, chick, and man.
18
Integument
The integument consists of two parts, the ectodermal epidermis and
the mesodermal dermis (corium). The epidermis soon delaminates
into two layers: the deeper germinativum, from which new'strata are
Periderm
Basal cells
Periderm
Stratum intermedium
Stratum germinativum
Corium'
Fig. 172. Sections through human fetal skin. A, Neck. B, Chin. {From/AtE_y,
ajter Prentiss.) /
)
proliferated toward the exterior; and an outer periderm or embryonic,
skin (Fig. 172). Beneath the periderm, cells derived from the germi-.
nativum form a stratum intermedium the outer layer of wh^ch is
transformed into a horny layer, the corneum.* In the amniotes the
stratum intermedium of the skin becomes further differentiated into
two other layers. The underlying dermis is essentially a ûpportihg
layer of mesenchyme cells. It is generally believed that the derinis
is derived mainly from the so-called dermatome, but some investiga-
tors hold that it originates from the somatic layer of the mesoderm,
at least in part. Both epidermis and dermis produce a number of
special derivatives.
258
Integument 259
The Corneum
This is the outer layer of cornified dead cells which are sloughed
off periodically or continuously. This layer gives rise to horny deriva-
tives such as scales, feathers, and hair. Scales originate as regions
of local growth in the corneum (Fig. 1734). They are found only
Epidermis
Gland
sheath
Fig. 173. Diagrams showing similar development in A, scale; B, feather; and C,

hair {after Kingsley).
among the amniota, where they are represented by structures such as

the scales of reptiles, or those found on the legs of birds, the tails of
rats, etc. Among the birds, scales are largely replaced by feathers,
which originate in much the same nianner as scales. The epidermal
plate, however, grows down like a^ cup to enclose a core of dermal
' Unguis
^"?"'= SubunguU_ ;^!:r!__Subunguis^
Fig. 174. Diagrams to ^how ectodermal primordia of A, nail, B, claw, and C, hoof.
A, B, C, sagittal sections; Ai, Bi, Ci, ventral view. {After Kingsley.)
origin (Fig. 173B). j The epidermal sheath gives rise to the quill and
barbs, the core gives rise to the pulp, 'by means of which nutriment
is supplied to. the developing feather. Among the mammals, hair arises
in a very similar fashion. An epidermal plate grows down into the
dermis to form the hair bulb, the proximal end of which invaginates
to receive a mesodermal core, the hair papilla, while around the whole
260 Integument
is a mesodermal hair sheath (Fig. 173C). The hair papilla, however,
does not grow out into the center of the hair like the pulp of the feather.
Claws, nails, and hoofs arise from the union of two epidermal primordia
like those of scales, a dorsal unguis and a ventral subunguis (Fig. 174).
The Germinativum
The germinativum is the living, actively proliferating basal layer
of the skin. In addition to producing the more superficial layers of
the epidermis it gives rise to the glands of the skin (Fig. 175). Among
the anamniotes, these glands are
Unicellular
gland
usually unicellular and, produce the
mucus which serves to diminish the
"<e.'eT»h ^?<>r«l|o"#»l li/^y friction of the skin against the water
M^-rifi!:] \^V^jS'-*A j - i Ep'- while the animal is swimming. Uni-
^îîî G 1 AK:fe>!.eV^? I dermis ,, , , , . j_,
cellular glands frequently aggregate
to produce multicellular glands, such
Dermis as the suckers or cement glands of
the frog. The sebaceous (oil) and
sudoriparous (sv/e'at) glands of the
mammals are also multicellular
Fig. 175. Section of Protopterus skin glands. The sebaceous glands are
to show glands (after Kingsley).
usually associated with hair follicles
(Fig. 173C). The mammary glands
of mammals are modified sudoriparous glands secreting the milk by
which the newborn are nourished through infancy.
These glands are developed by invagination of the stratum germina-
tivum into the dermis. The sebaceous glands are simple alveolar
glands; the sweat glands "are long tubular structures. /
The Dermis ;
The mesoderm of the dermis gives rise to the connective tissue^
muscle, and bony elements of the skin as well as the blood yessels
which supply it with nourishment. The bony, scales of fish are alô
dermal in origin. /
Two types of pigmentation are to be distinguished in, the integu-
ment. I The first is produced by pigment secreted in the ectodermal
epidermis, e.g., the melanin of the frog tadpole. The second is 'pro-
duced by chromatophores, which are mesenchyme cells of the dermis
or neural crest. These secrete pigment granules and form a^ layer
immediately below the epidermis, some even wandering into the epi-
dermis itself.
TYPE VERTEBRATES
The Frog
The epidermis of the frog develops cilia in stage 15 when the rota-
tion of the embryo in its egg envelopes begins. These cilia are borne
only on a particular type of rather large cell with clear protoplasm,
which is easily recognized. As development proceeds, the cilia dis-
appear except on the tail, to which they are limited in stage 25. The
horny jaws (Fig. 212) and oral combs of the tadpole are derivatives
of the corneum and consist of rows of horny denticles forming a
replacement series. Cornification commences in stage 24. The
anuran oral sucker, or cement gland, arises from either one or two
primordia. It. appears first as a pigmented area in the epidermis on
the ventral side of the head at stage 14. The epidermal cells thicken
and form two U-shaped mucus-secreting glands (Figs. 201, 207), one
on either side of the stomodeal pit. The suckers begin to degenerate
after stage 20, their site being marked only by a pigmented area (Fig.
213)'in stage 25. The pigmentation of the skin is derived from two
sources: the melanin of the egg, which is distributed to the epidermis;
and the mesenchymal chromatophores formed in the dermis, which
appear "in stage 21.
The Chick ,
The whole- body is covered by feathers derived from the corneum,
which are.arranged according to a definite pattern.
The- scales on the legs are typical reptilian scales and are derived
from the corneum; they sometimes bear feathers in the young bird
and so form a transition between scales and the characteristic avian
feathers. "^The claws arise in the corneum from two primordia, a
dorsal "claw plate" land a softer "claw sole." To prevent the sharp
claws tearing the embryonic membranes, the concavity of the claw
is filled with a pad known as the neonychium, derived from the cor-
' neum, which'is lost after hatching. The beak arises from the corneum
around the upper and lower margins of the jaws. The egg tooth is a
horny prominence on the dorsal side of the upper jaw, appearing on
the sixth day of incubation but not taking on its ultimate shape until
the fourteenth. It serves to aid in breaking the shell and is lost after
hatching. . (
Man .'
In man and the mammals in general the body is covered with hair.
The hairs are arranged in patterns which have been interpreted as
262 Integument
reminiscences of the ancestral scales. The first growth of hair -is
called the lanugo. I t is cast ofT, except over the face, soon after birth.
Sebaceous and sudoriparous glands are widely scattered over the
whole surface of the body. The mammary glands arise from two
longitudinal thickenings of the epidermis on the ventro-lateral surface
of the body, known as the milk ridges. Localized areas of invagination
produce glandular masses resembling aggregates of sudoriparous
glands.
The nails arise from nail plates and sole plates but the sole plates
are rudimentary structures. They are covered during fetal life by
the eponychium, consisting of the periderm and outer layers of the
corneum.
19
Nervous System
In the adult vertebrate the nervous system consists of the brain and
spinal cord, i.e., the central nervous system; their nerves, the peripheral
nervous system; and a semi-independent system of nerves and ganglia,
the sympathetic nervous system. Functionally these structures are
associated with the sense organs, or receptors, on the one hand, and
muscles or glands (effectors) on the other. From the developmental
point of view, the nervous system is inextricably associated with the
more concentrated sense organs, such as the nose, eye, ear, and lateral
line system (when present).
Both the nervous system and the sense organs arise from specialized
regions of the dorsal ectoderm, known respectively as the neural plate
and the" sense plates or placodes. Both the neural plate and the sen-
sory placodes withdraw from the surface and become subepidermal by
a process of invagination. The optic placode, however, is incorporated
into, and invaginates with, the neural plate, ô that when the retina
of the eye develops it does so from the brain.
NEURAL TUBE
The> neural tube originates from the neural plate, which, as we have
already seen (page 97), arises from cells that can be identified in
the blastula stage, if not earlier. I t will be remembered that this area
lies next to the area of the presumptive chorda-mesoderm (Figs. 55, 62).
It was seen earlier (Chapter 10) that the presence of the chorda-meso-
derm underneath th^ neural plate is necessary to bring about the for-
mation of the neural tube. The method by which the tube is formed
is described in Chapter 7. The cavity of the tube remains open as
the cerebrospinal canal. Its walls give rise to the brain and spinal
cord. • I
Neural Crest i
When the neural folds meet in the mid-line to produce the neural
tube (Fig. 176), a narrow strip of tissue is squeezed out on each side
263
264 Nervous System
between the dorso-lateral surface of the neural tube and the ectodenn.
This is the neural crest tissue, and it becomes divided into masses in
each somite from which the cerebrospinal ganglia develop. Groups
Neural fold
Fig. 176. Diagrams to show origin of neural tube and crest. A, Neural plate.
B, Neural groove and folds. C, Neural folds in contact. D, Neural tube.
of these cells migrate from their original position to participate in the

formation of the sympathetic ganglia, suprarenal gland, pigment, and,-
in the amphibia, head mesenchyme and the visceral skeleton.
Sensory Placodes
Although these plates give rise mainly to sensory organs, they also
contribute cells which are incorporated in cerebral and sometimes
spinal ganglia.
The Neurons
, The inner lining of the neural tube, corresponding to the outer-layer
of the neural plate, is called the ependyma. This is the center of cell
proliferation. Two types of cells are formed: 'the supporting cells,'or'•
spongioblasts; and the embryonic nerve cells, or neuroblasts (Fig. 17'7)..
The neuroblasts migrate out of the ependyma and form an ir^termedi-
ate mantle layer where they differentiate into neurons. These nerve
elements develop a prolongation at one end known as the axon or
nerve fiber and at the other end branched projections called dend^rites.
Thfe axons grow out from the mantle layer into the outer ov marginal
layer of the cord. Here the medullary sheaths of myelin, which act
as insulating coats, are formed. Not all axons become medullated.
In the ganglia, meantime, neurons and supporting cells are differenti-
ated. These ganglionic neurons are bipolar, i.e., have 2 processes.
The bipolar neurons arising in the ganglia are sensory ^x afferent
Neural T u b e 265
in nature, conveying nervous impulses from the receptor to the central
nervous system. Some neurons located in the ventral portion of the
tube itself send out axons from the ventrolateral angle to an effector,
and are therefore known as motor or efferent neurons. Other neurons
lie wholly within the walls of the tube and serve to connect afferent
and efferent neurons.
Sensory
(afferent)
Motor (efferent)
neurons
Fig. 177. Diagrammatic section of neural tube and ganglia, to show origin of
afferent and efferent neurons. /
Tlie Spinal Cord

The' spinal cord, or neural tube exclusive of the brain, very largely
retains its primitive characteristics. The cavity, or neurocoel, per-
sists as the central canal.' Between each pair of vertebrae the afferent
and.efferent neurons contribute to a pair of spinal nerves which run
out into the myotonies and hence have a metamerism equivalent to -
that of the..myotomes|, an. important point in considering the homologies
of the muscles. In fhe region of the pectoral and pelvic appendages,
several of the segmental nerves combine to form the brachial and the
sacral plexus, respectively. The development of the nerves will be
taken up in a later' section. The cord becomes surrounded by an
envelope of mesenchynae known as the meninx, which in the higher
vertebrates hecpmesl differentiated into an inner delicate pia mater
and an outer tough flura mater. Between the two lies the cobwebby
arachnoid layer. i
In cross-section it qan be seen that the spinal cord is made up of
the ependyma, the mantle layer, and the marginal layer. The roof
and the floor of the tube remain comparatively thin, but multiplica-
266 Nervous System • .
tion of neurons in the dorsal and ventral angles of either side leads
to a distinction between a dorsolateral alar plate (Fig. 178) (to which
the afferent neurons send their axons) and a ventrolateral basal plate
(from which the axons of the efferent neurons extend). Between the
Neural cavity Roof plate

Marginal layer. Alar plate
Dorsal root_
Sulcus limitans
Ependymal layer-
Spinal ganglion
Basal plate
Mantle layer-
Dorsal ramus-
Floor plate
Ventral root
Spinal nerve. .'•"'r^K Vertebra
Pig. 178.. Transverse section of human spinal cord a t 6 weeks, X30 {from Arey,
after Prentiss). ' . "
alar and basal plates there is a groove on the inner wall of each side
known as the sulcus limitans. The marginal layers contain bundles
of axons. Those on the dorsal side are from afferent neurons. Those
of the lateral and ventral region serve to connect different regions of
the cord itself or to connect these regions with the brain.
The Brain
In all vertebrate embryos the brain arises as a dilation at the
anterior end of the neural tube, and here the neural folds come
together earlier than in the cord. The first means of distinguishiiig
the parts of the brain is found in the relationship between brain "and
notochord. As the brain extends'farther forward than the notaphord,'
it consists at first of a prechordal and an epichordal • portion (Fig.
1794).. The prechordal portion soon bends ventrally arounji the- tip
of the notochord, thus giving rise to the first or cranial flexure. Three
regions of local dilation (primary vesicles) now make their appearance
(Fig. 179B}. In the prechordal portion there is the fore-brain or
prosencephalon; in the region of the cranial flexure, there is tl\6
mid-brain or mesencephalon. The hind-brain or rhombencephalon
arises in the epichordal region. The primary vesicles are soon con-
verted into the five definitive vesicles (Fig. 179C) through the division
of the prosencephalon into the anterior telencephalon and, posterior
diencephalon, and through a similar division of the rhombencephalon
Neural T u b e 267
Telencephalon f
Prosencephalon Optic vesicle
Prechordal
brain Diencephalon P
Mesencephalon
Mesencephalon
Notochord
Epichordal Rhombencephalon Metencephalon (^
brain
Myelencephalon n
.A B
Fig. 179. Diagram to show origin of main divisions of the brain. A, Before,
appearance of vesicles. B, At the 3-vesicle stage. C, At the 5-vesicle stage.
into tlie anterior metencephalon and ppsterior myelencephalon which

merges iilto the spinal cord. The mesencephalon is unchanged.
Within the brain itself local aggregates of neurons are formed.
These,are the nuclei and they are either sensory or motor in function.
Furthermore, on the dorsal surface there are three great enlargements,
the cerebral' hemispheres of the telencephalon, the corpora bigemina
(or quadrigemina of mammals), and the cerebellum. These are the
so-called higher centers-of the brain. In surveying the later develop-
ment of the.human brain (Fig. 180), we shall find it convenient to com-
mence at the posterior end.
MYELENCEPHALON. The roof plate of the myelencephalon is thin
and vascular, becoming the choroid plexus of the fourth ventricle.
This ventricle is made lip of the cavity of the myelencephalon
(myelocoel) and that of the metencephalon. The alar plate contains
sensory nuclei and the basal plate motor nuclei. The cranial nerves
originating from thig part of the brain (V-XII)_\vilI be discussed later.
The floor plate persists only as a raphe immediately beneath the
median sulcus.
METENCEPHALON. ' The roof plate persists as a short anterior velum
and posterior velum Separated by the cerebellum formed by the
greatly enlarged aUr plates. The basal plates give rise to the pons
,on the ventral side.j The floor plate is represented by a raphe. The
cavity of the mete^ncephalon (metacoel) unites with the myelocoel
to form the fourth ventricle of the adult.
MESENCEPHALON. The roof plate of younger embryos disappears
as the alar plates enlarge to form the optic lobes. These are known
268 Nervous System
as the corpora bigemina (to avoid confusion with the pHmordia' of
the retina) except in mammals where there are 4 such bodies, corpora
Rhombencephalon
Prosencephalon Mesencephalon Otic vesicle
Rhombencephalon
Optic vesicle Otic pit
Diencephalon
Telencephalon 4
Cranial flexure
Optic vesicle
Rhombencephalon Metencephalon
Mesencephalon Otic vesicle
Epiphysis Pontine flexure
Myelencephaloo
Diencephalon Inner eat

Infundibulum
Cerebral hemisphere
Olfactory
lobe
Cerebellum
Medulla'
Fig. 180. Stages in the development of the human brain. A, 3-mm. embryo.
B,j4-mm. embryo. C,,8-mm. embryo. D, Embryo at 7 weeks. 'E, Petits of-3
months. F, Fetus at 6 months. (A-E after Patten; F after Kollrnann.)
quadrigemina (colliculi). From the basal plates are formed the cere-
bral peduncles, which contain fibers connecting the parts of' the brain
anterior to the mesencephalon with levels posterior to it. I t is.stated
Neural T u b e 269
that the floor plate is not represented in the mesencephalon. The cavity
of the mesencephalon (mesocoel) is reduced to the narrow iter (aque-
duct) which connects the fourth ventricle with the third. The cranial
nerves of this division are the third and fourth (see page 273).
DiENCEPHALON. This section of the brain has a thin roof plate
which becomes the choroid plexus of the third ventricle, a name applied
to the diacoel in the adult. No basal or floor plates exist, according
to the latest investigations, so that the sides and floor of the dien-
cephalon are formed by the alar plates. The most dorsal division of
each alar plate is the epithalamus. In the posterior part of the
diencephalon the epithalami on either side unite in the mid-line and
give rise to an evagination known as the epiphysis. This becomes the
pineal gland of the adult, presumably endocrine, but of unknown
functions^- I t is not to be confused with the paraphysis, which in the
lower vertebrates sometimes gives rise to a rudimentary or vestigial
parietal or median eye. Ventral to the epithalamus on either side is
the thalamus, separated by the thalamic sulci from the hypothalamus
below. The hypothalamus forms the floor of the diencephalon. In
this region, commencing at the posterior end and extending forward, are
the following structures: a pair of majnmillary bodies, a median swell-
ing called the tuber cinereum, a depression known as the infundibulum
to which the hypophyseal pouch (page 172) attaches itself, the optic
chiasma .arising from the crossing of the optic nerves, and, most anterior
of all', the stalks of the optic vesicles from which the eyes arise (page
285). The thalami of the diencephalon contain many nuclei, including
those which receive the afferent impulses from the optic nerves (II) and
transmit impulses from one part of the brain to another.
TELENCEPHALON. Like the diencephalon, this part of the brain is
constructed solely from roof and alar plates. In the posterior part
of the telencephalon the roof plate unites with that of the diencephalon
to form the choroid, plexus of the third ventricle. More anteriorly
it is lost in the expatisidn of the alar plates. These give rise to three
divisions- of 'the telencephalon. Lowest is the corpus striatum, con-
tinuous with the thalamus. Anterior and dorsal to the corpora striata
come the olfactory'lobes (rhinencephalon, archipallium), which re-
ceive the first cranial nerves. The rest of the sides and roof become
the cerebral 'hemispheres (neopallium). These parts of the brain are
distinguished by the movement of neuroblasts through the white
medullated layer tojform a thin superficial layer of neurons, the cortex
of the cerebrum. The evagination of the cerebral hemispheres gives
rise to 2 cavities (lateral ventricles).
270 Nervous System
Spinal Nerves
It has been stated on an earlier page that, in addition to the neurons
whose axons lie wholly within the brain and cord (Fig. 181), there
exist afferent neurons whose cell bodies lie in the spinal ganglia and
efferent neurons whose bodies lie in the cord itself. Both these groups
Effector
Fig. 181. Diagram to sliow sections of the spinal cord at three differfent levels
-with pathways of communicating neurons indicated by dotted .lines.
may be subdivided further. Thus there are two general types of

afferent neurons: the somatic afferent neurons, which convey impulses
originating in the.skin; and visceral (splanchnic) afferent neurons,
which convey impulses originating in the viscera. There are also
special types of both somatic and visceral afferent neurons which are
found only in the cranial nerves. The efferent neurons also fall into
two groups: the somatic efferent neurons, which stimulate skeletal
Neural Tube 271
(striped) muscles; and tlie visceral (splanchnic) efferent neurons, which
stimulate smooth muscles and glands. Special efferent neurons are
found in the cranial nerves supplying the branchiomeric musculature.
The nerves are segmentally arranged bundles of afferent and efferent
neurons originally associated with the myotomes. The afferent neurons
arise in the ganglia, the efferent in the floor of the spinal cord. Ac-
cordingly, a typical spinal nerve (Fig. 182) has 2 roots connected to
Dorsal root •Marginal layer
Somatic sensory neuron Ependymal layer

Visceral sensory neuron. •Mantle layer
Visceral motor neuro:
Somatic motor neuro:

Dorsal xpmus^
Lai. terminal
division
Ventral terminal division of Aorta •

spinal nerve.
•Ramus communicans Sympathetic ganglion
Fig. 182. Diagram to show the neuron components of a spinal nerve. Transverse
sectioii of lO-mm. human embryo. (Prom Arey, ajier Prentiss.)
the cord: k dorsal afferent root containing the ganglion, and a ventral
efferent root-. These 2 roots unite to form the nerve trunk. The trunk •
soon divides into branches which are called rami, each containing
afferent and efferent'. fibers. The dorsal and lateral rami supply the
body wall; the ventr4.1 or communicating ramus connects with a sym-
pathetic ganglion through which the visceral afferent and efferent
neurons serve the viscera.
Origin of Reflexes
I t has been shown by Coghill that the development of behavior is
closely paralleled by the development of the connections (synapses)
. between the neurons: Thus in the urodele Ambystoma, the first reflex
of the embryo, a bending away from a light touch on the skin, does not
take place until an intermediate neuron in the spinal cord has estab-
272 Nervous System
lished synaptic relations with the sensory tract on one hand and "h
floor plate cell which already has established a synaptic relation to the
motor tract on the opposite side of the spinal cord (Fig. 183).
Fig. 183. Diagram to show in transverse section of Ambysloma larva, neurons

concerned in earliest reflex (from Coghill, Anatomy and the Problem of Behavior)..
The Cranial Nerves

The cranial nerves, or nerves of the head region, contain not, only
splanchnic and somatic afferent and efferent neurons coiftparable to
those of the spinal nerves, but also special afferent neurons frpm thfe
nose, eye, ear, and lateral line system. There are also speciarefferent
neurons to the branchiomeric muscles.
There are 10 cranial nerves in the anamniotes (Fig. 184), 12 -in .the
amniotes (Fig. 188). To these should be added in all cases the-
terminal nerve, unknown when the cranial nerves were first classified.
0. Terminal, a ganglionated nerve from the vomeronasal organ (of
Jacobson) entering the olfactory lobe. Its functions are unknown' but
it is probably sensory. Its fibers are not myelinated. . ^ - _
1. Olfactory, a lion-ganglionated special sensory nerve from the
olfactory epithelium of the nose to the olfactory lobe. The cell bodies
of this nerve originate in the nasal epithelium, and their fibers are not
myelinated.
II. Optic (ophthalmic), a special sensory nerve from the/ retina of
the eye to the floor of the diencephalon, where the "fibers froto the two
Neural T u b e 273
eyes cross (optic chiasma). Each set of fibers then enters the brain,
half its fibers crossing to the opposite side of the brain and forming
the optic chiasma. The layer of cell bodies in the retina which gives
rise to fibei's of the optic nerve is known as the ganglion layer of the
retina. The nerve fibers are myelinated. I t is claimed that in some of
the lower vertebrates efferent fibers are found in the optic nerve.
Somatic sensory
Visceral sensory
Somatic motor ' .
Visceral motor
Fig. 184. Diagram to show relationships between cranial nerves -and parts sup-
plied. Aj B, C, .Head somites. Arabic numerals, visceral arches. Roman
,'' ' numerals, cranial nerves.
III. Oculomotor (motor oculi), a general somatic motor nerve (with

some afferent fibers). Originating in the floor of the mesencephalon,
it supplies all the muscles of the eyeball except the superior oblique
and the lateral rectus, i
IV. Trochlear (patfietic), like the third, a general somatic motor
nerve (with some afferent fibers). It originates from the roof of the
brain at the isthmus ^nd supplies the superior oblique muscle of the
eyeball.
V. Trigeminal, a mixed nerve. Its efferent fibers leave the side of
the metencephalon a t a level higher than the ventral roots of the
spinal nerves. They are, therefore, to be described as special visceral
efferent neurons, and they supply muscles originating in connection
with the first visceral arch, which later become the jaw muscles.
The afferent fibers originate in the seniilunar (Gasserian) ganglion
274 ' Nervous System
which originates from the neural crest and for the most part -are
general somatic in nature, although some special visceral afferent
fibers have been described. In some lower vertebrates contributions
from epibranchial placodes (Chapter 20) to the semilunar ganglion
have been claimed.
VI. Abducens. This is a general somatic motor nerve, like I I I and
IV (with some afferent fibers). It originates from the ventral side of
the metencephalon and supplies the external rectus muscle of the
eyeball.
VII. Facial, a mixed nerve. Its efferent fibers are of the special
visceral type and supply the muscles originating in connection with the
second visceral arch, many of which become the facial muscles.
The afferent fibers originate in the geniculate ganglion, which earlier
forms a single, ganglionic mass with the acoustic ganglion (VIII).
This common primordium is designated the acousticofacial ganglion,
and it receives contributions from the otic placode (page 288). This
nerve has visceral sensory fibers connecting to the taste buds. .;
VIII. Acoustic (auditory). This is a special somatic sensory nerve',
originating from the acoustic ganglion. The common origin of this
nerve with the geniculate ganglion and the contribution from the otic
placode have been mentioned above. In the higher vertebrates the
acoustic nerve is divided into a vestibular and a cochlear nerve, each
with its own ganglion, which supply the semicircular canals of the ear
and the organ of Corti, as described in Chapter 20.
IX. Glossopharyngeal, a mixed nerve. Its efferent fibers, of the
special visceral motor type, arise from the sides of the myelencephalon
and supply muscles of the pharynx derived from the third visceral .
arch and, in mammals, the salivary glands.
The, afferent fibers arise from 2 ganglia, the superior and.petrosal
originating from the neural crest. They are of the visceral sensory
type, supplying the region of the] second and, third visceral arches."'
Epibranchial placodes are said to contribute to the petrosal ganglion -
of the ninth nerve. , ' ,
X. Vagus (pneumogastric), also a mixed nerve. Its efferent fibers,
which in the lower vertebrates supply the branchiomeric musclqfe of
the fourth, fifth, and sixth visceral arches, supply the pharyngealând
laryngeal musculature derived from those arches. They may then be
described as special visceral motor fibers. Some fibers innervate the
. smooth muscles of the viscera; hence the older name "pneumogastric."
The afferent fibers arise from a number of ganglia, of which the first
or jugular ganglion arising from the neural crest is the largest. The
others are vestigial, but their presence lends confirmation to the theory
T h e Symijathetic Nerves 275
that the vagus is composed of a number of originally separate nerves
which might have supplied the more posterior visceral arches sepa-
rately. The dorsal roots of the tenth cranial nerve pass through a
nodose ganglion before they are distributed. This nerve supplies the
lateral line organs of the anamniote vertebrates, and its ganglia may
receive contributions from epibranchial placodes.
XI. Spinal accessory. This nerve is not one of the cranial nerves
in the anamniotes, and is first included in the head by the reptiles.
It is closely associated with the vagus. Only motor elements have
been described, and these supply the head-turning muscles. They
are said to arise from branchiomeric musculature, in which case the
neurons are of the special visceral motor type.
XII. Hypoglossal. This is a motor nerve, whose roots originate
from the side of the myelencephalon ventral to those of the vagus
and accessory and are more nearly on the level of the ventral roots
of the typical spinal nerves. They are then of the general somatic
motor type." This nerve is included in the head of amniote vertebrates
only, an\i supplies the muscles of the tongue. In the anamniotes
this organ is supplied by the spinal nerves of the occipital region.
Although there are no afferent neurons in the adult, the embryos of
some mammals possess for a short time a vestigial ganglion (of
Froriep). , •* '
Metamerism of the Head »

One of the burning questions in the phylogenetic period of compara-
tive embryology was that of the metamerism of the head. It was
generally assumed that the head represented the consolidation and
specialization of a number of metameres. Some writers tried to work
this out by calculating the original number of complete cranial nerves
before dorsal and ventral roots separated or were lost. Others at-
tempted to correlate the visceral arches with lost somites. Yet others
studied the neuromeres, constrictions in the developing brain which in
some vertebrates haye rather constant numbers in the different regions
of the brain. It mu'st be admitted that so far these studies have not
resulted in any generally accepted theory.
THE SYMPATHETIC NERVES

The brain, spinal, cord, and cranial and spinal nerves are grouped
t by anatomists as the central nervous system. Associated with this is
the sympathetic (autonomic) nervous system, consisting of nerves and
ganglia controlling the smooth muscles of the viscera and blood
276 ' Nervous System
vessels, and some glands. This system arises from the neural plate,
like the central nervous system, but from the lateral margins which
Glossopharyngeal
ganglion Vagus
ganglion
Aorta
Ciliary ^
ganglion © '-L^
Otic
Sphenopalatine ) /"ganghon
ganglion ^
Submaxillary
ganglion
Cardiac ^ J^
plexus 0^r
Chain
ganglion
Coeliac //^ '

plexus //[^"^^
Submucus 1^
plexus
j-^.-r-^J-
'mlbtp
Fig. 185. Diagram to show migrations of sympathetic ganglia in human develop-
ment (after Streeter).
become the neural crests. At the time when the neural crests are
dividing into the cerebrospinal ganglia, some of the cells ibigrate
inward toward the dorsal aorta, where they aggregate and multiply to
form the chain ganglia. The chain ganglia on each side become con-
nected by fore and aft extensions, which form the sympathetic trunks.
They retain a connection with the cranial and spinal ganglia by means
of the communicating rami, and send out nerves along the principal
blood vessels. In the head the 4 prevertebral ganglia (ciliary,
sphenopalatine, otic, and submaxillary) arise from the semilunar gan-
glion of the fifth cranial nerve, and later acquire connections with the
chain ganglia (Fig. 185). These ganglia, along with the cervical
and lumbo-sacral groups, constitute the primary ganglia of the sym-
pathetic system.
By secondary migrations and fusions a series of collateral ganglia
are formed. These include the cardiac, coeliac, and hypogastric
plexuses (Fig. 185).
The terminal ganglia and nerve plexuses among the visceral organs
arise by further migrations, producing among others the elaborate
submucous plexus (of Meissner) and myenteric plexus (of Auerbach)
in the wall of the gut.
It has already been noted (page 212) that some of the 'cells from
the sympathetic ganglia .(chromaffin.cells) migrate to the vicinity of
the mesonephros to form the suprarenal gland.
TYPE VERTEBRATES
The Frog
CENTRAL,. NEHyoxJS SYSTEM. The origin of the neural tube has
already been described (page 110). There is no anterior neuropore,
and the neurenteric canal is represented, if at all, by a pigmented streak
where the neural folds .close over the blastopore. The divisions of,
the brain are poorly marked at first, but, assuming that the mesen-
cephalon occupies the area where the cervical flexure over the anterior
tip of the notochord ds to be seen (Fig. 200), the relative positions of
prosencephalon and rhombencephalon can be determined. In the
embryo at the hatching stage (20) certain landmarks are apparent. On
the roof of the brain (Fig. 206) the limits of the mesencephalon are
marked by two constrictions with a swelling between. On the floor a
thickening at a point just anterior to the tip of the notochord, and
known as the posterior tubercle, marks the posterior end of the mesen-
cephalon ventrally. ' In the prosencephalon, a definite evagination on
the roof marks the primordium of the epiphysis. On its floor is a
definite depression (optic recess) with one swelling behind (optic
278 Nervous System
chiasma) and one in front (lamina terminalis), which was the original
anterior end of the neural tube.
In the young tadpole stage (25) the differentiation of the grosser
features of brain anatomy are well established (Fig. 186). The cer-
vical flexure has been much reduced (Fig. 212). In the rhomben-
cephalon there is a relatively small cerebellum, a well-developed
choroid plexus, but the pons is scarcely developed, if at all. Corpora
Nasal tube — A ^ —
Cerebral _ r r r .
hemisphere "V
Epiphysis
Diencephalon -4 A—
Eye — 7 — - •"-'^
Optic lobe E-
Cerebellum - 7 ^ ^ - ^
Ear ——/—y
Medulla —
1st Spinal
Pig. 186. Brain and sense organs of 11-mm. Rana pipiens embryo dorsal view,
X50 (from a wax plate reconstruction prejKired by E. Phipps. and E. Van Drasek). '
(Note: Cranial nerve X, closely associated with IX,-does not appear in this view.)
bigemina are apparent on the roof of the mesencephalon. The dien-

cephalon has its choroid plexus on the dorsal side and a prominent
epiphysis the cavity of 'which no longer connects with the diacoel.
On the floor the trough-like infundibulum is partly constricted away
from the diencephalon, and is now firmly attached to the hypophyseal
portion. The optic chiasma is relatively larger than before, and the
optic recess is clearly marked. The lamina terminalis extends upward
and forward, beginning to form a partition which will separate the
cerebral hemispheres internally as a longitudinal groove feeparates
them externally at this time. The cerebral hemispheres never become
very large in the frog, nor is the neopallium formed. It should be noted
that definite neuromeres do not appear in the developing brain.
PERIPHERAL NERVOUS SYSTEM. There are about 40 pairs of spinal
nerves formed in the tadpole, but only 10 are retained after meta-
morphosis and the loss of the tail. Cranial nerves, 10 pairs only, make
their appearance. The ganglionated nerves are the first to be dis-
tinguished. Four ganglionic masses can be seen in the embryo at
stage 20. The first of these gives rise to the semilunar ganglion of the
fifth nerve and seems to receive a contribution from a placode which
develops just external to it. The second becomes the acousticofacialis
(VII and VIII), which receives a contribution from the auditory
placode. The third forms the ganglion of the ninth nerves, and the
fourth gives rise to the ganglion of the tenth. The two ganglia were
at an earlier stage associated in a common mass (postotic), and each
receives a contribution from an epibranchial placode.
The optic, nerves are well developed at stage 20, but the olfactory
nerves do not make an appearance. until stage 25. The nerves of
the eyeball muscles, III, IV, and VI, can be distinguished at stage
25, as the eye is a functioning organ at this time.
The ganglion cells which will form the sympathetic ganglia have
reached their final positions at stage 25.
The Chick
CENTRAL NERVOUS SYSTEM. The neural folds are just meeting at
the 24'-hour stage (page 113). Between this time and the thirty-third
hour, 11 neuromeres appear, of which 3 are absorbed by the pro-
sencephalon, 2 by the mesencephalon, and 6, by the rhombencephalon.
At 33'hours the most prominent part of the brain is the prosencephalon
(Fig. 223), marked by iihe large optic vesicles. On the floor a small
infundibular evagination can be distinguished. By 48 hours (Fig. 229)
there is a very well-developed cranial flexure and a small posterior
tubercle extending inward at the tip of the curved notochord. The
optic recess is small, land the epiphysis is a shallow evagination. At 72
hours (Figs. 187, 236) the division of the prosencephalon into telen-
cephalon and diencephalon can be distinguished by a constriction in
the roof between them; On the ventral side the boundary is marked
by the anterior.end pf the optic recess. Another transverse constriction
in the roof separated the diencephalon from the mesencephalon. The
metencephalon at this time is distinguished from the myelencephalon
only through the greater thickness in the roof of the former. In
later days of incubation the cerebral hemispheres, corpora bigemina,
280 Nervous System
cerebellum, and pons are developed. Two additional flexures occur:,
the cervical at the junction of myelencephalon and spinal cord, and
the pontine in the floor of the myelencephalon at the level of the pons.
PERIPHERAL NERVOUS SYSTEM. Thirty-eight pairs of spinal nerves
are formed by the eighth day, according to Lillie. The ganglionated
cranial nerves arise from 3 large ganglionic masses. The first is the
Myelencephalon
Metencephalon
Otic vesicle
Mesencephalon
Diencephalon
Epiphysis
" Telencephalon
Fig. 187. Brain of the 72-hour chick embryo. Compare Fig. 235.
primordium of the semilunar, the second is the acousticofacial, the

third the postotic. At the 48-hour stage the postotic segment has given
rise to the ganglia of the glossopharyngeal and vagus nerve's.' By 72
hours all the cranial nerves may be recognized except the trochlear
and abducens, which do not appear until the sixth day, and the spinal
accessory atid hypogastric, which can be recognized on the fourth.^
SYMPATHETIC NERVOUS SYSTEM. The primordia of the sympathetic
ganglia are in evidence during the fourth day of incubation.
Man ./ •
CENTRAL NERVOUS SYSTEM. The human brain passes through the^
3- and 5-vesicle stages, and by the time the embryo is 8 mm. in length;
the brain is in about the same stage as that of the 10-mm. pig. (îgs.'
243, 244). At this time the primordia of the cerebral vesicles are ap-
parent. The telencephalon is separated from the diencephalon by
two points of reference: the optic recess in the floor, and the velum
transversum in the roof. From the diencephalon spring the optic
stalks, leading to the optic cups, and the infundibulum, now in contact
with the hypophysis as mentioned above. The posterior boundary
of the diencephalon is indicated by the posterior tubercle arising from
the brain floor. The epiphysis seldom appears at this stage. The
mesencephalon is demarcated at its posterior end by the deep constric-
tion of the isthmus. The metencephalon is distinguished from the
myelencephalon by its thicker roof. The pons is not yet distinguish-
able. Cervical and cranial flexures have developed, but'the pontine is
still to be formed. In later stages the development of the human brain
is marked by the great increase in size and complexity of. the cerebral
hemispheres of the telencephalon. The optic lobes are quadripartite
(corpora quadrigemina), of which the two anterior lobes are especially
associated with vision, the two posterior ones with hearing.
Fig. 188. Diagram to sho\y origin of cranial nerves in man (after His).
PERIPHERAL NERVOUS' SYSTEM. The spinal and cranial nerves (Fig.

188) are formed as in pother vertebrates. In the 10-mm. pig, corre-
sponding roughly to ani 8-ram. human embryo, all the cranial nerves,
with the occasional exception of the first, can be demonstrated.
Froriep's ganglion (XII) is distinguished only with difficulty from
the accessory ganglia of XL
SYMPATHETIC NERVOUS SYSTEM. The ramus communicans of each
spinal nerve (Fig. 182) .leads to a sympathetic ganglion which can
be seen by the time 'the stage is comparable to the development of
a 10-mm. pig.
282 Nervous System
NEUROEMBRYOLOGY ''
The field of neuroembryology is a special experimental area.con-
cerned with the development of the nervous system. I t is, however,
largely outside the scope of this book, but several important findings
need brief mention.
Beginning with the basic experiments of Harrison, much work has
been done on the growth of nerves in vitro. Questions as to the
mechanism directing growth have been carefully investigated, and it
appears from the work of Weiss that the pattern of directional tensions
developed in the surrounding tissues is largely responsible for estab-
lishing the path of growth of the nerve fiber.
The process of ingrowth of nerve fibers to limb buds has been .studied
experimentally in Amhystoma. Here it is possible by implanting limb
rudiments in the early embryo to obtain extra functional limbs. The
normal limb is innervated by a plexus derived from spinal nerves 3,
4, and 5. Limbs grafted one or two segments caudally receive normal •
innervation. However, even if the graft is placed four or five seg-"
ments posteriorly, some of the original brachial- nerves may grow
caudally into the limb bud. A second limb bud may be implanted
orthotopically behind the normal, and, if it receives a branch of the
fifth nerve, will function synchronously with the normal. ^However,...
when transplanted to the gill, region, the limb will exhibit gill-like
movements.
Another fact of considerable interest which has been demonstrated
by transplantation experiments is that segmentation of the spinal.cord
and growth of peripheral nerves is entirely subservient to mesodermal
segmentation. Thus in Amhystoma the intercalation or deletion of,'
several somites will cause the development or omission of a" 'corre'-
sponding group of spinal nerves and ganglia.
With respect to the establishment of various reflex patterns experi-
ments indicate that this is entirely independent/ of functional activity.
Frog larvae may be anesthetized before active movements have Jaeen
inaugurated and kept under an anesthetic until after the time when
certain movements normally begin. When the effect of the anesth'etic
wears off', and even without any intervening period of "practice,'^the_
larvae exhibit normal'movements.
I These few examples show clearly that experimental modification of
the developing nervous system is a valuable method for determining
the correlation of structure and function within the central nervous
system.
20
Nerve Terminations
The central nervous system not only receives stimuli from various
sensory structures located throughout the body but also sends out
motor impulses to control .the activity of muscles and glands. It is
important to realize that the innervation of these structures is estab-
lished by the outgrowth of nerve fibers from centrally located neurons
—a fact firmly established by the classic experiments of Harrison
(1905) on the outgrowth of nerve fibers from transplanted neuroblasts.
THE SENSORY TERMINATIONS
For the reception of stimuli, specia,l organs—the sense organs—are

developed. Of these the most conspicuous are the eyes, the ears, and
the nose. In addition, it must be remembered that the entire skin
functions as a sense organ by means of special receptors. These may
be in the form of free nerve terminations or special tactile end organs.
Stimuli are also received from the muscles, the viscera, and other
internal structures by means of free nerve terminations. The mouth
contains taste buds, especially on the tongue. The free nerve endings
are ectodermal as are the receptor corpuscles (of various types) of the
skin, • On'the other hand the taste buds seem to be derived from
endoderm, at least in amphibia. The actual receptors (sensory cells) •
of the eye, ear, and nose are of ectodermal origin, but the organs of
which they form a part also contain elements from mesoderm, and the
ear, from endoderm.
(The eye, ear, and nose are alike in that they arise from localized
thickenings known asi placodes or sense plates,! already mentioned in
the preceding chapters. It is now generally recognized that these and
other (epibranchialj placodes contribute to the building of many
cranial ganglia. These placodes invag'inate to form pits, and those
of the lens of the eye and the inner ear detach themselves completely
from the surrounding ectoderm to become vesicles. The optic placode,
which is the primordium of the retina, is incorporated into the neural
. 283
284 Nerve Terminations
plate at the level of the prosencephalon. I t is, therefore, carried into
the neural tube and later evaginates from the prosencephalon with
which the eye is permanently connected.
Free Nerve Terminations

These structures consist of simple arborizations of the minute
telodendria growing out from the end of the sensory nerve fiber around
and among the epithelial cells.
Encapsulated End Organs

These structures are formed by the association of the nerve termina-
tion with groups of cells specially arranged for the reception of tactile
stimuli. An excellent example of one of the many types is the
Neural tube
I—Nasal septum- Qosmg plate pnmitive

Nasal choanae
pit
ExtemaKi X J : ' ' External'

nares y-û^ ^ s nares
P r e - Z f T " " ^ Palate
maxilla ^^—.^.^^
Mandible MaxillaiV .. A,,„ Tongue
process' M»n<'''"e Internal rikres
E
Fig. 189. Diagrams to sliow origin of nose.' A, Nasal placode. B, Nasal pit.
C, Vomero-nasal organ. T>, Connection between nasal pit and mouth. jE/fSagit7'
tal Section to show origin of primitive choanae. F, Sagittal section to show origin,
of internal nares.
Pacinian corpusclp. These are scattered abundantly throughout the

skin and even among the viscera. These consist of the termiiia^l nerve
fiber surrounded by many layers of connective tissue cells derived from
the mesoderm.' '
The ^ o s e
' The nose arises as a pair of local thickenings of the ectoderm at the
anterior end of the head '(Fig. 189). These thickenings are thereafter
known as the nasal or olfactory placodes. Later they invaginate to
form the nasal pits, which persist as the nose of all fish except the air-
breathing dipnoi. The cyclostomes are peculiar, however, in tliat they
T h e Sensory Terminations 285
possess a single median nasal pit. Among the higher vertebrates, the
nasal pits acquire, by means differing in the various classes, openings
into the mouth or pharynx (Fig. 190). The olfactory epithelium
contains cells which greatly resemble ganglionic neuroblasts. These
Frontal
Nasolachyrmal
duct
Auditory
tube
Pharynx
Soft
Palate
Pig. .190. Hemisection through human nose (after Howden).
become bipolar neurons which send their axon^ back into the rhinen-
cephalon of a fore-brain to becoine the first cranial nerve..
From each nasal pit on the median side an evagination gives rise
to the vomeronasal organ (of Jacobson). This is thought to have
some special olfactory function, particularly in aquatic vertebrates.
I t sends nerve fibers to join the olfactory nerve and is also connected
with the terminal nerve.
The Eye
The area from which the retina of the eye will develop can be
recognized in amphibia as a pigmented region with long columnar cells
while the neural folds are still widely open, and has in fact been
located in the blastula stage by means of vital dyes. After the closure
of the neural folds tl(is field is located on the ventral side and at the
ventrolateral angles of the fore-brain (Fig. 191). As the retina evagi-
nates from the fore-brain, a pair of optic vesicles are formed whose
constricted proximal portions constitute the optic stalks.
At the point where the optic vesicle approaches the ectoderm, two
reactions occur: (1) a local thickening of the ectoderm, called the lens
placode, from which the lens of the eye develops; and (2) an invagi-
nation of the outer surface of the optic vesicle whereby this vesicle is
transformed into a two-layered optic cup. This inA'agination con-
tinues into the optic stalk to produce a groove on the under side called
the choroid fissure.
T H E LENS. The lens placode invaginates to form the lens pit, which,
then withdraws still further from the surface and becomes closed in by
the union of its external lip to form the lens vesicle. The lens vesicle
becomes solid by the elongation of its inner cells, which later become
clear and transparent.
Optic field Lens field

Diencephalon
"S"'^l^^^s>''& Pigment layer
iT^rC'* 7 .î>».i| Rods and cones
^ Outer nuclear
layer
Inner nuclear
Pigment layer retina ^ layer
Optic stalk \ Sensory layer
Optic cup J\_retina
Lens pit x^^C^^^^^Xêns Ganglion cells
Kbrous layer
^ E Optic nerve
F
Fig. 191. Diagrams to shoiv origin of eye. A, Optic field of neural plate.
B, Optic vesicle early. C, Optic vesicle, late. D, Optic cup. E, Sensory "and
pigment layers of retina. F, Details of retina. ~~
T H E OPTIC CUP. The inner layer of the optic cup becomes the sen--
sory portion of the retina, the outer layer, the pigmented portion
(tapetum). The sensory layer of the retina soon becomes stratified.
The outer layer of cells of the retina", i.e., the layer of cells farthest
from the cavity of'the optic cup, corresponding to the ependym^ and
mantle layer of the neural tube, gives rise to a layer of cells which
form the rods and cones (Fig. 191F). These communicate by way of
several intermediate layers of cells and nerve fibers with large ga;n-
glion cells, making up the ganglion layer. The axons from these cells
grow out into the fibrous layer lining the cavity of the cup and corre-
sponding to the marginal layer of the neural tube. In this layer, the
axoms converge toward the optic stalk and turn inward at that point
to grow down the choroid fissure and become the optic nerve. In tire
pigmented layer of the retina, melanin is secreted. Meantime the
cavity of the optic cup becomes filled with a clear fluid secreted by
the surrounding cells, which later becomes viscous and forms the
vitreous body (humor).
T H E ENVELOPES OF THE EYEBALL. Around the optic cup and stalk,
a layer of mesenchyme accumulates. This layer later differentiates
into an inner delicate layer called the choroid, which contains pigment
and capillaries and may be compared with the pia matter of the brain,
and an outer dense layer known as the sclera, which may be compared
Comes Anterior chamber

Iris
Posterior ch'amber
Ciliary
process
lateral Median
rectus rectus
Vitreoua
. body Hyaloid
canal
Optic nerve ,
I Fig. 192. Horizontal section of humaii eye (after Howden).
with the dura matter of the .brain. The external portion of the sclera
over the lens-makes contact with the epidermis and becomes trans-
parent to form the cornea (Fig. 192). The epidermis over the cornea
of the eye forms the conjunctiva. In some vertebrates, sclerotic
cartilage, or even bonp, is formed, representing a~vestige of an optic
capsule. The edge of the choroid, in front of the lens, gives rise to the
iris, a circular curtain with a central opening called the pupil of the
eye. The muscles of the iris are apparently of ectodermal origin.
The iris divides the space between the lens and the cornea into two
chambers, an. anterior/ and a posterior chamber, which are filled with
a fluid, the aqueous humor. The muscles of the eye arise comparatively
late! It will be recalled that in the elasmobranch these muscles arise
from 3 short-lived preotic somites. In all other vertebrates they are
formed from condensations of the head mesenchyme.
T h e Ear
The vertebrate ear consists of the vestibule or equilibratory organ
and the cochlea or organ of hearing. Three parts of the ear are dis-
tinguished (Fig. 193). The inner ear, common to all vertebrates, giving
rise to the vestibule and the cochlea, arises from an ectodermal otic or
auditory placode. The middle ear appears for the first time in the
amphibians, and is derived from the endoderraal distal end of the first
viVceral pouch. The outer ear, found only in the amniotes, is an ecto-
dermal derivative of the proximal end of the first branchial groove.
In mammals, an outgrowth from the mandibular and hyoid arches is
known as the pinna.
Neural crest
Neural plate otic field
Saccule
Middle ear
T^mpanvim
Fig. 193. Diagrams to show origin of ear. A, Relation between neural plate and
otic field. B, Otic placode. Ci, Otic pit. C-, Otic vesicle (otocyst). D^, Divi-
sion of inner ear. D^, Relation between inner and middle ear, ,
T H E INNER EAR. This originates ^rom the otic placode, which

invaginates to form an otic pit (Fig. 193) and later closes over to'with--
dra\s' from .the epidermis as the otic vesicle or otocyst. In some verte-
brates, e.g., the elasmobranchs, the vesicle retains its connection with
the exterior by means of a hollow stalk, the endolymphatic duct.
Usually this connection is lost and the endolymphatic duct of th^ adult
is a new formation The vesicle constricts into a ventral sacculus and
a dorsal utriculus. From the sacculus the lagena is developed and'in
mammals this becomes th'e coiled cochlea -in which is developed the
organ, of hearing, or organ of Corti. The utriculus gives rise by con-
istriction to 3 semicircular canals, each with a dilation at one end, the
ampulla. These are arranged at right angles in three planes of Space.
The cavity of these structures is known as the membranous labyrinth,
and contains a fluid, the endolymph. Concretions, the otoliths, may
appear in the endolymph of the utriculus. Around this labyrinth the
otic capsule, or skeletal labyrinth, is formed. This later ossifies to
give rise to the otic bones of the skull. The skeletal labyrinth contains
a fluid known as the perilymph. In those vertebrates which possess a
middle ear, two openings are formed in the skeletal labyrinth, the
fenestra rotunda, closed off from the middle ear by a membrane, and
the fenestra ovale, into which the stapes projects. The acoustic nerve,
which is ganglionated, divides into a vestibular and a cochlear nerve,
each with its separate ganglion.
T H E MIDDLE EAR. The middle ear arises from the first visceral
pouch, which constricts into a proximal auditory (Eustachian) tube
and a distal tympanic cavity. It is separated from the exterior by the
tympanic membrane, a persistent closing plate formed from ectoderm
of the first branchial groove mesoderm and endoderm. Through the
tympanic cavity there is a chain of bones (auditory ossicles) con-
necting the tympanum with the fenestra ovalis. In anurans and
sauropsids, this chain of auditory ossicles consists of the columella,
a rod originating in part from the roof of the tympanic cavity and in
part from tfte wall of the otic capsule (stapedial plate). This bone has
been compared to the hyomandibular cartilage of the elasmobranch
and to the stapes of the mammal. In mammals 3 auditory ossicles are
found. The stapes originates from the second visceral arch, the
malleus and incus from the first. These have been compared to the
articular and quadrate bones of reptiles respectively'.. The muscles of
the middle ear, tensor tympani and stapedial, muscles, arise from
mesoderm of the mandibular and hyoid arches, which is associated
with these structures in development. They are innervated by the
trigeminal and facial nerves.
T H E QUTER EAR. The external ear consists of the external auditory
meatus, derived from the first visceral groove. In crocodiles and some
birds (owl) a- flap of skin partially protects the external auditory
meatus. Only mammals develop a pinna, which arises from tubercles
on the mandibular and hyoid arches. It is coniposed of mesoderm
• and ectoderm, contains muscles, and is strengthened by cartilage.
Its innervation is derived from the facial nerve.
The Lateral Line System

This is a diffuse sensory organ consisting of sense buds arranged in
rows over the head and body of aquatic anamniotes. Its function
apparently is to detect) slow vibrations in the water. The origin of the
lateral line system is; a lateral thickening of the sensory ectoderm
which later breaks up into separate epibranchial placodes. These are
found in the embryos of the amniotes but soon degenerate. The lateral
•290 Nerve Terminations
line system is of particular interest inasniucli as tlie lateral thickening
referred to is in some cases continuous with the otic placode which
gives rise to the ear. The principal nerve supplying the lateral line
system is the facial, although trigeminal, glossopharyngeal, and vagus
often contain lateral line components.
Pigment layer
Optic vesicle
Optic field Sensory
• layer
Lens
placode
Rods and
cones
Fig. 194. iSections of frog embryos to-slio\v origin of eye. A, Stage 14. B, Stage
16. C , Stage 17. C^, Stage 18. Di, Stage 19. D^, Stage 20. FA, Stage ,23.
jSr-', Stage 25. X28.
TYPE VERTEBRATES
The Frog
T H E NOSE. The nasal placodes appear in the frog embryo a t stage
16 as two thickenings in the sense plate. They begin invaginating
in the following stage (17) and by hatching time (stage 20) have
formed 2 circular pits (Fig. 210). In stage 21, these pits grow back
toward the mouth into which they open at stage 23. At stage 25 the
vomeronasal organ forms an evagination on the mesial side of each
nasal tube (Fig. 216).
T H E EYE. The retinal field (Fig. 194) may be distinguished in the
neural plate in stage 14, and by stage 16 optic vesicles (Fig. 201) are
well developed. The lens placode can be seen in stage 18, is invagi-
nating in stage 19, and has become a vesicle (Fig. 207) in stage 20.
Rhombencephalon
pit (Late)
Otic pit
(Early) Otic
vesicle
B C
Fig. 195. Three stages in the development of the inner ear of the frog embryo.
A, Stage 15. B, Stage 16. C, Stage 17. X20.
During these stages the invagination of the optic cup is accomplished.

In stage 20 the cornea of the eye is transparent and, after this, the
inner cells-of the lens fill the cavity of this structure. The division of
the retina into a cellular and fibrous layer is apparent in stage 22, and
by stage 25 all. the layers of the retina, including the rods and cones,
are finally established (Fig. 213).
T H E EAR. The auditory placode (Fig. 195) may be distinguished
aa a thickening in stage 15 and commences to invaginate in the stage
following. A .•vesicle, still adhering to the overlying ectoderm (Fig.
202) is formed in stage 17. In stage 22 an endolymphatic duct is
formed by a dorsomesial invagination from each vesicle, and an
oblique partition indicates the beginning of the separation of utricle
from saccule. The lateral horizontal semicircular canal (Fig. 214) is
being constricted from ijhe utricle in stage 24 and, in the stage follow-
ing, the dorsal anteroposterior canal appears. The tubotympahic
cavity arises from the first visceral pouch, which in the frog is vestigial
and has no cavity. From this rudiment a strand of cells grows dorsad
and later acquires a lumen. It loses its connection with the pharynx
and moves backward trt the ear region where it acquires a secondary
connection with the pharynx (Fig. 196). The tympanic membrane is
apparently entirely ectodermal. The columella, which connects the
tympanum with the ihner ear, arises from two primordia: the inner
stapedial plate, which is a part of the otic capsule; and a cartilage
derived from the palatoquadrate bar,
LATERAL LINE ORGANS. The lateral line organs arise from the frag-
mentation of the placode which contributes to the tenth cranial nerve.
Similar epibranchial placodes appear on the head and are innervated
by the seventh, ninth, and tenth nerves. They are larval sense organs
and disappear at metamorphosis.
Brain . j - . Utriculus and
Auaitory semi-circular canals
Sacculus
Columella
Tympanum
Stapedial
plate"
Capsule and
perilymph
Eustachian
-- tube
Pharynx
Fig. 196. Rana pipiens, diagram to show the parts of the ear. Schematic cross-
section through head.
The Chick
T H E NOSE. The nasal placodes are first seen in the chick after 60
hours of incubation, and in the 72-hour chick they have invaginated
to form pits (Fig. 239). During the fifth day the pits are divided
into anterodorsal and posteroventral portions, the first remaining at
the surface as the external nares while the second are carried into the
roof of the mouth to become the posterior nares (primitive cho'a-nae).
In the second week of development, the growth of the palate carrie^
the posterior nares back to enter the pharynx as the secondary choanael
A vestigial vomeronasal organ appears but does not persist until
hatching. ,
T H E EYE. The optic vesicles (Figs. 223, 225) are prominent in the
33-hour chick and have invaginated to form cups (Figs. 229, 231)'at
48 hours. The lens has become a vesicle at this stage but is still opiBn
to the exterior. At 72 .hours the cells of the inner wall are elongating
.(Fig.'238).
T H E EAR. In the chick of 33 hours, the auditory placodes (Fig. 226)
are visible and at 48 hours they have invaginated to form pits (Fig.
229). By 72 hours they are constricted* almost wholly from the over-
lying ectoderm (Figs. 235, 237) as the auditory vesicles. There is
still a narrow canal connecting them to the exterior. This is the
primordium of the endolymphatic duct, which in later stages will shift
its position to the median surface of the vesicle. The semicircular
canals arise as outpocketings of the otocyst prior to its separation into
utricle and saccule. The cochlea is more highly developed than in the
frog. The tubotympanic cavity arises from the first visceral pouch.
The tympanum is formed from ectoderm and endoderm and includes
a middle layer of mesenchyme. The columella arises from a stapedial
plate and hyomandibular cartilage. The external auditory meatus is
short, and no pinna is developed.
Man
T H E NOSE. The human nose arises as a pair of nasal placodes which
become'pits (Fig. 247). These obtain an opening into the mouth by
the rupture of the thin epithelium separating them from it. The
openings into the mouth (primitive choanae) are carried backward
by the formation of the palate until they open into the pharynx as
the permanent choanae or posterior nares. Thus the nasal passages
Utricle Semicircular canal
Stapes Incus Malleus
External
auditory •
meatus
Tympanum
Cochlea
Auditory tube Tympanic cavity
Fig. 197. Diagram of the parts of the human ear in a, fetus of 3 months
{after Arey).
represent the cavities of the nasal pits plus part of the original
cavity of the mouth. A poorly developed vomeronasal organ appears
in each nasal pit.but ysually disappears before birth.
T H E EYE. An optic field has been recognized in the region of the
fore-brain before the neural tube has closed, and the evagination
of the optic vesicles is also precocious. In the stage comparable to
.the 10-mm. pig embryo the optic cup (Fig. 246) and choroid fissure
have formed, the cellular and fibrous layers of the retina can be
294 ' Nerve Terminations
distinguished, and tlie lens is a hollow vesicle. These become asso-
ciated with mesodermal derivatives as already described (page 287).
T H E EAR. The inner ear arises early as an auditory placode which
invaginates to form first a pit and then a vesicle (Fig. 245). The
vesicle loses its connection to the exterior, but the endolymphatic diict
arises from the vesicle in the region where the connection formerly
existed. Toward the end of the second month the cochlea with its
intricate organ of Corti commences the coiling which is so character-
istic of the mammalian ear (Fig. 197). The middle ear arises from the
first visceral pouch (with a possible contribution from the second).
The external auditory meatus originates from the first visceral groove
and the pinna from tuberculations on the first and second visceral
arches.
Nerve
Muscle fiber
Fig. 198. Motor end plate developing on striated muscle fiber (after Cuajunco).
MOTOR TERMINATIONS
There are two general types of motor nerve endings. The simplest
are the free nerve terminations consisting of an arborization of minute
terminal branches of the axons in association with the cells' jnnerr
vated by them, as in many glands.
By contrast, a second more elaborate type of nerve ending is devel-
oped in association with the muscle fibers. In skeletal muscle thfe
nerve fiber accompanied by some of the sheath cells of the axon pene-
trates 'the sarcolemma. These form the specialized motor end plains
in contact with the muscle protoplasm (Fig. 198). Smooth muscle'
fibers have less elaborate nerve end organs consisting of the terminal
knobbed branches of the nerve fiber, sometimes forming a flattened
disc associated with the muscle fiber.
21
Atlas of Vertebrate Embryos

As the chapter title indicates, the reader will find here illustrations
portraying the anatomy of representative stages in the development
of the frog, chick, and pig, as these are commonly studied in the
laboratory. They have been referred to often in previous chapters,
but the student will find it advantageous to go over them again for the
mental exercise of comparing transverse with sagittal and frontal sec-
tions, and also sections of all kinds with transparent whole mounts.
He should remember that these sections are not idealized but are
exactly the same kind of material as that he will encounter in the
laboratory. On the other hand, since all êmbryos vary slightly in the
stage of their development and the method of preparation employed,
the student will never encounter sections exactly like those portrayed
here. They- are labeled extensively but not completely, and they
should be considered, at most, a starting point for intensive individual
work in the laboratory. . ' .
296 Atlas of Vertebrate Embryos
Epiphysis
Mesencephalon
Otic pit
Rhombencephalon
Somite III
Notochord
Mid-gut
Hind-gut
Neural tube
Cloaca
Fig. 199. 3-mm. frog embryo, viewed from right side as a transparent object
(stage 17) X25. / ' " •
Note: The frog embryos illustrated belong to the species Rana pipiens. All
references, in the text, in the absence of specific statements to tlie contrary, are, to '
R. pipiens and are based on personal examination of embryos raised in the labora-
tory from identified adults of this species. Embryos of other species of Rana will
differ from those described and figured here.
/
Atlas of Vertebrate Embryos 297
Dorsal thickening
Mesencephalon
Posterior
tubercle .Prosencephalon
Hypophysis
Rhombencephalon
Fsre-gut
Infundibulmn
Notochord
Somite
•Hind-gut
Neural tube
Cloaca
Fig. 200.1 3-mm. frog embryo, sagittal section, X42.
Prosencephalon
Optic
vesicle
Fore-gut
Stomodeum
Sucker
Fig. 201. 3-mm, frog embryo, transverse section through optic vesicle, X52.
Rhombencephalon
Otic pit
Notocbord
Mesoderm
Sucker
Fig. 202. 3-mm. frog embryo, transverse section through otic (auditory) vesicle,
X52.
Neural tube
Notochord
Somite
Hypochord
Mid-gut
Liver
Fig. 203. 3-mm. frog embryo, transverse section through mid-gut and liver, X52.
Prosencephalon- Optic stalk
Hind-gut/
Fig. 204. 3-mm. frog embryo, frontal section through optic stalks, liver, and
hind-gut, X52.
Prosencephalon
Fore-gut
Optic cup
Mesencephalon
Oral gland
Otic vesicle
Rhombencephalon
Pronephros
Myotomes-
—^Hind-gut
>*' -Cloaca
P's
^
Fig. 205. 6-min. frog larva (just hatched), transparent preparation, viewed from
I right side (stage 20), X 1 5 . -
Epiphysis Diencephalon
Posterior Telencephalon
tubercle
Mesencephalon
Optic recess
Stomodeum
Metencephalon Optic chiasma
Infundibulum
Hypophysis
Sucker
Pharynx
Myelencephaloft
Heart
Liver
Notochord
Mid-gut
Somite
Fig. 206. 6-mm. frog iai-va, sagittal section, anterior portion, X42.
Mesencephalon
Optic iPigment layer Diencephalon

'^"P iSensory layer
Hypophysis
Pharynx
Thyroid
Sucker
Fig. 207. 6-mm. frog larva, transverse section through optic cup, X52.
Myelencephalon
Endolymphatic duct
Notochordi
Otic vesicle
1 St efferent branchial
artery
1st afferent branchial

artery
1st external gill

Pericardial
cavity
Ventricle
Fig. 208. 6-mm. frog larva, transverse section through otic vesicle, X52.
Spinal cord
Notochord
Hypochord
Dorsal aorta
Glomus Nephrostome
ffl-i:iaf! ^^"'Ss: V-K;^ \-..-.^wr-*—Pronephric

J O l i l V i v J HmhS>-7m tubule
K5\3.//tSWv^^ \:V:~i " V - ' i ^ Intestine
Coelom
Liver
veins ' y
Fig. 209. 6-min. frog larva, transverse section through pronephros, ><52; ' '
Nasal pit
^gmental
muscles
mmw.
iff:
Fig, 210. 6-mm, frog larva, frontal section through nasal pit and visceral
pouches, X52.
306 • Atlas of Vertebrate Embryos
Olfactory » . ,
•• •' • *
Eye '/^"K ' JJ V
Ear- - . - r •-' I A , ,
V gills
Pronephro; . '
I
I
ilntestine
-Cloaca
Tail fin H
Fig. 211. 11-mm. frog larva, transparent preparation viewed from right side
(stage 25), X15.
Epiphysis
Optic recess
Infundibulum
Optic chiasma
Posterior Hypophysis
tubercle
Mesencephalon
Stomach
Lfver
Notochord
Intestine
Dorsal
Yolk
• Muscles
of tail
Fig. 212. 11-mm. frog larva, sagittal section, anterior part, X40.
Diencephaloi
Pigmented
layer
Sensory
layer
Sucker
Fig. 213. 11-mm. frog larva, transverse section, through eye, X42.
Myelencephalon
Notochord
Semicircular canal
Inner ear
Phai^mx
Ppercular
chamber
Ventricle
Fig. 214. 11-mm. frog larva, transverse section through ear, X42.
308 '
Myelencephalon
Notochord
•Aortic root
Glomus
Lung
Opercular
chamber
Large intestine
Fig, 215. ll-mm. frog larva, transverse section through pronephros, X42.
External narM
Pigment layer
Sensory layer
Diencephalon
Intestine
Spinal cord ^
S^;mental musde
Fig. 216. 11-mm. frog larva, frontal section through nose, eye, and ear, ><42.
„ , .,, Anterior neuropore ,,

Head fold f Proamnion
\ i''t rior
Amn:c-
cardjcj
vesi( V
. •^.' -'f'rx 1 '• ru TT-3fcri
1 If-* \\ portal
- ~ \ irilfold
N iural
-roove
^
Noto-_
chord
«.% _ IV
Somite
f: .*' •
L * "
Ar( »
pellut di
,- r'riinitive
~~ '"' knot
\
IMmitive
.w streak
Area
vniwilosa
i
'-
*
-
.'*''
Fig. 217. 24-hour chick embryo, cleared preparation from dorsal side, X25.
312 Atlas of Vertebrate En;bryos
Mesoderm
Fig. 218. 24-hour chick embryo, sagittal section, X37%.

Epidermis
Brain
Mesenchyme
Notochord
r%r V<V:^•,>««~.^.«l»•r••<^•. • • . • . • / / / -•»«=-—

a.:;!!/.,7.,.-;;S~-=;;-s.;.^^^ W&ifef'°~'°^--.--;&^^ ^^ "-s
/ Somatic mesoderm / Proamnian Splanchnic mesoderm

Ectoderm Endoderm
Fore-gut
Fig. 219. 24-hour chick embryo, transverse section through brain region. The
neural folds have met but are not yet fused together. X42.
Axial mesoderm,
» Notochord
'Somatopleure
*••••,••'' '"••••i;i'~*vlft'ff^K^.2i*''
•^Vs.,'"*"'^*''.-.
- »••—•-••-•,•,; Epimyocardium'^%!-'*'
?^'"-Xr-.,..--i,,<<.
J/Md
#^^^^ks#' ---"^^^gi?
Splanchnopleure
Endocardium
Amniocardiac
vesicle
Fig. 220. 24-houi: 'chick embryo, transverse section through region of intestinal
.portal, X42. ^ •
Somite IV
Neural groove
Exocoel Ectoderm
Blood island
Intermediate rnesoderm Endoderm

Fig. 221. 24-hour chick embryo, transverse section through-fourth somite, X42.
Primitive groove
Ectoderm, Mesoderm
Endoderm
Fig. 222. 24-hour chick embryo, transverse section through primitive streak,
X42.
Head fold
of amnion
Anterior
neuropore
Prosencephalon
\ -Aa I, ^ Optie
*i ' . vesicle
Mesencephalon -T
Rhombencephalon
Somite 6
Notochord
Sinus
i ' f •'••"'•'• 'h i'-'rhomboidialis-'
streak
T:t4' - ' ^
1 M •<• ij s K •- * /I ? ^'4
^'^^
'^ X
Fig. 223. 33-hour chick embryo, cleared preparation from dorsal view, X25.
Head fold
pf amnion
Prosencephalon
Subcephalic
pocket
Mesencephalon
Fore-gut
Pericardial
cavity
Rhombencephalon
Heart
Notochord
jjl|), Anterior
m) intestinal
porfa(
I)
\ ». streak
Fig. 224. ^3-hour chick embryo, sagittal section, X25,

••1
316 • Atlas of Vertebrate Embryos
Epidermis Mesenchyma
Optic vesicle
Somatopleuie
Subcephalic
pocket
Splanchnoplevire
Fig. 225. 33-hour chick embryo, transverse section through optic vesicles, X42.
Rhombencephalon
Notochord Ôtic (auditory) placode
Fore-gut> .Dorsal aorta
Somatopleure 3 5 « . y T % % . ^ -Lateral sulcus
mesocardium __^/_
^^-sC^s^*^ "'^%^^
Epimyocardiun - ^
Splanchnopleure
Endocardium^
Fig. 226, 33-hour chick embryo, transverse section through otic placodes, X42,
Spinal cord
Somite
, Intermediate mesoderm
, Exocoel /
" — V Mid-«„t l , ^ - - ^ '

Coelom vein
Fig. 227. 33-hour chick embryo, transverse section through viteiJjae veins, X42.
Spinal cord
Neural crest
Dorsal aorta
Coelom
^::-:--:>-'-
<?^-SiS:--^
Notochord Splanchnic layer
Mid-gut
Fig. 228. 33-hour chick • embryo, transverse section through sixth somite, X42.
Mesencephalon
Hhombencephalon-./."'! ' - / ^ Optic cup

Otic vesicle Lens vesicle
Visceral cleft I
II Prosencephalon
III Atrium
-Bulbus arteriosus
Sinus venosus ^ j i ~ *~ .—J
Vitelline vein • ^' -'• ,— '^'•"—Ventricle
Neural tube
^ ^Tail fold
JP"' ' I'P
Fig. 229. 48-hour chick embryo, transparent preparation from dorsal view
' (head from right side), X15.
Mesencephalon
Metencephalon
Diencephaloa
Stomodeal
Notochord -f-f plate
' f
•7^ Telencephalon
Pharyn
Bulbus
arteriosus
Heart
(ventricle)
Doi'sal aorta
Fig. 230. 48-hour chick embryo, head in sagittal section, somite region in frontal-
section due to torsion, X44.
, ^ . J- , • Dorsal aorta
Anterior cardinal vein p
•Aortic arch I
Otic pit
Lens pit
Chorion Optic cup
Yolk sac Kotochoidf . ; r ^ ^ ^ l ^ M ^ ^ . ^ Blood island

Visceral groove I \ ^ ^ V ^ P i g m e n t layer
Visceral pouch I Hypophysis Sensory layer
ig. 231.' 48-hour chick embryo, transverse section through otic pit and optic
cup, X50.
Common cardinal Bulbus

vein arteriosus (jjioi-ion
Dorsal aorta Fore S " ' ^ / ' ^ ^ / ? ^ ' ^
Notochord
Spinal cord
Epidermis-
Yolk sac
Coelom
Dorsal mesocardium
Fig. 232.^ 48-hour chick embryo, transverse section through heart, X50.
Somite
Notochord Dorsal aorta Vitelline •
iJhorion •-!;^, Ventricle
fe;l\
ife-^s?
Posterior cardinal
vein
^.»^>'*St^.
ViteUine Mid-gilT'-''' ^'''^''''
Fig. 233. 48-hour chick embryo, transverse section through liver, X50.
319
Amniotic raphe
Spinal cord Notochord
iî—Posterior cardinal vein

Mesonephric duct
Dorsal
Coelom' aorta
Lateral sulcus Mesonephric
tubule
Fig. 234. 4S-hour chick embryo, transverse section through mesonephros, XSO.
Myelencephalon
Otic vesicle Mct^ncephalon
\
Visceral'
cleft I "
-'k^- l>
-Mesencephalon
m— -Choroid fissure
;;Ôptic cup
Atrium- and lens
~ ~T" Diencephalon
Nasa.1 pit - Epiphysis
Telencephalon
Ventricle-
Anterior .
limb bud \ V
-4
Vitelline
:v A —!»- Somite'26
artery
t 1
1
. . . \
Vitelline L . . . ^ - 'If
J Posterior
vein hmb bud
,^
J
r/ wiit
Fig. 235. 72-hour clik ___1_\ j , .!„Ljparent preparation from dorsal view, head
seen from right side, X15. (.
Aortic arches
Dorsal
aorta JMyelencephalon
Metencephalon
Infundibulum
Isthmus
Atrium
Spina!
cord
Notochord
Ventricle
Amnion
Mesencephalon
Diencephalon
Telencephalon Epiphysis
Mesonephros
Notochord
Spinal cord.—
Fig. 236. 72-hour chick embryo, sagittal section, X25.

otic vesicle g^^gj;^^
Amnion SH, H n ^
Chorion
Epidermis
, , : # " Mesencephalon
Yolk sac'
Fig. 237. 72-hour chick embryo, transverse section through otic vesicle, X25.
External carotid artery-, Le„g ^^^^^^

Dorsal aorta ,
Aortic arches te l^^'^'^'y ^^^^'
Chorion
III II /\ • / ^^Pigment layer
Amnion
Somite,
Spinal /
Diencephalon ^''
cord
Notochord

Pharynx
III II I Thyroid Internal carotid artery
Visceral arches
Fig. 238. 72-hour chick embryo, transverse section through optic cup, X25.
Esophagus p^. Common cardinal Bulbus arteriosus /-•'

Chonon Amnion bionchus <; ^ " ^ - a=ici:?:a::
Somite
TelencephalonJ ' -rr—Epidermis
Spinal
cord - ' / .>^ ^—'
^ Yolk sac
Notochord ""/^-'''i
Dorsal aorta
Pleural groove
Atiium Nasal pit
venosus Pericardial
ricardial v
cavity
savity
Fig, 239. 72-hour chick embryo, transverse section through heart and'lung, X25.
Posterior
Dorsal cardinal Dorsal
Amnion aorta vein mesentery Lwer
Chorion^
Somite
Allantoic vein
Duodenum Ventral mesentery
Meatus venosus
Fig. 240. 72-hour chick embryo, transverse section through Uver, X25.
Amniotic raphe
'osterior cardinal vein
Sclerotome
Dermatome.
Myotome
Mesonephric
duct
Mesonephric '
Lateral sulcus tubule
Dorsal aorta- Vitelline
artery
Fig. 241. 72-hour chick embryo, transverse section through vitelline arteries
leaving body, X25.
Chorion Mesonephric
Amnion \ duct Somite Dorsal aorta
Leg bud,
Hind-gut
Allantois
Fig. 242. 72-hour chick embryo, transverse section through allantois, X25.
Metencephalon
Myelencephalon
^-"T^r^^^ ,
/ \ .^Mesencephalon
Plni
\
Oesophagus,, — Diencephalon
/ ^ Lye
•N' S Telencephalon
Trachea-- -
'1
V-^^—Heart
Anterior. ^ ^ \;V—Body stalk

limb bud
4. ^ f j'
Roots of ^
spinal nerves - -j-Posterior
1^ limb bud
Liv"
N., Î^. )nephros
\
Fig. 243, lO-mm.'pig embryo, transparent preparation from right side, X U .

Metencephalon
Pharynx ^yeêncephalori
Mesencephalon
Aortic arch
Pre oral
gut
Oeso|)Vi ICLI
Dien-
cephalon
Hypo-
physis
Atrium
"Sptic chiasma
•Telencephalon
Trachea-^
Tongue
Lung
I 7
'fintval pancreas
m___VitelIine vein
.Body
, Dorsal _ \ ' - - - \ j stalk
pancreas \ , \ Umbilical
artery
Viteffin V
(ant. mesenl IILIX
artery \ — Cloaca
Notochoi
Meta-
nephroa
Mt n p' !<•
Fig. 244; 10-riim. pig embryo, sagittal section, X16%,

Noi\e XI
Nerve S
14'
tf,
and jugular T ^ / Ganglion IS
ganglion ' • ' (superior)
Otic vesicle
Ganglion 2 m
MyelencephaIonV7 (acoustic)
Ganglion Y'
(semilunar)
-J—Basilar
artery
Nerve III
Internal
carotid artery
Mesencephalon^'^^
Fig. 245. lO-mm. pig embryo, transverse .section through otic vesicles, XTGVB.
Spinal cord^ .^r-v~v, r. i

/ | f » V N^ Spinal ganglion
., 4 a f i ^ . \ Ventral root
Notochonl^f _U "^^^j: V Dorsal ramus
~~u
Anteri '
cardinal i " (jang-Jion X
Aort] nodosum)
arch i n Radix aortae
Viscenil
Visceral arch
TongU'
Nerve -> .
I
Infundibului i - \
1-
T
—-j-ilypophysis
/_ Anterior
Ler —tv, irdinal vein
Sensory layer ,
Optic ct p Pigment layer
'" {—Diencephalon
Fig. 246. 10-mm. pig embryo, transverse section through optic cup, X16%.
1 cord
Notochord Mjotome
Nerve
Dorsal aorta
Oesophagus Anterior
Trachea cardinal vein
Left
Right
atrium atrium
Bulbus
aortae
Olfactory
pit
Telencephalon— V ' y ^ J f
Fig. 247. 10-mm. pig embryo, transverse section through nasal (olfactory) pit,
X161/2.
Spinal cord
Ganglion
Notochord
Brachial
plexus
Common Dorsal aorta
cardinal vein
Esophagus
•Trachea
Left atrium
Right _ ventricle
ventricle
Fig. 248. 10-mm. pig embryo, transverse section through sinus veno$us, X16%.
Spinfl c—1
G " '1 n
Nulji.! n.1
D •• 1 aoiia
I osterior
iinal vein
Anterior. Mesonephros
Jimb bud-
Subcardinal
Oesophagus
Coeloiii^ liUng bud
r bea
vena ca' "ij/
atrium
Uft
Righl utricle
ventricle
Fig. 249. 10-mm. pig embryo, transverse section through lung buds, X161/4.
Spinal cord
•Notochord
•Dorsal aorta
Bowman's Mesonephros
capsule
Stomach
Liver
Septum
transversum .Pericardial
cavity
Fig. 250. 10-mm. pig embryo, transi'erse section tlirougli stomach, XW/2.
Spinal cord
Ganglion
Notochord
Dorsal aorta
Bowman's
Mesonephros capsule
Posterior
vena cava
Mesonephric
duct
Liver
Left umbilical
vein
Body stalk
Vitelline artery
Fig. 251. lO-mm. pig embryo, transverse section through gall bladder, X 1 6 ^ .
Spinal cord
Notochord
Dorsal aorta, Posterior
cardinal
vein
Posterior
Mesonephros. vena
cava
Sub-
cardinal
vein
\ Mesonephric. Left
duct vitelline
(portal)
Gut vein
Right Left
umbilical umbilical
vein
vein Left
-^ -^vitelline
artery
Left
umbilical
AUantois' artery
Right
umbilical
artery
Fused
umbilical
veins
Fig. 252. 10-mm. pig embryo, transverse section ,through umbilical stalk in
region of intestinal loop, X16%.
332. Atlas of Vertebrate Embryos
Spinal cord
Coelom
MesonepVxros
Mesonephric
duct
Mutanephric
duct
Notochord
Fig. 253. 10-mm. pig embryo, transverse section through metanephric duct and
posterior limb buds, X16%.
Neural tube
Basilar
artery
Anterior.
cardinal Notochord
vein Internal
carotid artery
Olfactory pit
Thymus
Visceral 3rd Aortic arch
poucli 4th Aortic arch
6th Aortic arch •
Sinus
venosus
Right
atrium
Subcardinal
anastomosis
Dorsal
aorta
Notochord
Neural tube-
Fig. 254. 10-mm. pig embryo, frontal section through aortic arches and ductus
venosus, X16%.
22
Embryological Technique
Embryos, according to their size, may be studied as opaque objects
or, after they have been properly treated, as transparent objects. The
older generation of embryologists depended largely upon delicate dis-
sections of these minute objects, and this method is still of great value.
The method most employed in the study of comparative embryology
is that of cutting a preserved egg or embryo into a series of extremelj
thin slices, and arranging these in order upon a glass slide, so that
they may be examined under the microscope. Yet it is a difficult-
mental exercise to translate sections into terms of the whole embryo,
for the single section, especially, is meaningless except when interpreted
as a part of the complete series. It is very helpful, therefore, when
facilities permit, for each student to prepare for himself a whole
mount and a series of sections through one of the embryos he is to.
study.
FIXATION
The preliminary preparation of material for microscopical work'

involves three distinct-operations: killing, fixing, and preservation.
In practice, two or three of-these operations are performed by'a'single
reagent known as a "fixing fluid," Such a reagent should kill, the_
embryo so rapidly that it will undergo the minimum of postmortem
changes; it should preserve the structures of the embryo with as li'fe-'
like an appearance as possible; and it should harden the soft'parts so
that they may undergo the later processes of technique without loss
of form or structure. Some fixing fluids, such as alcohol or formalin,
may be used indefinitely as preservatives, but the majority are-used
fpr|a particular optimum period, and are then washed out and replaced
by alcohol.
The Frog
The frog's egg, before hatching, is best fixed by Smith's fluid.
33.1 •
Fixation 335
Potassium bichromate 0.5 gram
Glacial acetic acid 2.5 cc.
Formalin 10.0 cc.
Distilled water 75.0 cc.
1. Cut the egg masses into small pieces of about 25 eggs each, and
submerge them in a dish of Smith's fluid for 24 hours. A quantity equal
to ten times the volume of the eggs should be used.
2. Rinse the eggs in water and wash with a 5 per cent aqueous solu-
tion of formalin until no more free color comes out. The eggs may be
kept indefinitely in this fluid. If it is desired to remove the egg
membranes, proceed as follows:
3. Wash in water for 24 hours, changing the water several times.
4. Place the -eggs in eau de Javelle> diluted with three times its
volume of water, and shake gently from time to time during a period
of 15 to 30 minutes until the membranes are almost dissolved and
will shake Off.
5. Rinse in water and run through 50 per cent and 70 per cent
alcohol, I^hour to 1 day each, and preserve in 80 per cent alcohol.
After hatching, larvae are best fixed in Bouin's fluid.
.. Picric acid, saturated aqueous solution 75 cc.
Formalin 25 cc.
Glacial acetic acid 5 cc.
1. Larvae are left in this fluid 1 to 18 hours, according to size.
2. After rinsing in 50'per cent, alcohol, wash in .70 per cent alcohol,
to which has been added a few drops of lithium carbonate saturated
aqueous solution, until the yellow color is extracted. Preserve in 80
per cent alcohol.
The Chick
The chick embryo miist be removed from the shell, albumen, and
yolk before fixation. As the early stages are more difficult to handle,
it is advisable to practice this operation on embryos of 72 hours'
incubation and then work backward toward the stages of the first day.
1. Obtain a dish 3 inches high and 6 inches in diameter, two-thirds
full of normal saline solution, warmed to 40°C.
Sodium chloride 0.75 gram
Water ' 100.00 cc.
Place a piece of dry absorbent paper cut a little larger than a cover
slip in a clean dry watch glass.
Grease one surface of a cover slip to receive the embryo after its
removal.
336 ' Embryological Technique
. 2. Crack the shell of the egg at the broad end with the flat of the
scaipe], and pick away the pieces of shell until an opening slightly
larger than a half dollar has been made. Remove the outer and inner
shell membranes. Invert the egg beneath the surface of the salt solu-
tion and allow the contents to flow out. The blastoderm, containing
the embryo, will rotate until, it is uppermost. With fine-pointed
scissors, cut rapidly a circle of blastoderm, about the size of a quarter,
with the embryo at the center. With blunted forceps, pull the blasto-
derm and adherent vitelline membrane away from the yolk and
albumen, waving it gently beneath the surface of the salt solution to
remove all yolk.
3. Submerge a Syracuse watch glass in the salt solution and float
the embryo into this. Remove the watch glass carefully from the
large dish and examine the embryo with a dissecting lens. If the
vitelline membrane has not yet separated from the blastoderm, it_
should be removed at this time with fine-pointed forceps and needles.
Make sure that the embryo lies dorsal side up, as it did when the
egg was opened.
4. Slide a cover glass, greased side up, under the embryo, and remove
all salt solution with a pipette, taking care that the embryo lies in the
center of the cover glass. Lift the cover glass by one corner so that
the overhanging edges of the blastoderm fold under, and place it in a
dry watch glass on a piece of thin absorbent tissue paper. Add at once
a few drops of F.A.A. fixing fluid, prepared immediately before using.
Formalin 2 parts
. Alcohol (85%) 17 parts ..
Glacial acetic acid ' 1 part
While the embryo is becoming attached to the paper, remove- the
yolk, albumen, and pieces of shell from ,the dish of salt solution to a
slop jar, reheat the salt solution to 40°C., and prepare another embryo.
Three embryos of each stage are to be prepared.
5. After 5 minutes, drop the cover glass, Qvahvyo side up,/ into, a
small slender dish of F.A.A. and leave for 4 hours.
6. Wash in 70 per cent alcohol for 30 minutes and preserve in
80 per cent alcohol or stain at once.
I •
The Pig
Embryos of 6-mm. body length and over are easily located in the
uterine wall. Slit open the uterus and remove the embryo with fine- •
pointed forceps and a horn spoon, taking pains not to rupture the
membranes. Place at once in Bouin's fluid. Embryos of 10-nim. body
Whole M o u n t s 337
length should be fixed for 4 hours. Rinsing and preserving are done
as for the frog or chick. Larger embryos should have the body cavity
slit open to admit the fixing fluid. Fetal pigs of 6 inches or more
should be injected through the umbilical artery with formalin (20 per
cent aqueous solution). This solution is also injected into the body
cavity and cranium, after which the fetus is submerged in the same
medium for a week and preserved in 6 per cent formalin.
WHOLE MOUNTS
I t is very helpful to have some embryos mounted entire for com-
parison with the serial sections. In making these whole mounts, the
embryos are stained, cleared, and mounted, i.e., transferred to a final
medium for preservation and examination on the slide beneath a cover
glass.
The Frog
Frog eggs and embryos may be mounted as opaque objects with the
natural pigmentation, or they may be cleared and stained as trans-
parent mounts.
OPAQUE WHOLE MOUNTS. Most of the older methods of preparing
whole mounts are unsatisfactory. Better permanent mounts may be
made by mounting the embryos in plastic. Materials for this purpose
and directions- for their use may be obtained from companies manu-
facturing or selling them.
TRANSPARENT STAINED MOUNTS

1.' Bleach the embryo, until white, in hydrogen peroxide. About
1 week is required for this purpose. Embryos that have been preserved
in 80 per cent alcohol should first be passed through 70 and 50 per
cent alcohol to water, 1 hour or more in each fluid. Embryos in forma-
lin must be rinsed in water for 1 hour.
2. Stain in dilute borax carmine 4 days or more.
Borax, 4% aqueous solution 100 cc.
Carmine 1 gram
Boil until dissolved and add alcohol, 70% 100 cc.
To dilute; take 5 cc. of the borax carmine and 95 cc.
of .35% alcohol and add a crystal of thymol.
3. If overstained, remove the surplus color with hydrochloric acid
(1 per cent solution in 70 per cent alcohol) after passing through water
and 50 per cent alcohol, 1 hour each. If acid has been used, several
changes of alcohol during the hour are recommended.
338' Embryological Technique
4. Run up through -80, 95, and 100 per cent alcohol, 1 hour each,
and place in xylene (xylol) until transparent.
5. Prepare a mounting diagram by drawing an outline of a slide on
a piece of carboard and on this lay off an outline of the cover glass
to be used. Place a clean slide on the diagram, and, just inside
the right and left margins of the cover-glass outline, put a small piece
of broken cover slip as a support. Place a few drops of Canada bal-
sam, or clarite, dissolved in xylene, between the supports, place the
embryo in position, and lower a clean cover glass gently. Try to
avoid the formation of air bubbles. If these appear later, they may
be removed by a needle which has been heated or dipped in xylene.
A little fresh balsam or clarite may be run into the cavity.
The Chick
Total mounts may be stained either with the borax carmine or with
Mayer's hemalum.
Hematoxylin 1 gram
Distilled water 1000 CO.
After this has dissolved, add
Sodium iodate 2 gram
Alum 50 gram
(Does not keep well)
1. Run the embryo from the 80 per cent alcohol down to water
through changes of 70 and 50 per cent alcohol, 1 hour each.
2. Stain in borax carmine, undiluted, overnight, or in hemalum
1 to 3 hours. Either stain may be diluted still further and the staining
period prolonged. In laboratory schedules which require a 4-day
staining period, 5 per cent solutions of the borax carmine or hemalum'
may be used. The borax carmine is preferred for whole mounts, the
hemalum for material which is to be sectioned. '
3. Destain, if necessary, in acid "alcohol until the desired color^,is
obtained. Embryos stained with hemalum will turn red in the acid
alcohol, and the blue color must be restored by washing them in ruur
ning water or, after washing in neutral 70 per cent alcohol, placing
them in alkaline alcohol (1 per cent ammonia in 80 per cent alcohol)
4. Run up the alcohols, 80, 95, and 100 per cent, 14 hour e^ch.-
Pour off half the 100 per cent alcohol and add an equal amount of
xylene. When the diffusion currents disappear, transfer to pure xylene
and leave until the embryo is transparent. In rainy weather, or when
100 per cent alcohol cannot be obtained, phenol-xylene (phenol crys-
tals, 25 grams, and xylene, 75 cc.) may be substituted. /
5. Remove the embryo from the cover glass (if it has not^ already
Serial Sections 339
detached itself) and trim tiie surrounding blastoderm to the form of
an oblong or circle. Arrange a clean slide on the mounting diagram,
as described for the frog, place broken bits of cover slip for support,
and mount the embryo in Canada balsam or clarite with the same
side uppermost as when the egg was opened. Put the slide away
where it may lie flat and free from dust until the balsam has hardened.
This will take at least a week, after which the slide may be cautiously
cleaned and studied. The process may be hastened by drying the
slide in a paraffin oven.
The Pig
Embryos up to 10 mm. body length may be prepared as whole
mounts' by staining in dilute borax carmine, destaining until only a
trace of color persists, and mounting in Canada balsam. The time
spent in each alcohol should be at least I hour for the larger embryos.
SERIAL SECTIONS
In the preparation of serial sections of an embryo, the fixed material
is (1) embedded in a suitable matrix and (2) sliced into extremely
thin sections, wliich are (3) mounted in serial order upon slides. The
embryo may be stained before or after sectioning.
EMBEDDING." There are two principal methods of embedding, in
paraffin or in celloidin. For especially delicate objects, the best results
are obtained by a combination of these methods,.the embryo being
first impregnated with celloidin in order to avoid the shrinkage (about
10 per cent) caused by paraffin embedding, and the block of celloidin
thei^ immersed in paraffin so that ribbons of serial sections may be cut.
In spite of the shrinkage caused by paraffin, the necessity of having the
sections adhere to each other to form a ribbon (page 341) has resulted
in the almost universal use of paraffin sections.
EMBEDDING IN PARAFFIN. In preparing the first few embryos for sec-
tioning, it is advisable to stain, dehydrate, dealcoholize, and clear as
if for a total mount, i Later, the staining may be omitted until after
the sections are affixeijl to the slide.
1. After clearing in' xylene, which should be done in a warm place,
for example, the lowTtemperature oven at about 40°C., pour off half
the xylene and add ap equal amount of paraffin chips. A paraffin of
about 55°C.' melting! point, obtained by mixing commercial paraffin
with parawax, should be used. The parawax, unfortunately, varies
in melting point, so that the formula is empirical. A rubber paraffin.
Tissue mat, now on the market, is better for frog embryos. The
embryo may be left in this xylene paraffin for 2 days.
340 Embryological Technique
2. If the mixture lias liardened it should again be melted in the
low-temperature oven. Fill a clean stender dish with melted paraffin
transfer the embryo to this, and place in the high-temperature oven
at about 56°C. (or 1 degree above the melting point of the paraffin
used) for not more than 2 hours. The xylene-paraffin should be dis-
carded. Take care not to get any xylene in the high-temperature
oven or in the paraffin used for the final embedding.
3. Smear the interior of a small watch glass with Vaseline, and fill
it with fresh melted paraffin. Transfer the embryo to this, making any
necessary adjustments in position- with a heated needle. Place the
embryo dorsal side up, and note the position of the head. .Cool the
surface of the paraffin by blowing on it gently until it is congealed.
Then plunge it immediately into a dish of cold water or waste alcohol
and leave it there for 5 minutes. Mark the block for identification.
Objects may be left in paraffin indefinitely.
4. On removing the block of paraffin from its container, examine
for the following flaws:
a. Air bubbles, if they are not near the embryo, may be removed
with a hot needle. Otherwise it is better to trim the block close to
the embryo, put it into melted paraffin, and re-embed.
h. Milky streaks are due to the presence of xylene. These will
crumble during sectioning, so that it is best to re-embed if they occur-
near the embryo.
c. If the paraffin has ' fallen" in the center, it is because the sur-
face was cooled too long before the block was immersed in the water.
If any part of the embryo is exposed, it must be re-embedded.
SECTIONING AFTER PARAP;FIN EMBEDDING. Before sectioning the first
embryo, be sure that you understand the mechanism of the mjerotome
and have practiced the technique of sectioning on a block ôf paraffin.
There are three standard planes of sectioning corresponding to the axes,,
of the body (Fig. 255)} Transvers'esections are obtained by cutting the
cephalic end of'the body first, with the knife entering the left side.
Sagittal sections are made by cutting the right side first, with 'the knife
entering the ventral surface. Frontal sections are made by com-
mencing at the dorsal surface, the knife entering the left side. • I t is
best to begin with transverse sections. '
est
Attach the paraffin block to the object-carrier of the microtome
'^ In transverse sectioning of embryos having a marked torsion of the head, as in
the 72-hour chick embryo, it is best to cut the cephaUc end first, hut with the knife
entering the ventral side of the blastoderm. This procedure permits a closer
trimming of the paraffin block, which will then yield a ribbon with a compact
series of sections that may be mounted on fewer slides. '
Serial Sections 341
in the proper manner to obtain the type of section desired. This is
done by heating the surface of the carrier until it will just melt paraffin,
pressing the block against it in the desired orientation, and lowering
into a dish of cold water. A little melted paraffin may be poured
aroun.d the base of the block and this again cooled to secure additional
support.
L
Transverse
Fig. 255. Diagram to show method of orienting embryo with reference to micro-
tome knife according to type of section desired.
2. Place the object-carrier in the microtome and, after orienting

the block with respect to the knife, trim it so that/the end of the block
is a perfect rectangle with one of the longer sifles parallel to the knife
edge. If one of the angles is cut off slightly there will ,be a series of
indentations in'the ribbon, which will assist in orienting the sections
on the slide!
3. If microtome knives are not available, place a new safety-razor
blajde (Autostrop type) in the holder provided, allowing the edge to
project between Yig and iVs inch. Screw the holder in the knife-carrier
so that the edge ofthei blade is tilted inward about 10° from the
perpendicular. '
4. Set the regulator for 20 microns (thousandths of a millimeter).
5. Run the feed screw as far back as it runs freely; do not force it.
6. Advance the kriife-carrier until the edge of the blade just clears
the block.
7. Release safety Icatch and turn the wheel steadily until the knife
begins to cut the block. Cut slowly, msiking necessary adjustments to
the block and knifej until you are cutting a perfectly straight ribbon
without wrinkles or splits. The principal causes of trouble and their
.remedies are:
a. The ribbon curls to right or left. This happens because (1) the
342- - ' Embryological Technique
block is thicker on the side away from which the ribbon curls, or
(2) the knife is duller on the side toward which the ribbon curls.
Remedy: (1) trim the sides of the block parallel; (2) shift the knife
to one side.
b. The sections curl and the ribbon is not continuous. This is due
to (1) too much tilt of the knife, (2) too hard a grade of paraffin, or
(3) too cold a room. Remedy: (1) lessen tilt of knife; (2) re-embed
in softer paraffin; (3) move microtome to warmer place, light an
electric light or micro-Bunsen burner near microtome, or cut thinner
sections.
c. The ribbon wrinkles badly. This is caused by (1) too little tilt
to thelsnife, (2) too soft a grade of paraffin, (3) too warm a room, or
(4) a dull or dirty knife. Remedy: (1) increase the tilt of the
knife; (2) re-embed in harder paraffin; (3) move to a cooler room, or
cool the knife and block by dropping alcohol on them and blowing
vigorously, or cut thicker sections; (4) clean knife edge with cloth
moistened in xylene or shift to a new place on the knife.
d. The ribbon splits lengthivise. This is due to (1) a nick in the
knife, (2) a bubble in the paraffin, or (3) dirt on-the knife edge or
side of the block. Remedy: (1) shift to new cutting edge; (2) paint
surface with thin celloidin; (3) clean knife edge and block.
e. The sections refuse to ribbon; they fiy apart or cling to the knife
or the block. This is due to the electrification of the sections caused
by unfavorable atmospheric conditions. Many remedies have been
suggested; usually it is advisable to wait for more favorable condi-
tions, or use a radioactive discharger. ,
8. Remove the ribbon in 6-inch lengths with a camel's-liair brush
and arrange these in order, shiny side down, in a shallow cardboard
box. Avoid air currents of all kinds. The ribbons may be covered and
put away in a dust-free place if the room is not too warm. It is better
to affix them to slides as soon as possible;
AFFIXING P.^RAFP'IN SECTIONS TO THE SLIDE
f
1. Prepare a mounting diagram by laying off the outline of a slide

as before, but enclose in this the outline of a long cover glass (24 by
60 mm. approximately) and leave space for a label on the right-hand
side.
, 2. Glean a slide thoroughly by washing with acid alcohol and then
distilled water. Place this over the mounting diagram and brush 'over
the surface above the outline of the cover glass with the following
dilute solution of egg albumen:
Serial Sections 343
Egg albumen, beaten and skimmed 50 cc
Glycerin 50 cc
Filter and add thymol 1 crystal
Dilute 2 drops of this to distilled water 25 cc
3. Cut the ribbon into lengths about 20 per cent shorter than the
length of the cover glass. Using the wet brush from which most of the
albumen solution has been squeezed, pick up these lengths and arrange
them on the albumenized slide so that the sections will follow each
other like the words on a printed page. The shiny side of the ribbon
should be next to the slide. Great care should be taken to lower the
ribbon slowly so as to prevent the formation of air bubbles beneath it.
4. Carefully warm the slides on a warming plate or a piece of plate
glass, previously heated in the paraffin oven, until the sections are
expanded and perfectly smooth. If bubbles appear beneath the rib-
bon, prick them with a hot needle while the ribbon is still soft and hot.
Drain off the surplus water, carefully realign the sections, mark the
slides^ with a glass-marking crayon, and set them away in the low-
temperaturesoven to dry, at least 2 days. They may be kept indefi-
nitely in this condition if not exposed to dust.
STAINING SERIAL SECTIONS. When the embryo has been stained be-
fore sectioning, it is necessary only to remove the paraffin, replace with
Canada balsam, or clarite, and cover, if the stain proves to be satis-
factory. Sometiines, however, it is advisable to strengthen or weaken
the stain or to add a contrasting dye.
To EXAMINE STAIN. Before proceeding further, the quality of the
stain should be examined by placing the slide, section side toward
you, in a Coplin'staining jar of xylene. After 5 minutes, wipe the
back 'of the slide dry with a paper towel and examine immediately
under a microscope. CAUTION: xylene evaporates very rapidly. Get
the slide back in the jar of xylene as fast as possible. If satisfactory,
mount at once (see bel()w),.
To STRENGTHEN A WEAK STAIN _
1. Xylene, 5 minutes. '
2. Xylene and absolute alcohol (equal parts), 5 minutes.
3. Absolute alcohol, 5 minutes.
4. 95%, 80%, 70% alcohol, 1 minute each.
5. Distilled water, 1 njinute.
6. Stain, undiluted, as required.
7. Distilled water, 1 minute.
8.' 70%, 80%, 95% alcohol, 1 minute each.
9. Absolute alcohol, 5 niinutes.
344. ' Embryological Technique
10. X}'!ene and absolute alcohol (equal parts), 5 minutes.
11. Xylene, 5 minutes.
To WEAKEN A.N INTENSE STAIN

Steps 1-4 as above.
5. Acid 70% alcohol, as required.
6. Rinse in 70% alcohol, 1 minute.
7. Alkaline 70% alcohol, 5 minutes.
Steps 8-11 as above.
To CouNTEESTAiN, In Older to differentiate the parts of the embryo
more sharply, it is often desirable to add a second stain contrasting
with the first. The stains that have been employed in the previous
exercises are nuclear dyes; that is, when extracting by acid alcohol, the
color will persist in the nucleus after it has been washed oujt of the
cytoplasm. The second stains affect the cytoplasm and should con-
trast in color with the nuclear stain employed. After borax carmine,
a blue stain (indigo-carmine, saturated solution in distilled water)
or a green stain (indigo-carmine prepared as above and mixed with"
saturated aqueous solution of picric acid in-equal parts) is useful.
After hemalum a 0.1 per cent solution of eosin in 95 per cent alcohol
is good.
1. Run down the alcohols to the stage corresponding to the medium
in which the counterstain is dissolved (water for indigo-carmine and
picro-indigo-carmine; 95 per cent alcohol for eosin).
2. Stain (5 minutes for indigo-carmine and picro-indigo-carmine;
10 seconds for eosin).
3. Run up the alcohols to xylene'and mount.
To ]\IouNT SECTIONS AFTER STAIN IS SATISFACTORY. Wipe back and
sides of slide dry with paper toweling. Add about 3 drops of Canada
balsam or clarite. Place tip of needle (or forceps held in left hand)
to left of area to be covered.- Dip left end of cover slip in benzene,
rest it against needle, and lower gently with-forceps. This should be
practiced several times before trying to cover sections. It must be
done rapidly so that xylene will not evaporate before sections are
covered.
STAINING WITH HEIDENHAIN'S HEMATOXYLIN. This is one of the
most) important embryologicai stains.
1. Remove the paraffin from the sections and run down the alcohols
to distilled water. N.B. If embryo has been stained before sectioning,
the color must be removed by acid alcohol, and the acid neutralized
before proceeding.
2. Four per cent aqueous solution of iron alum, 1 hour to overnight.
Embryological Drawings 345
3. Rinse in distilled water and place in 0.5 per cent aqueous solution
of hematoxylin, same time as in the iron alum.
4. Rinse in distilled water and return to the iron alum until sections
are a pale gray. Check from time to time by rinsing in distilled water
and examining under microscope to see that the desired structures are
still visible. N.B. Many investigators prefer to destain in a saturated
aqueous solution of picric acid, neutralizing with running water until
gray color is restored.
5. When the embryo is sufficiently destained, wash in running water
for 20 minutes, or in distilled water, with frequent changes, for 2 hours.
6. Run up the alcohols, clear, and mount. .
FucHSiN AND PICKO-INDIGO-CARMINE. This polychromatic stain is
especially fine for.organogeny.
1. Remove the paraffin and run down the alcohols to distilled water.
2. Stain in basic fuchsin, saturated aqueous solution, 20 minutes.
3. Rinse in distilled water and place in picro-indigo-carmine for
5 minutes.
Picric acid, saturated aqueous solution 50 cc.
Indigo-carmine, saturated aqueous solution 50 cc.
4. Pass -rapidly through 70, 95, and absolute alcohol into xylene-
alcohol. The green dye is extracted most rapidly by the 70 per cent
alcohol, the red by the absolute. Only experience will teach the right
time allowance for each alcohol.
5. Clear in xylene and mount.
TECHNICAL RECORDS
Not the least important part of technique is the keeping of exact
records covering every technical operation. For each embryo there
should be a card, giving the following data:
i
1. Kind of embryo and stage of development.
2. Method of fixation, time and date. _
3. Bulk staining, time and date.
4. Method of embedding, time and date.
5. Plane and thickness 'of sections and date.
6. Slide staining, time and date.
7. Method of mounting' and date.
8. Name of preparatorj'
EMBRYOLOGICAL DRAWINGS
Free-hand drawings of microscopic objects can only approximate
an accurate representation. However, great pains should be taken to
346 • Embryological Technique
secure at least accurate proportions, neat and clean-cut lines, arid
complete labels. Accurate outlines can be secured by the aid of the
camera lucida, various types of projection apparatus, or micro-
photography.
EQUIPMENT. The student will need a hard lead pencil (4H), a
medium pencil (HB), blue, red, and yellow pencils, and an eraser.
FEEE-HAND DRAWING
1. Lay off the space to be occupied by the drawing, by placing four
dots at the corners. Rule in two lines, intersecting at right angles in
the center of this space. These will represent the dorsoventral and the
dextrosinistral axes, if the drawing is to be of a transverse section.
2. Measure the corresponding axes of the sections by means of the
ocular micrometer (see below), multiply by the desired magnification of
the drawing, and lay off these magnified measurements on the cross
lines already drawn. The following magnifications are recommended:
for the 24-hour chick, 60 X ; for the 33-hour chick, 50 X ; for the 48-
hour chick, 40 X ; for the 72-hour chick, 30 X ; for the 10-mm. pig, 20 X.
3. Draw in a careful outline of the section and of the internal struc-
tures, paying particular attention to the proportions, which should
be measured with the ocular micrometer and laid off on the axes at
the proper magnification.
4. On one side of the dorsoventral axis, all structures should be
colored in accordance with the following scheme: ectoderm, blue;
mesoderm, red; and endoderm, yellow.
5. Label all structures represented in the section, using broken lines
at right angles to the long axis of the paper to connect the label with
the structure indicated. ,
6. Identify the drawing fully, by means of a serial number, the
species, and stage of development, the number given to the' series,
slide, and section, the type of sections, and the amount of magnifica-
tion. Example: No, 23, Chick, 48 hours. Series 1102, Slide 2, section
28, transverse section 50 X. If a drawing lias already been made of
the total embryo or a total mount, indicate on this, by meaHs of a
heavy ruled line, the position of the section just drawn, and number
this line with the serial number of the section.
MICROMETRY. The unit of measurement in microscopy is the micron,
(/i).' I t is the one-thousandth part of a millimeter. Measurement
of microscopic objects is performed with the aid of micrometers, of
which there are two types, the stage micrometer and the ocular microm-
eter. The former is a glass slide, in the center of which, under a. cover
glass, is a line, usually 2 mm. long, divided into 200 equal parts, each
of which, therefore, is equivalent to 10 ix. The ocular micrometer is
Ehibryological Drawings 347
a glass disc, placed in an ocular at the level of the ocular diaphragm,
on which is engraved a scale with arbitrary subdivisions. Some
oculars are furnished with a draw tube so that the upper lens of the
system may be focused more sharply upon the scale. The value of the
divisions indicated on the scale varies according to the amount of mag-
nification of the real image, and so must
be obtained for each objective inde-
pendently, according to the following
method:
1. Set up the microscope, taking par-
ticular care to secure the proper tube
length.
2. Focus the eye lens on the ocular
micrometer scale by means of the ocular
draw tube. Focus the objective on the
stage micrometer.
3.-Make the lines of the stage mi-
crometer parallel with those of the ocu-
lar micrometer, and determine the
value of the divisions of the ocular
micrometer in terms of those of the
stage micrometer. Thus, if it requires
10 spaces of the ocular micrometer, and
the latter is equal to 0.1 mm., then the
value of a single space of the ocular
micrometer for that particular objective
Fig. 256. Diagram showing prin-
and at that -{iarticular tube length is ciple of the'Abbe camera lucida.
0.01 mm. or 10 ix.' Determine the value Path of image seen in microscope
of the ocular micrometer for each ob- shown in broken lines, that on
jective in the same way. drawing paper shown in unbroken
lines. {From Gage.)
ABBE CAMERA LUCI'DA. , This is an
attachment which reflects the light from the drawing board, by means
of a mirror, to a silvered prism (whence the ligKl is reflected to the
eye) superimposed on the image of the object which is transmitted
through a small hole in the silvered surface of the prism directly above
the ocular of the mici;osQope (Fig. 256).
1. Attach the .camera toythe draw tube of the microscope in such a
way that the-mirror proj'ecps to the right,'and the opening in the prism
lies above the center of the ocular.
2. Extend the mirijor arm to its greatest length and set the mirror
at an angle of 45°. The mirror arm must be parallel to the drawing
board.
348. ' Embryological Technique
3. Try various combinations of objectives and oculars until an image
of the desired magnification appears on the paper. Magnifications
intermediate to those obtainable in this way may be secured by varying
the tube length or by raising or lowering the drawing board. If the
stage of the microscope interferes with the drawing, the mirror should
be set at an angle of 40° or 35° and the drawing board tilted toward,
the microscope at an angle of 10° or 20°, respectively, by means of
wooden wedges. If the image is stronger than the reflection of the
pencil point, a smoked glass may be replaced beneath the prism, or the
aperture of the iris diaphragm may be reduced. If the reflection of
the pencil is stronger than the image, smoked glass may be placed at
the side of the prism or the amount of light falling on the paper
reduced by means of a screen.
4. Draw in the outlines of the sections and the larger internal struc-
tures. The details may be added free hand.
5. Remove the slide and substitute a stage micrometer. Trace in
part of the scale by means of which both the magnification of the
drawing and the absolute size of the object may be computed readily."
PROJECTION APPARATUS. Where many drawingsâre to be made, as
in the case of reconstructions, some form of apparatus by means of
which the image of the section may be projected directly upon the
paper is very helpful. There are many types of. projection apparatus,
directions for the use of which may be obtained with the instruments.
A photographic enlarger can be used very successfully.
PHOTOMICROGRAPHY. The photography of minute objects with the
aid of the microscope is of great assistance in embryology. However,
the methods are so difficult, the apparatus so complex, expensive, and
delicate, and the process requires so much technical knowledge and
skill, that photomicrography.has been considered a field too advanced
for the beginning student. The motion-picture camera has been
adapted for use with the microscope, and excellent results have already
been obtained. - '
RECONSTRUCTION
After an embryo has been sectioned, it is sometimes necessary to
reconstruct some part of it from the sections. There are two important
methods: graphic reconstruction, in which a geometric projection of a
•sagittal section, for example, might be made from transverse sections;
and plastic reconstruction, in which magnified replicas of each section
are made of wax and piled together so as to make an enlarged model
of the object to be studied. A complete series of sections of iuniform
Reconstruction 349
thickness and accurate orientation is required for either type of recon-
struction, and an outline drawing of the embryo before sectioning is
of great assistance.
T H E GRAPHIC METHOD (OF H I S ) . This method can best be described
by giving practical directions for a particular problem, e.g., to prepare
a geometrical sagittal projection 20X of the neural tube of a 10-mm.
pig embryo from a series of transverse sections 20 jn in thickness.
1. From the lateral view of the embryo drawn before sectioning,
make an outline drawing 20 X.
2. Draw a median line corresponding to the cephalocaudal axis, the
length of which, in this case, should be 200 mm.
3. Count the number of sections in the series, in this case, 500.
4. Lopate the position of each transverse section drawn on the
median line of the outline. Thus if the most anterior section drawn
was the fiftieth of the series of 500 sections, it would be located at a
point one-tenth of the total length of the axis (200 /n), or 20 mm. from
the cephalic end.
5. Theoretically, each, section is at right angles to the median line,
but this angle may be greater or less as a result of variations in tech-
nique. Study each drawing of a cross-section in connection with the
drawing 'o'f the total embryo and determine the angle made by that
section with the cephalocaudal axis of the embryo. Draw in, at each
point located on the median line, a cross line at the proper angle so
determined. These lines represent the dorsoventral axes of the trans-
verse sections. • Their lengths should correspond with those of the
dorsoventral axes of the drawings of the transverse sections previously
made at the sanie magnification, 20 X.
6. 'Plot in on each section-plane line (dorsoventral axis) the dorsal
and ventrahboundaries of the neural tube as determined from meas-
urenaents of .the drawings already made. Interpolate by direct
measurement and magnification of these points on intervening sections.
7. Sketch in the contours of the neural tube by connecting up the
points which have just been plotted. Compare "the dra^ving with a
sagittal section of an embryo in the same stage of development.
PLASTIC RECONSTEUGTION. This method also will be indicated by
practical directions for'the reconstruction of a particular organ, in this
case, a model 50 X of tlie heart of a 10-mm. pig, from a series of trans-
verse section, 20 fn in thickness.
1. Prepare a number of wax plates of the proper thickness. In this
case, if every section is to be reconstructed, the thickness of the plates
must be 50 X 20 ft., or 1 mm. Nearly as good results can be obtained
by reconstructing every second section and making the plates twice as
350 Embryological Technique
thick. The wax is prepared according to the following formula:
Beeswax 6 parts
Paraffin, 56°C. m.p. 4 parts
Rosin, white lump 2 parts
Mix and melt.
Pour 130 grams of this wax into a pan with an inside measurement
of 500 X 280 mm., into which boiling water has been poured to a depth
of 15 mm. This amount of wax will make a plate 1 mm. in thickness.
Bubbles in the wax may be removed by playing the flame of a Bunsen
burner over the surface as it is cooling. As the surface hardens, cut
the edges free from the sides of the pan. When the wax has set but
is still malleable, roll up the plate and remove it to a soapstone slab,
where it is unrolled and allowed to cool.
2. With the help of a camera lucida or projection apparatus, prepare
outlines 50 X of the heart in all the sections in which it is found. Num-
ber the drawings consecutively and note the serial number of the
sections drawn, so that it will be possible to check the drawings later
if necessary. Note also whether the right and left sides of the drawing
actually correspond with the right and left sides- of the embryo or
whether this condition is reversed. This is very important, as a mis-
take at this point would render the reconstruction valueless.
3. Transfer the drawings to the wax plates by means of carbon
paper. Place the wax plates on a sheet of glass, and cut out the parts
to be preserved with a sharp scalpel, leaving bridges of wax to connect
. the parts which would otherwise be separated. These bridges are best
made in the form of arches bending toward the outside of the section.
4. Pile the sections in order, taking care to avoid the I'eversal of
right and left sides, and to get an accurate fit. It is best to group the
seqtions in piles of 10. A steady pressure of the hand will be sufficient
to cause the sections to adhere to each other. The bridges may be cut
away and stout pieces of wire substituted. Heat the wire at eachênd
and press into position. After the wire is set", the wax bridges are cut
away and the edges of the piece smoothed with a heated scalpel or
aluminum modeling tool.
5. When all the sections have been combined in groups of 10, these
groups should be united and the completed model smoothed in -the.
samei way. Such models may be painted or dissected, and mounted on
I wooden supports as desired. They are quite permanent if not exposed
to high temperatures. Plaster of Paris molds and casts may be made
from them in the customary manner.
Glossary
This glossary includes the technical vocabulary of vertebrate embry-
ology as used in the text of this book but does not include terms used
in classification and comparative anatomy. Technical words employed
in cytology, genetics, and experimental embryology are distinguished
by the abbreviated name of the particular science in parentheses, e.g.
(Cyt.). Synonyms are included with the definition but not always
indicated separately. For cross references to synonyms, see Index.
ABERRATION. (Cyt.) Irregularity in the number or constitution of the chromo-

somes, producing modifications in development. See Mutation.
AcRosoME. A body at the apex of the vertebrate sperm. Syn., perforatorium.
ADNBXA. Extraembryonic structures produced during development in the
amniotes'and discarded before birth or hatching, e.g., yolk sac.
AGGLUTIXATION. (Exp.) A reaction in which sperm collect in a clump under
the influence of an enzyme (fertilizin).
ALBUMEN. A tertiary egg envelope secreted by the wall of the oviduct in
amniqte animals and used as a foodstuff.
ALLANTOIS. ^ An extraembryonic sac formed in the development of the Amniota
as a diverticulum of the hind-gut.
ALLELE. (Gen.) One of two genes located at the same locus in homologous
chromosomes but inducing alternative expressions of a particular character. Syn.,
allelomorph.
AMITOSIS. A form of cell division in which no chromosomes appear. Syn.,
direct division. ,
AMNIOCARDIAC VESICLE, A region of the coelom in the anterior part of the chick
embryo contributing to the pericardial cavitj'. '
A M N I O N . An extraembryonic sac enclosing the embryo, found' only in the
amniota. ' " , *
AMNIOTA. Reptiles, birds, and mammals.
AMNIOTIC RAPHE. • The point where the amniotic folds meet and fuse. Syn.,
sero-amniotic or chorio-amniotic raphe.
AMPLEXUS. The sexual embrace assumed by amphibians during mating.
ANAMNIOTA. Cyclostomes, fish, and amphibia.
ANAPHASE. (Cyt.) T h a t phase of mitosis in which the chromatids (daughter
chromosomes) are separating from each other.
ANASTOMOSIS. The union of two parts of a branching network, e.g., blood
vessels.
ANDROGBNESIS. (Exp.) (The development of an egg which contains paternal
chromosomes only.
ANESTRUM. T h e period following metestrum in the female mammal.
ANGIOBLAST. A t^rm applied collectively to all cells participating in the forma-
tion of the blood vascular system. '^
ANIMAL (POLE OR HEMISPHERE). T h e region in which the polar bodies are
formed. Syti., apical (pol$ or hemisphere).
APPENDIX TESTIS. A poHi6n of tho Miillerian duct persisting in the adult male
mnmmal in nssociation with the tMtis.
3.'il
352 Glossary
ABCUAMA. Small blocks of connective tissue formed from the sclerotome and
taking part in the formation of vertebrae.
AREA OPACA. A region of the chick blastoderm immediately surrounding the
area pellucida. Here the yolk is in close connection with the cells of the blasto-
derm.
AEEA PELLUCIDA. The inner region of the chick blastoderm in which the body
of the embryo develops. Here the yolk is separated from the cells of the blasto-
derm by a cavity.
AKEA VASCULOSA. A region of the area opaca in which the vitelline blood vessels
develop.
ABEA viTELLiNA. A region of the area opaca surrounding the area vasculosa.
AsTES. (Cyt.) A group of fibers extending radially from a centrosome during
mitosis.
ATBIOPOHE. An aperture from an atrial chamber. Syn., spiracle.
ATTACHMENT POINT. (Cyt.) T h e region of a chromosome which is the first to
move toward the centrosome in the anaphase. Point where chromosomal spindle
fiber is attached. Presumably free irom genes. Si/n., kinetochore, chromooenter,
centromere.
ATSTOSCIMS. (.Cyt.) Aay chromosome except t h e X- or Y-sex chromosomes.
AUXOCYTE. (Cyt.) A germ cell just prior to the meiotic divisions. Syn.,-
meiocyte, oyte. See Oocyte, Spermatocyte.
AXIAL FILAMENT. T h e contractile element in the tail of a sperm.
AXIAL MESODERM. The region of the mesoderm nearest to the notochord, Syn.,
epimere.
BALANCER. Paired structures on the head of a urodele embryo which are used
as adhesive organs in place of suckers.
BLASTEMA. A group of cells prior to their organization into a definite tissue.
BLASTOCOEL. A cavity associated with the blastula. Syn., segmentation cavity.
BLASTOCYST. T h e type of blastula peculiar to mafhmals.
BLASTODERM. T h e sum total of blastomeres before gastrulation. "Especially the
living part of the hen's egg from which the embryo and all its membranes are
derived (Lillie).
BLASTODISC. The disc-shaped mass of protoplasm lying on the yolk in the ex-
treme type of telolecithal egg. Syn., germinal disc. ,
BLASTOMEBE. A cell arising during cleavage of the egg, prior to gastrulation.
BLASTOPORE. The aperture connecting the gastrocoel with the exterior. Closed
by the yolk plug in amphibia. Represented b y primitive streak' in the Amniota.
BLASTULA. A spherical or disc-shaped embryonic stage marking the end of
cleavage and just prior to gastrulation.
BLOOD ISLAND. An isolated area of mesenchyme in t h e splanchnic mesoderm
which will become a blood vesicle, one of the primordia of the vascular system..
BRACHIAL. Having to do with the fore-hmb.
BRANCHIAL. Having to do with the gills.
BRANCHIOMEBY. A form of metamerism associated with the visceral arches.
CELL LINEAGE. T h e study of the blastomeres, their origin and fate in later
development. Syn., cytogeny.
CENTROSOME. (Cyt.) A small body characteristic of the cell an^l occupying
the center of the aster during mitosis,(Boveri, 188S). Centriole used".as synonym
Glossary 353
by many cytologists who define centrosome as centriole plus clear substance
immediately surrounding it.
CEEEBROSPINAL. Pertaining both to the brain and the spinal cord.
CERVICAL. Pertaining to the neck, e.g., cervical flexure.
CHALAZA. Twisted albumen, the "strings" seen in white of egg.
CHEMOTAXIS. Movement in response to a chemical stimulus.
CHIMERA. An individual which has two different sets of genes represented in
different parts of the body, usually rising from chromosomal aberrations after
fertilization of the egg.
CHONDRIFICATION. T h e process of forming cartilage.
CHONDKIOBLASTS. Cartilage-forming cells.
CHONDROCBANIUM. That part of the skull originally cartilaginous.
CHORDA-MESODERM. T h a t part of the embryo which will give rise to the noto-
ohord and the mesoderm.
CHOBDA-'NEVBAL CRESCENT, A region in the protochordate egg from which is
derived the notochord and the neural plate.
CHORIO-ALLANTOIS. A membrane formed by the fusion of the wall of the cho-
rion and that of the allantois.
CHORION. 1. An extraembryonic sac external to and enclosing the amnion and
allantois. Found only in Amniota. Syn., serosa, false amnion.
2. An egg envelope formed by the cells of,the ovarian follicle.
CHOROID. Used with reference to delicate vascular membranes, e.g., choroid
layer of the eye, choroid plexus of the brain, etc.
CHROMATID. (.Cyt.) A half-chromosome. One of the four parts of a tetrad
(McClung, 1900),
CHROMATIN. (Cyt.) Nuclear material readily stained with, basic dyes.
CHROMATOPHORE. 'A cell containing a mass of pigment granules.
CHROMIDIA. [Cyt.) Granules in the cytoplasm having the staining reactions of
chromatin.
CHROMONEMA. {Cyt.) A slender thread of chromatin which becomes the core
of a chromosorqe during mitosis.
CHROMOSOME. {Cyt.) A mass of chromatin, containing matrix and one or two
chromonemata, apparent during mitosis.
CLEAVAGE. T h e division of the fertilized egg into blastomeres. Syn., segmen-
tation.
CLEAVAGE PATH. The p^th taken by the pronuclei during fertilization from
the point where they meet to their position in readiness for the first cleavage
division. , i
CLEIDOIC. The type of qgg characteristic of reptiles, birds, and oviparous mam-
mals, protected by a shell' (Needham, 1931).
COELOBLASTDLA. Spherical type of blastula with a central blastocoel (Haeckel).
COBLOM. T h e body cavity formed by the separation of the somatic and
splanchnic layers of roesoderin.
COLLECTING TUBULE. Part of nephric tubule leading to nephric duct.
COMPETENCE. {Exp.) ' T h e ability of an embryonic area to respond to the
action of an evocator. !
CONCRESCENCE. T h e coming together of parts of the embryo which were origi-
nall3' separate.
COPULATION PATH. T h e path taken by the male or the female pronuclei in their
approach towards each other.
354 Glossary
CORONA BAMATA. A. layer of follicle cells surrounding the mammalian egg' a t
ovulation.
CORPUS LTITEUM. A yellow substance secreted in the vesicular follicle following
ovulation in mammals.
COTYLEDON. A brush-like group of villi characteristic of the chorion in some
mammals, e.g., the cow.
CRANIAL. Pertaining to the head.
CROSSING OVER. {Gen.) A mutual exchange of corresponding regions between
two chromosomes during synapsis.
CRYPTS. Depressions in. the uterine wall for the reception of placental villi.
CUMULUS OOPHORUS. T h e mass of cells connecting the mammalian egg to the
wall of the vesicular follicle.
CYTB. The germ cell just prior to meiosis, either oocyte or spermatocyte.
CYTOKINESIS. (Cyt.) T h e phenomena displayed in the cytosome during
mitosis.
CYTOLOGY. T h e study of cells.
CYTOPLASM. The material of the cell exclusive of the nucleus.
CYTOSOME. T h e body of the cell exclusive of the nucleus.
CYTOTROPHODERM. T h e inner cellular layer of the trophoderm.
DBCIDUA. T h a t portion of the uterine wall cast off at parturition.

DECIDUA BASALIS. T h e portion of the decidua which contributes to the forma-
tion of the placenta.
DECIDUA CAPSULARIS. T h e portion of the decidua immediately investing the
chorion.
DECIDUA VERA. T h e portion of the decidua neither basaiis nor capsularis.
DECIDUATE. A type of placentation characterized by the destruction of maternal
tissue during implantation and loss of tissue at birth.
DELAMINATION.. Separation by splitting, involving division, migration, and re-
arrangement of cells.
DENTAL PAPILLA. T h e mesodermal portion of a tooth primordium.
DERMATOME. T h a t portion of a somite which contributes to the dermis of the
skin.
DERMOCRANIUM. T h a t portion of the skull which does not pass through a
cartilaginous stage in development. Syn., membranocranium.
DETERMINATE. A type of cleavage iii which the blaslomeres have not the poten-i
tiality of producing a complete embryo. Syn., mosaic type.
DETERMINATION'. {Ex-p.) T h e mode of development in which an embryonic
area will develop only in a particular way under any conditions in which develop-
ment is possible.
DEUTOPLASM. Lifeless material in the egg cytoplasm used as food.
DIACOEL. The cavity of the diencephalon. Syn., third ventricle.
e iESTRUM. The period intervening between metestrum and the foUowitig pro-
iim in polyestrous mammals.
DIFFERENTIATION. T h e act of becoming different. The appearance of unlike
parts and regions in the embryo.
DIGAMETY. T h e condition of having two different kinds of sperm (or eggs)
according to the number or kind of sex chromosomes represented.
DIPLOID. T h e number of chromosomes characteristic of somatic cells. Two
complete haploid sets.
Glossary 355
DiscOBLASTULA. A disc-shaped blastula characteristic of telolecithal eggs, e.g.,
the hen's egg (Haeokel).
DiVEKTicuLUM. A blind outpouching from a tubular structure.
DOMINANCE. (Gen.) Mendel's principle that, when two allehc genes are pres-
ent in the same fertilized egg, the effects of but one of them will be evident.
DOMINANT. {Gen.) A gene whose effects are apparent even in the presence of
its allele.
DUCTUS ARTERIOSUS. A pers-isting portion of the sixth aortic arch serving as a
connection between the pulmonary artery and t h e dorsal aorta, characteristic of
the mammalian fetus. &yn., arterial ligament.
DUCTUS VENOSUS. A vein running through the liver connecting t h e umbilical
vein with the hepatic vein, characteristic of the mammalian fetus.
DYAD. A chromosome composed of 2 chromatids.
ECTODERM. The outermost germ layer. Syn., epiblast,

ECTODEBMALIZATION. (Exp.) A modification of normal development b y which
a greater proportion of the embryo gives rise to ectoderm at the expense of the
other germ layers.
EGG ENVELOPE. Material enveloping t h e egg, b u t not part of the egg cell, e.g.,
vitelline membrane, albumen, etc.
EGG JELLYV T h e egg envelope secreted by the wall of the oviduct around the
amphibian egg.
EGG TOOTH. A horny structure developed on the beak of the chick before
hatching.- .
EJACULATION. T h e emission of sperm from the body.
EMBRYO. Any stage in the, development of the fertilized egg. Usually re-
stricted to stages incapable of obtaining food from external sources. I n human
embryology restricted to the period between the second week and the second
month.
EMBRYONIC DISC,_ T h e region of the mammalian embryo where the ectoderm
and endoderm are in close contact, comparable to the area pellucida of t h e chick.
EMBRYONIC KNOB. T h e inner cell mass of the mammalian blastocyst.
EMBRYONIC SHIELD. T h a t region of the blastoderm which will give rise to the
body of the embryo in fish.
EMBRYOTROPH.. T h e material obtained from breaking down maternal tissue
by the mammalian embryo prior to the establishment of the placental circu-
lation. I '
ENAMEL ORGAN. T h e qotodermal portion of the tooth_ primordium.
ENDOCARDIUM.' T h a t p i r t of t h e splanchnic mesoderm giving rise t o the inner
lining layer of the heart. •
ENDODERM. T h e innermost germ layer. Syn., entoderm, hypoblast.
ENBODEBMALIZATION. (Exp.) A modification of normal development by which
a greater proportion of' the embryo gives rise to endoderm a t the expense of the
other germ layers. • L
ENTEBOCOEL. • T h e mesodermal coelomic pouch characteristic of the amphioxus.
Syn., coelomic pouch, gut pouch.
ENTYPY. A type of gastrulation seen in rodents where the elongate embryonic
knob is covered with endoderm which is, therefore, external to the ectoderm of
the amnion.
EPARTERIAL BRONCHUS An unpaired lung bud.
356 Glossary
EPIBOLY. A mode of gastrulation characterized by the fact that the ectoderm
grows out over the endoderm.
EPIBRANCHIAL PLACODE, A placode formed in the region external to the gills
which coiltributes to the formation of the lateral hne organs and certain cranial
nerves. Syn., suprabranchial placode.
EPICABDIUM. T h a t part of the splanchnic mesoderm forming the outer layer
of the heart.
EPICHOBDAL BRAIN. T h a t portion of the brain lying dorsal to the notochord.
Syn., deutencephalon.
EPIDIDYMIS. Persisting mesonephric tubules which carry sperm from the mam-
malian testis.
EPIGENESIS. T h e theory that development proceeds from the simple to the
complex, opposed to the theory of preformation.
EPIMERE. T h a t portion of the mesoderm lying adjacent to the notochord and
from which the somites are f-ormed. Syn., axial mesoderm.
EPIMYOC.WDIUM. The epicardium and the mesoderm which will form the muscle
cells of the heart wall.
EPITHELIAL BODIES. Structures arising from the endoderm of the visceral pouches,.,
e.g., thymus, parathyroids.
EPONYCHIUM. T h a t part of the skin overlying the nails during fetal life.
EPOOPHORON. A vestigial structure comparable to the epididymis associated'
with the ovary of the female mammal.
EQUATION DIVISION. (Cyt.) A meiotic division in which the chromatids com- •
posing t h e daughter chromosomes are identical. Contrast reduction division.
EQUATORIAL PL.4TB. (Cyt.) The metaphase chromosomes as viewed at right
angles to the axis of the spindle.
ESTRIN. A hormone formed in the ovarian follicles.
EsTROUs CYCLE. A periodic series of changes in the mammalian uterus culmi-
nating in its preparation for the implantation of the fertilized egg.
EsTRUS. T h e period in which the uterus is prepared for implantation.
EVOCATOR. (Exp.) An agent, not necessarily living, or part of the embryo,
which calls forth a developmental reaction from a competent embryonic area.
ExocoEL. A cavity produced by the separation of the somatic and splanchnic,
layers of mesoderm beyond the limits of the embryonic body. Syn., extraembryr
onic coelom. - ' '
BXOGASTRULA. (Exp.) A type of gastrula produced experimentally in which
the mesendoderm is not enclosed by the'ectoderm.
EXPLANATION. (Exp.) The development of part of an embryo removed into
a nutrient medium. Syn., in vitro culture. /
EXTRAEMBRYONIC. N o t a part of the embryonic body.
/
FERTILIZATION. The entrance of a sperm (or sperm) into an egg thereby.in-
ducing development. - ^
EEBTILIEATION CONE, A mass of cytoplasm extending from the surface of the egg
and engulfing the sperm.
FERTILIZATION MEMBRANE. A membrane apparently lifted away from the surface
of the egg when fertilization is complete and produced by some modification of
the vitelline membrane.
FERTILIZIN. A substance secreted by the mature egg before fertilizatiqn (liillie).
Glossary 357
FETUS. A mammalian embryo which has attained the recognizable characters
of the species.
FIELD. (Exp.) T h e complex of physicoohemioal agents determining the pattern
of development in a given' area of the embryo.
FIELD DISTRICT. iExp.\ T h e region in which a field normally exercises its
activities.
FLEXURE. Bending, e.g.,-the cranial flexure, a characteristic bend of the brain
over the tip of the notochord.
FOLLICLE. A mass of cells forming an envelope; e.g., the one enclosing the
ovarian egg. The vesicular (Graafian) follicle is characteristic of the mammalian
egg before ovulation.
FORAMEN OVALE. An oval opening in the bony labyrinth of the ear. Syn.,
foramen vestibuli.
FORE-BRAIN. T h e most anterior of the three primary vesicles of the brain.
FoRE-GUT. The most anterior portion of the digestive tube.
FOVEA. A small unpigmented spot on the surface of the frog's egg under which
the nucleus is located prior to fertilization.
FREEMABTIN". A sterile female developed along with a male twin with which it
shares a common chorion, e.g., in cattle.
GAMETE. A mature germ cell, ovum, or sperm.

GAMETOGENESIS. T h e development of the germ cells.
GARTNER'S CANAL. Persistent remains of the mesonephric duct associated with
the vestibule in female mammals.
•GASTREA. A hypothetical animal supposed to be an extinct evolutionary stage
comparable to the vertebrate gastrula (Haeckel).
GASTROCOEL. T h e cavity of the gastrula. Syn., archenteron.
GASTROHEPATIC OMENTUM. Part of the ventral mesentery persisting as a con-
nection between the stomach a:nd liver.
GASTRULA. A stage in embryology in which the germ layers are separated from
each other.
GASTRULATIONI' ' The process by which the gastrula is formed.
GEIJE. (Gen.) Theoretically, a minute body, located in the ehromonema,
whose presence, absence, or modification induces definite effects in development.
"The unit of heredity."
GENETICS. T h e study of heredity.
GENIC BALANCE. (Gen.) Th,e theory that the development of the individual,
particularly with respect t6 the determination of sex, is due to the relative pro-
portion of the kinds of genes represented as well as to the'different kinds of genes.
GENITAL. Having to do 'with reproduction.
GENITAL RIDGE. An elevation along the mesial side of the mesonephros caused
by the multiplication of the gonia. The primordium of the gonad.
GENITAL TUBERCLE. A cresc^ntic ridge surrounding the base of the phallus, the
primordium of the labioscrotal swellings in mammals.
GENOTYPE. Individuals \Vith similar gene complexes.
GERM. T h e beginning'of a new individual. Often used for early stages in
development, i.e., during cleavage.
GERM CELL. Egg or sperrri or any cell ancestral to these.
GERM LAYER. One of^the layers of cells separated during gastrulation or later.
358 Glossary
GERM LINE. The genealogy of the germ ceils during the development of an in-
dividual. Syn., germ track, Keimbahn.
GERMPLASM. T h e germ cells in the body of an individual taken collectively.
GERM WALL. T h e advancing boundary of the blastoderm as it grows around the
yolk.
GESTATION-. T h e act of carrying the unborn young.
GILL PLATE. A thickening of the ectoderm in the embryo posterior to the sense
plate in which the visceral grooves are formed.
GLAND FIELD. An area of the fore-gut floor which takes part in the formation of
the tongue.
GOLGI BODY. iCyt.) An organelle in the cytoplasm of the cell demonstrable
with silver nitrate or osmium tetroxide; often forming a network. Syn., dic-
tyosome.
GONAD. Ovary or testis. Syn., germ gland.
GONE. One of t h e four cells arising from the two meiotic divisions (Sharp,
1934).
GONIOM. A germ cell in the gonad prior to the meiotic divisions. Oogonium
or spermatogonium.
GONOMERY. A phenomenon visible in the egg fertilized b y sperm of a different
species when the two sets of chromosomes remain distinct during clea\'age
divisions.
GRADIENT. (Exp.) A gradual variation in a given direction; e.g., axial gradient,
i.e., variation, along the egg axis from animal pole to veg;etal pole.
GRAFT. (Exp.) A portion of one embryo transplanted t o a different position in
the same individual or in a different individual. Syn., transplant.
GRAY CRESCENT. A erescentic area on the surface of the frog's egg appearing
after fertilization. I t is in this area that the dorsal lip of the blastopore is
formed.
GYNANDROMORP.H. An individual showing female characteristics in one part of
the body and male characteristics in another.
GYNOGENESIS. (Exp.) T h e development of an egg which contains maternal
chromosomes only, although development }B initiated by the action of a sperm.
t
HAPLOID. The number of chromosomes characteristic of the gamete in any par-

ticular species. Syn., monoploid.
HEAD FOLD. In the Amniota, a fold which marks the;: elevation of the head above
the blastoderm or embryonic disc. " "-
HEAD FOLD OF THE AMNION. The fold of the am'nio'n which envelops the head-of
the embryo. ,
HEMIPLACBNTA. T h e chorion plus the yolk sac and/or the allantois which serves
as, an organ to supply nutrition to the uterine young of marsupials.
HEMOBLAST. T h e earliest stage in the development of a blood corpuscle.
.HERMAPHRODITE. An individual possessing both ovary and testis.
'HETEROPLASTIC. {Exp.) A graft or transplant made from the body of one indi-
vidual to that of another belonging to the same species (Diirken, 1932). Note:
Some authors use this term to mean transplantation to a host of a different species.
HETEROZYGOUS. (Gen.) Possessing unlike genes at the same locus of homol-
ogous chromosomes. Syn., hybrid.
HIND-BRAIN. T h e most posterior of the three primary brain vesicles.
HIND-GUT. The most posterior region of t h e digestive tube.
Glossary 359
HISTOGENESIS. - The development of tissues.
HoLOBLASTic. A type of cleavage in which the entire egg is divided.
HOMOLOGY. A type of resemblance between structures based on structural rather
than functional identities. A very common error is to assume that homology is
based solely on developmental identities.
HOMOPLASTIC. (Exp.) A graft or transplant made into the body of the same
individual (Diirken, 1932). Syn., autoplastic. Note: Some authors use the term
when the graft is made to a different individual of the same species.
HOMOZYGOUS. [Gen.) Possessing identical genes at the same locus of homol-
ogous chromosomes.
HOMTJNCULUS. An imaginary miniature human adult supposed to exist in the
egg or sperm according to the theory of preformation.
HYALOPLASM. (Cyi.) The ground substance of cytoplasm.
HYPOCHORD. A temporary mesodermal rod of unknown significance lying under
the notochord of the amphibian embryo. Syn., subnotoehordal rod.
HYPOMEBE. That portion of the mesoderm farthest removed from the noto-
chord and giving rise by splitting to the coelom. Syn., lateral mesoderm.
HYPOPHYSIS. A solid or hollow structure usually arising from the stomodeum
and attaching itself to the brain, where it gives rise to the anterior and inter-
mediate parts of the pituitary gland. Syn., Rathke's pouch.
IDIOSOME. (Cyt.) The clear (chromophobic) area associated with the Golgi
bodies, usually surrounding the centrosomes. Syn., idiozome.
IMPLANT.^TION. 1. T h e process whereby the mammalian embryo establishes
itself in or "on the surface of the uterine wall.
2. (Exp.) The transplantation of a bit of tissue from one individual to an-
other into a cavity in the body which serves as a nutrient chamber. Syn.,
interplantation.
INCUBATION. The application of heat to the developing eggs, as in t h e brooding
of the hen.
INDECIDUATE. A type of placentation in which there is no destruction of ma-
ternal tissue. ,' • '
INDETERMINATE. .Cleavage in which the early blastomeres have each the poten-
tiality of producing a complete embryo if artificially separated. Syn., regulation
type. •
INDUCTION. (:Exp.) An effect produced on one part of the developing embryo
by another, as demonstrated !^y transplantation.
INFUNDIBULUM. That part' of the floor of the diencephalon to which the
hypophysis attaches itself. I t gives rise to the nervous part of the pituitary
gland. I
INTERMEDIATE MESODERM. T h a t part of the mesoderm from which the gonad
and kidney arise. Syn., mesomere.
INTERPHASE. The period in the life of the cell between mitotic divisions.
INTERRENAL. An endocrine gland arising from intermediate mesoderm. Be-
comes the cortex of the mammalian adrenal.
INTERSEGMENTAL. Passing between somites.
INTERSEX. (Gen.) An individual abnormal so far as its sexual characteristics
are concerned.
INTERSTITIAL CELL. A cell found in the interstices between the seminiferous
tubules of the testis. Supposed to have endocrine properties.
360 • Glossary
INTESTINAL LOOP. A loop of the intestine extending into the umbilical cord in
mammals.
INTESTINAL PORTAL. T h e opening between the mid-gut and the fore-gut (an-
terior) or the mid-gut and the hind-gut (posterior).
INVAGINATION. T h e movement of one surface into the interior of a cavity, as
in the gastrulation of t h e coeloblastula.
INVESTING BONES. Bones formed around and partially replacing others already
in existence.
INVOLUTION. T h e movement of cells into the interior along a definite line as in
the gastrulation of the frog's egg.
ISOLECITHAL. A type of egg characterized by an approximately equal distribu-
tion of the yolk. Syn., homolecithal.
ISTHMUS. A connection, as in the j'olk isthmus connecting the yolk in the cen-
ter of the hen's egg to t h e nucleus of Pander.
KARYOKINESIS. T h e phenomena displayed by the nucleus during mitosis.

KARYOLYMPH. T h e ground substance of the nucleus. Syn., nuclear sap.
KARYOPLASM. T h e substance of the nucleus. Syn., nvieieopiasm.
LABIO-SCROTAL SWELLINGS. The primordium of the labia majora (female) or

part of the scrotum (male) in mammals.
LACUNA. A gap, e^g., that portion of the gastrocoel roof devoid of endoderm
during the early period of gastrulation in amphioxus and t h e frog.
LAMINA TERMINALIS. A swelling on the floor of t h e embryonic brain, marking
the anterior end of the neural tube.
LANUGO. T h e fetal hair of mammals.
LARVA. A stage in development in which the individual obtains its food from
external sources, has an appearance markedly different from t h a t of the adult,,
and has not attained t h e power of reproduction.
LATEBRA. A central mass of white yolk in the yolk of. t h e hen's egg.
LATERAL MESODERM. T h a t part of the mesoderm which forms the lining of the
coelom (and exocoel). Syn., hypomere. ^ ~~
LIMITING SULCUS. A groove undercutting the body of the embryo, thus elevat-
ing it from ,the remainder of the blastoderm in telolecithal eggs.
LINKAGE. (Gen.) T h e continued association of two or more hereditary charac-
teristics due to the fact that the genes concerned are located in the same chromo-
some. .,
LIQUOR. A fluid, .e.g., liquor foUiculi—the fluid contents of the vesicular follicle
of mammals. ,
MACROLECITHAL. A type of egg containing a lafge amount of yolk. This type

of egg is always telolecithal. Syn., megalecithal.
MACEOMERE. A large blastomere, usually yolk-laden.
MARGIN OF OVERGROWTH. T h e rim of the germ wall.
MARGINAL BELT. A ring of blastomeres slightly above t h e equator of the am-
phibian blastula and intermediate in size between the micromeres and macromeres.
Coincides with the area originally occupied by the gray crescent.
MATURATION. T h e act of becoming mature. Especially the period in which
the meiotic divisions of the germ cells take place.
Glossary 361
MEATUS VENOSTJS. T h e channel formed by the confluence of the vitelline veins
before entering the sinus venosus.
MEIOSIS. The process by which the number of chromosomes is reduced from
diploid to haploid during maturation of the germ cells.
MELANIN. A black pigment formed in the cell.
MENSTRUATION. Hemorrhages characteristic of the primate estrous cycle.
MEEOBLASTIC. A type of cleavage in which the egg is not completely divided.
MEROGONY. T h e development of an enucleate egg when fertilized by a sperm.
MESECTODERM. Term applied to the outer layer of a gastrula containing ecto-
derm, mesoderm, and notochord cells before these are separated from each other.
Syn., "primary ectoderm."
MESENCHYME. Loose aggregates of embryonic cells not organized in a layer,
and derived either from mesoderm, or, in some cases, the neural crest.
MESENDODERM. Term applied to the inner layer of a gastrula containing endo-
derm, notochord, and mesoderm cells before these are segregated from each other.
Syn., mesentoderm, "primary endoderm."
MESOCARDIUM. Part of the ventral mesentery persisting temporarily in the
region of the heart.
MESOCOEL. Cavity of the mesencephalon. Syn., iter, aqueduct.
MESODERM. T h e middle germ layer, exclusive of the notochord. Syn., meso-
blast. s,
MESOHEPAR. Part of the ventral mesentery persisting in the region of the liver,
e.g., gastrohepatic omentum.
MESOMERE. 1. The intermediate region of t h e mesoderm, Syn., intermediate
mesoderm.
2. Sometimes, used for blastomeres intermediate in size between macromeres
and micromeres.
MBSONEPHROS. Functional kidney of Anamniota, an embryonic organ of Am-
niota.
MESORCHIUM. A double fold of the peritoneum supporting the testis.
MESOVARIUM. A double fold of peritoneum supporting the ovary.
METABOLIC. Pertaining to metabolism, the chemical reactions taking place in
protoplasm.
METABOLIC CELL. (Cyt.) A cell that is not dividing. Syn., resting cell.
METAMORPHOSIS. A more or less sudden change in structure and form: (1)
applied to the ti'ansformation of the larva into" the adult; (2) applied to the
transformation of the spermatid into the sperm, syn., spermioteleosis.
METANEPHROS. The functional kidney of the Amniota.
METAPHASE. {Cyt.) T h a t phase of mitosis in which th'e~attachment points of
the chromosomes occupy positions in a plane at right angles to the long axis of the
spindle. i
METAPLASM. (Cyt.) The lifeless materials contained within the cytoplasm,
e.g., yolk, pigment, etc.
METESTRUM. A period of the estrous cycle in which the destruction of tissue
during the preceding period'is repaired preparatory to the anestrum (Marshall).
MICROLECITHAL. A type of egg containing a small amount of yolk. Syn., oligo-
lecithal, meiolecithal. '
MICROMERE. A small blastomere, usually near the animal pole.
MICEOPYLE. An opening in, the chorion (egg envelope) permitting the entrance
of sperm.
362 • Glossary
MID-BRAIN. The middle vesicle of the three primary vesicles of the brain. '
MID-GUT. Middle region of digestive tube.
M I L K MDGB. A linear elevation on the ventral surface of the mammalian
embryo on which the mammary glands develop at intervals.
MiTOCHONDHiA. (.Cyt.) Small bodies in the cytoplasm, demonstrable with
such vital dyes as Janus green B and Janus red, and apparently having the
power of independent growth and division. Syn., chondriosomes.
MITOSIS. T h a t mode of cell division in which chromosomes appear and are
divided longitudinally. Syn., indirect division.
MORULA. A stage in blastula formation in the mammal during which no cavity
exists.
MOSAIC. {Exp.) A term applied to an egg or embryo in which the prospective
fate of the different regions is determined.
MiJLLERIAN DUCT. Oviduct.
MUTATION. (Gen.) A change in the composition or structure of a gene
whereby it induces new characteristics in development. Syn., point variation.
See Aberration.
MYELOCOEL. • The cavity of the myelencephalon. Syn., fourth ventricle.
MYOCARDIUM. T h e muscular layer of the heart.
MYOCOEL. A temporary cavity in a somite.
MYOTOME. That part of a somite which contributes to the development of •
muscles.
NEONYCHIUM. A horny pad filling the concavity of the claw in birds before
hatching.
NEOTENY. The assumption of sexual maturity in a larval stage, e.g., the axototl.
Syn., paedogenesis.
NEPHRIC. Having to do with the kidney.
NEFIIROCOEL. A cavity of the nephrotome.
NEPHROGENOUS. Giving rise to kidney tissue.
NEPHRON. The functional unit of a kidney, consisting of a nephric tubule and
its glomerulus.
NEPHBOSTOME. An opening from the nephric tubule into the coelom.
NEPHPOTOMB. A metameric portion of the intermediate mesoderm correspond-
ing to a somite of the axial mesoderm.
NEURAL. Having to do with the nervous system.
NEURAL CHEST. A ridge of cells at the line of fusion of the neural folds forming
a temporary connectjon between the neural tube and epidermis of the skin. Gives
rise to the ganglia.
NEURENTERIC CANAL, A connection between the neural tube and digestive tube
formed by the closure of the blastopore.
NEUROBLAST. Early embryonic nerve cell of the nervous system.
,,NEUROCOEL. Cavity of the neural tube.
NEIUROCRANIUM. T h a t ' p a r t of the cartilaginous cranium enclosing t h ^ brain
afld sense organs.
NEUROMBRE. A pseudometameric division of the neural tube.
NEUROPORE. A terminal opening of the neural tube in early development.
NEURULA. An embryo at the time the neural plate is visible.
NEURULATIOX. A term applied to the period during which the neui-al tube is
being formed.
Glossary 363
NoN-DisjUNCTiox. (Gen., Cyt.) A variety of chromosomal aberration. T h e
failure of chromatids derived from the dissimilar members of a synaptic pair to
s e p ^ r ^ e during the reduction (disjunction) division.
••yNoTOCHORD. An axial rod derived from the middle germ layer, characteristic of
all chordates in some stage of development. Syn., chorda dorsalis.
NUCLEI PDLPOSI. T h e intervertebral discs which represent the remains of the
notochord in higher vertebrates.
NUCLEOLUS. {Cyt.) A body in the nucleus. Syn., plasmasome.
NUCLEUS. That part of the cell containing the chromatin.
OCCLUDE. T o close, or fill, a cavity.

OLFACTORY. Pertaining to the nose or sense of smell. Syn., nasal.
OxTOOBNY. T h e hfe history of an individual organism.
OOCYTE. A female germ cell during the period of maturation.
ÔOGENESIS. T h e development of the germ cells of the female.
OOGONIUM. T h e fernale germ cell after the development of the ovary and prior
to maturation.
OOTID. A generic term for the o^'um and its polocj'tes. T h e cells produced by
the meiotic divisions of the oocyte.
OPERCULAR APERTURE. Opening oS the opercular (peribranchial) cavity on t h e
left side of a^ tadpole. Syn., "spiracle."
OPERCULUM. A cover. Especially with reference to the covering of.the internal
gills.
OPTIC. Having to do with the eye or sense of sight. Syn., ophthalmic.
ORAL. Having to do with the mouth.
ORGAN FIELD. ,{Exp.) T h e region from which a specific part of the embryo
will be formed.
ORGAN-FORMING AREAS. Regions of the embryo which in the course of normal
development will give rise to the primordia of particular sttuctiires.
ORGAN-FORMING SUBSTANCES. (Exp.) Substances formed in the egg and
segregated • into different blastomeres, resulting in a mosaic stage of develop-
ment.
ORGANIZER, (Exp.) A region characterized by self-differentiation and capable
of inducing organization in neighboring regions, e.g., the dorsal lip of the blasto-
pore in amphibia. Syn., organizator.
ORGANOGENY. T h e development of the organs from their primordia.
ORONASAL GROOVE, A groove connecting the mouth with the nasal pits.
OSSIFICATION. T h e proce'ss of bone formation.
OSTEOBLAST. A. cell concerned in bone formation.
OSTIUM TUBAE. T h e opening of t h e oviduct.
OTIC. Pertaining to the ear or sense of hearing. Syn., auditory, acoustic.
OTOCYST. T h e cavity of the inner ear. Syn., otic (auditory) vesicle.
OVIPAROUS. A term applied to those animals in which the new individual leaves
the body of the mother as an egg, i.e., enclosed in egg envelopes.
OviPosiTioN. T h e act o r discharging the eggs'from the body. See Spawning.
OVULATION. T h e discharge of the eggs from the ovary.
OVUM. T h e mature egg.j I n a strict sense the female germ cell after the meiotic
divisions and before fertilization. This stage does not exist in vertebrates as such
because the sperm enters the egg before the completion of the second meiotic
division.
364- ' Glossary
PARABIONTS. (Exp.) Embryos experimentally united side by side.
PAKADIDYMIS. A group of mesonephric tubules forming a small body near the
testis of the adult male mammal.
PARANUCLEUS. (Cyt.) A body found near the nucleus and composed of mito-
chondrial material. Syn., nebenkern.
PARAPHYSIS. A dorsal evagination from the roof of the diencephalon anterior
to the epiphysis. Primordium of the pineal eye of reptiles.
PARIETAL RECESS. A passage connecting the pericardial cavity with the abdomi-
nal cavity in the mammalian embryo.
PAROOPHORON. A mass of tissue derived from a group of mesonephric tubules
lying near the ovary and corresponding to the paradidj^mis of the male.
PARTHENOGENESIS. A method of sexual reproduction in which the egg develops
without fertilization by a sperm.
PARTURITION. The act of giving birth.
PENETRATION PATH. T h e path followed by the sperm immediately following its
entrance into the egg.
PERIBLAST. T h a t part of the blastoderm in which the cells are not completely
separated b y a plasma membrane. I n early cleavage there is both a marginal,
ring and a lower layer of periblast, the latter of which soon disappears.
PHALLUS. An elevation on the posterior ventral surface of the mammalian em-
bryo which is the primordium of the glans penis (male) or glans clitoridis
(female).
PHENOTYPE. A group of individuals possessing similar hereditary characteristics..
Cj. Genotype.
>. 'PLACENTA. An extraembryonic structure of mammals, serving as an organ of
interchange between fetus and mother.
PLACODE. An ectodermal plate-like thickening.
PLASMA MEMBRANE. {Cyt.) The outer membrane of the cytosome.
PLASMATBOPHODERM. Outer syncytial layer of the trophoderm after implanta-
tion. Sj/n., syncytiotrophoderm.
PLASTICITY. (Exp.) T h e ability to develop into parts of the body other than
those formed in normal development. --
PLASTID. (Cyt.) A body in the cytoplasm of plant cells having the power of
independent growth and division.
POLAR. Pertaining to the animal pole, of the egg.
POLAR BODY. One of the small cells formed during the maturation of the egg,
usually at the animal pole. Syn., polocyte.
POLAR FURROW. A groove at the animal pole of the egg, resulting from the
rounding up of the'blastomeres at the 4-cell stage.
POLARITY. The possession of unlike poles.
POLE. The apex of the animal or vegetal hemisphere.
POLOCYTE. One of the small cells formed during the maturation of the egg, usu-
ally at the anima,l pole. Syn., polar body.
PoLYESTRous. Mammals with several estrous cycles in 1 year.
Pol YiNVAGiNATioN. Method of segregating endoderm in the hen's egg accord-
ing to Pasteels. Individual endoderm cells migrate beneath the surface of the
blastodisc and spread out to form lower layer.
POLYSPERMY. The entrance of several sperm into the egg, as in the hen's egg.
POSTANAL GUT. The digestive tube posterior to the point where the proctodeum
joins the gut. Syn., postcloacal gut.
Glossary 365
PosTEEiOE TUBERCLE. A Swelling on the ventral surface of the brain floor, lo-
cated at the anterior end of the notochord and marking the line of separation be-
tween the prosencephalon and mesencephalon. Syn., tuberculum posterius.
PosTNUCLEAR CAP. A cup-shaped structure covering the posterior surface of the
nucleus in the head of the mammalian sperm.
PRECHORDAL BRAIN. T h a t part of the brain anterior to the anterior end of the
notochord. Syn., archencephalon.
PRECHORDAL PLATE. A small area of endodevm invaginated before the notochord
and hence lying in front of it after gastrulation.
PREFORMATION. The theory that the several parts of the adult are preformed
in the egg (or sperm). Cf. Epigenesis.
PHEORAL GUT. The digestive tube anterior to the point where the stomodeum
joins the gut. Syn., Seessel's pouch.
PRIMITIVE STREAK. An axial thickening of the blastoderm or embryonic disc
from which the notochord and mesoderm originate. Homologous with the blasto-
phore of Anamniota.
PRIMORDIAL GERM CELLS. The first stage at which the potential germ cells are
completely set apart from the soma cells. The stage in which the germ cells are
first recognizable in vertebrate embryology.
PRIMORCIUM. T h e first distinguishable stage in the development of a new
structure. Syn., anlage.
PROAMNION. The region just anterior to the head fold of the chick embryo,
containing no mesoderm. T h e head fold of the amnion develops in this region.
PROCTODEUM. An invagination on the ventrail surface of the embryo just anterior
to the tail which will unite with the hind-gut to form the cloaca.
PROESTRUM. The stage in the estrous cycle just prior to estrus.
PROGESTIN. A hormone formed b y the corpus luteum. / ,
PRONEPHROS. The first kidney formed by the embryo. Functional only in the
larvae of Anamniota.
PRONUCLEUS. The haploid nucleus of the egg or sperm as found in the fertilized
egg prior to the first cleavage division.
PROPHASE. {Cyt.) T h e phase of mitosis in which the chromosomes become
apparfent.
PROSOCOEL. . The cavities of the prosencephalon. Syn., lateral ventricle.
PROTOPLASM. The material of which living things are formed. Sometimes con-
trasted with metaplasm.
RAMUS. A branch, e.g., 6i a tepinal nerve.

RAUBER'S CELLS-. The remains of the trophoblast lying above the embryonic
knob in amnion formation'of some mammals (rabbit).
RECAPITULATION. The theory that the stages of embryology recapitulate stages
in the evolution of the systematic group to which the individual belongs.
RECESSIVE. (Gen.) A gjene whose effects are not apparent in the presence of
its allelomorph. _ i
REDUCTION DIVISION. (G'yt.) T h e meiotic division in which the unUke chro-
matids of the tetrad are separated from each other. Syn., disjunction division.
REGULATION EGG. (Espj) A type of egg with cleavage in which each of the
early blastomeres has t h e . capacity of developing a complete embryo when
separated.
RESORB. T O reabsorb, or remove by phagocytosis.
366 Glossary
RETICULUM. A network. (Cyt.) The chromatin network of the nucleus. '
RHOMBOIDAL SINUS. T h e region contained within the widely open neural folds
in the posterior region of the early chick embryo. Syn., sinus rhomboidialis.
SACCULE. That portion of the inner ear which gives rise to the cochlea. Syn.
sacculus.
SCLEROTOME. T h a t part of a mesodermal somite which contributes to the forma-
tion of the skeleton.
SECRETORY TUBULE. T h e part of the nephric tubule actually concerned in remov-
ing wastes from the blood.
SENSE PLATE. A thickening of the ectoderm from which the primordia of the
nose, lens, and inner ear originate.
SEPTUM. A partition wall, e.g., septum transversum, a wall of mesoderm sep-
arating parts of the coelom.
S I N U S TERMINALIS. T h e circular blood vessels marking the outer limit of the
area vasculosa of the yolk sac.
SITUS INVERSUS. A reversal ol left-right symmetry.
SOLE PL.\TE. A mass of the stratum corneum lying beneath the nail.
SOMATIC. (1) Pertaining to the body; contrast germinal.
'(2) Pertaining to the body wall; contrast splanchnic.
~ SOMATIC MESODERM. The outer layer of lateral mesoderm.
_ÔMATOPLEURE. The somatic mesoderm plus the ectoderm immediately adjacent
to it.
SOMITE. A metameric division of the axial mesoderm.
SPAWNING. The act of discharging the eggs of Anamniota.
SPERM. The mature male germ. cell. Syn., spermatozoon.
SPERMATID. T h e male germ cell after the completion of the meiotic divisions
but before metamorphosis.
SPERMATOCYTE. The male germ cell during the meiotic divisions.-
SPERMATOGENESIS.' T h e development of the male germ cells.
SPERMATOGONIUM. The male germ cell in the testis before the meiotic divisions.
SPINA BIFIDA. An abnormality in development in which the vertebral column is
cleft at its posterior end. >
SPINDLE. A mass of material in the form of a double cone lying bet^veen the
centrosomes during mitosis, and' involved in the mechanism of separating the
chromatids.
SPLANCHNIC. Pertaining to the'viscera^^ Contrast Somatic (2).
SPLANCHNIC MESODERM. T h e inner layer of lateral 'mesoderm.
•^SPLANCHNOCRANIUM. • T h a t part of the cartilaginous skull derived from the
visceral arches.
^SPLANCHNOPLEURE. T h e splanchnic mesoderm plus the endoderm immediately
adjacent to it.
SPONGIOBLAST. An epithelial cell of "the neural tube which gives rise to support-
ing elements or neuroglia/cells of the nervous system.
STEM CELL. A blastomere which divides into a soma cell and another stem cell.
. Eventually one of the stem cells divides to form 2 primordial germ cells.
STOMODEUM. An ectodermal invagination on the ventral surface of the head
which unites with the fore-gut to form the mouth.
STROMA. Connective tissue or supporting framework of an organ.
SUBSTITUTION BONES. Derm bones which replace cartilage bones.
Glossary 367
SUCKER. Adhesive gland characteristic of anuran larvae when first hatched.
Syn., cement organ, oral gland.
SUPRARENAL. A gland formed from neural crest cells which migrate to become
the medulla or inner portion of the mammalian adrenal.
SusTENTACULAR CELL. A nourishing cell, e.g., follicle cell of ovary or Sertoli cell
of testis.
SYNAPSIS. (Cyt.) The union of the paternal and maternal homologous chromo-
somes in the prophase of the first meiotic division. Syn., "pseudoreduction."
SYNCYTIUM. A multinucleate mass of protoplasm (Haeckel).
SYNGAMY. T h e union of two gametes. Syn., fertilization, zygotogenesis.
TELOBIONTS. (Exp.) Amphibian embryos experimentally fused head to tail.

TELOLECITHAL. Type of egg in which the yolk is accumulated in the vegetal
hemisphere.
TELORHASE. iCyi.) The concluding phase of mitosis, in which the daughter
chromosomes return to the reticular condition and the cytosome is divided.
TERATOLOGY. The study of abnormalities in development.
TETRAD. {Cyt.) A compound chromosome composed of 4 chromatids arising
by the splitting, of the two synaptic mates in the prophase of the first meiotic
division.
THIGMOTAXIS. Movement in response to a tactile stimulus.
THYROOLOSSAii DUCT. A temporary connection between the thyroid gland and
the pharynx near the base of the tongue.
TORSION, The twisting of the chick embryo so that it lies on its left side.
TRACHEAL GROOVE. A depression on the floor of the pharynx which is the
primordium of the trachea and lungs.
TRANSPLANTATION. {Exp.) The grafting of part of an embryo into the body
of another.
TROPHOBLAST. T h e outer layer of the mammalian blastocyst which contributes
to the chorion.
TuBERCULUM posTERius. A projection on the floor of the brain marking the
posterior boundary of the diencephalon.
UMBILICAL. Having to do with the navel. Hence used in reference to the cord
connecting the fetus with the placenta and any structures contained in the cord.
UNGUIS. A claw. ,
URACHUS. The canal cpnneqting the allantois and urinary bladder in mammalian
embryos. '
UROGENITAL. Pertaining to both excretory and reproductive functions. Syn.,
urinogenital. , !
UTRICLE. A bladder-like structure, e.g., utricle of the ear; prostatic utricle.
Syn., utriculus.
VEGETAL (POLE OR HEMISPHERE). At the extremity of the pola.r axis opposite

the animal pole. Syn., vpgetative, abapical, antipolar.
VELAR PLATE. An exteiision of the pharyngeal floor extending over the visceral
clefts and aiding in retaining solid particles while permitting the free passage of
water.
VILLUS. A projection; ei.g., chorionic villi.
VISCERAL. Pertaining to t h e viscera.
368 Glossary
VISCERAL CLEFTS. Openings connecting the pharynx with the exterior. Sy'n.
pharyngeal, branchial (in p a r t ) , gill clefts.
VISCERAL GROOVES. Ectodermal furrows which contribute to the formation of the
visceral clefts if completed.
VISCERAL POUCHES. Endodermal pockets which contribute to the formation of
the visceral clefts if completed.
VITELLINE. Pertaining to the yolk; e.g., vitelline vein carrying blood from the
area vasculosa of the yolk sac.
VIVIPAROUS. A term applied to those animals which bring forth the young in
an advanced stage of development.
WOLFFIAN BODY. Term applied to mesonephros.

WOLFFIAN DUCT. Term applied to mesonephric duct.
X-cHROMOsoME. (Cyt.) One of the paired sex chromosomes in most verte-

brates.
XENOPLASTIC. {Exp.) A form of transplantation in which the host belongs to
a different species (Diirken, 1932).
Y-CHROMOSOME. {Cyt.) A chromosome pairing with the X-chromosome in the

maje of most vertebrates.
OYoLK. A form of metaplasm found in the egg and used for food by the early
embryo. Syn., deutoplasm.
YOLK NUCLEUS COMPLEX. {Cyt.) The idiosome and associated mitochondria
in the oocyte.
YOLK PLUG. A mass of large yolk-laden cells protruding through the blastopore
of the amphibian egg.
SAC An extraembryonic sac of splanchnopleure surrounding the yolk.
YOLK-SAC PLACENTA. A form of hemiplacenta In which the bldod vessels are
derived from the area vasculosa of the yolk sac.
YOLK-SAC UMBILICUS. T h e region where the yolk is not surrounded by the
yolk sac until the development of the albumen sac. —
1
ZONA PELLUCIDA. A thick capsule with radial striations enclosing the human
ovuin. There is some uncertainty as to whether it is formed by the egg or by
folhcle cells.'
ZONE OF JUNCTION. T h e region of the germ wall of the chick blastoderm imme-
diately internal to the inargin of overgrowth. Here the cells are not sharply
separated from the underlying yolk. ^_
ZYGOTE. The cell formed by the union of two gametes. Syn., fertilized egg.
Bibliography
To list all the books and journals consulted in the preparation of this
book would increase its size unduly. The following references are
classified in the hope that they may be of service to students who desire
to obtain more information in special fields than can be given in an
introductory book.
ATLASES
Duval, M. 1884. Atlas d'embryologie.
Goette, A. 1874. Alias zur Entwickelungsgeschichte der Unke.
Keibel, F . (ed.) 1897-1938. . Normentafeln zur Entwicklungsgeschichte der
Wirbeltiere.
Kohlitiann, J. 1907. Handatlas der Entwickelungsgeschichte des Menschen.
Long, J. A. 1937. A Steroscopic Atlas of the Chick.
BIBLIOGRAPHIES
Biological abstracts, commencing with literature of 1926.
Concilium' Bibliographicum, card index, commencing with hterature of 1896.
(See also bibliographies in other references cited.)
Minot, C. S. 1893. "A bibliography of vertebrate embryology." Mem. Boston
Soc. Nat: Hist. 4:487-614.
COLLATERAL TEXTBOOKS
Barth, L. J. 1953. Embryology, revised edition.
Huettner, A. F . 1949. Fundamentals of Comparative Embryology of the Ver-
tebrates, Revised Ed.
McEwen, R. S. 1949. Vertebrate Embryology, 3rd Ed.
Richards, A. 1931. Outline of Comparative Embryology.
Wieman, H . L. 1949. An Introduction to Vertebrate Embryology, 2nd E d .
COMPARATIVE INVERTEBRATE EMBRYOLOGY

Dawydoff, C. 1928. Trîte d'embryologie comparee des invertebres.
Korschelt, E., and Heider, K. 1902-1910. Lehrbuch der vergleichenden Ent-
wicklungsgeschichte der wirbellosen Tiere.
Korschelt, E:, and Heider, K. 1936. Vergleichenden Entwicklungsgeschichte
der Tiere. I
MacBride, E . W. 1914. Textbook of Embryology, Vol. 1, "Invertebrates."
L
COMl»ARATIVE VERTEBRATE EMBRYOLOGY
I
Brachet, A. 1935. Traite d'embryologie des vertebres, 2nd Ed.
Chiarugi, G. 1929-1935; '^rattato di Embriologia.
Hertwig, 0 . (ed.) 1906. • Handbuch der vergleichenden und experim,entallen
Entwickelungslehre der Wirbeltiere, 6 volumes.
369
370 Bibliography
Jenkinson, J. W. 1913. Vertebrate Embryology.
Kellicott, W. E. 1913. Chordate Development.
Kerr, J. G. 1919. Textbook of Embryology, V o l 2, "Vertebrates Exclusive of
Mammals."
Nelsen, 0 . E . 1953. Comparative Embryology oj the Vertebrates. .
EXPERIMENTAI. EMBRYOLOGY
Allen, E. (ed.) 1939. Sox and Internal Secretion, 2nd Ed.

Bertalanffy, L. von, and Woodger, j . H. 1933. Modern Theories oj Develop-
ment.
Brachet, A. 1931. L'oeuj et les jacteurs de I'ontogenese.
Brachet, J. 1950. Chemical Embryology.
Brambell, F . W. R. 1930. The Development oj Sex in Vertebraten.
Child, C. M. 1915. Individuality in Organisms.
Child, C. M. 1941. Patterns atid Problems oj Development.
de Beer, G. R,. 1934,. Introduction to Experimental Embryology, 2nd Ed.
Dalcq. A . M. 1938. Form and Causality in Early Development.
Detwiler, S. R. 1936. Neuroemhryology,
Duesberg, J. 1926. L'oeuj et ses localisations germinales.
pUrken, B. 1932. Experimental Analysis oj Development (trans.).
Faure-Fremiet, M. E. 1925. La cinetique du developpement.
Huxley, J. S., and de Beer, G. R. 1934. The Elements .oj Experimental Em-
bryology.
Jenkinson, J. W. 1909. Experimental Embryology.
Jenkinson, J. W. 1917. Three Lectures on Experimental Embryology.
Korsehelt, E . 1927-1931. Regeneration and Transplantation.
Morgan, T. H. 1927. Experimental Embryology.
Morgan, T. H. 1934. Embryology and Genetics.
Needham, J. 1931. Chemical Embryology.
Needham, J. 19421 Biochemistry and Morphogenesis.
Newman, H . H . 1923. The Physiology oj\ Twinning.
Pincus, G. 1936. The Eggs oj Mammals.
RufSni, A. 1925. Fisiogenia. .
Russei!, E. S. 1930. The Interpretation of Development and Heredity.
Schleip, W. 1929. • Die Determination der Primitiventmcklung.
Spemann, H. 1938. Embryonic Development and Induction.
Waddington, C. H'. 1936. How Animals Develop. •
Waddingtoti, C. H . 1940. Organizers and Genes. ' <
Weiss, P . 1930. Entwicklungsphysiologie der Tiere.
Weiss, P. 1939. Principles of Development.
Windle, W. F . 1940. Physiology oj the Fetus.
GERM CELLS AND CHROMOSOMES
Cowdry, E, V. (ed.). 1924. General Cytology.

Kellicott, W. E . 1913. General Embryology.
Sharp, L. W. 1934. Introduction to Cytology, 3rd Ed.
Wilson, E. B. 1925. The Cell in Development and Heredity, 3rd Eji.
Bibliography 371
H I S T O R Y O F EMBRYOLOGY
Castaglioni, A. 1941. A History oj Medicine.
Cole, F . C. 1930. Early Theories oj Sexual Generation.
Locy, W. A. 1915. Biology and Its Makers, 3rd Ed.
Mayer, A. W. 1939. The Rise of Embryology.
Needham, J. 1931. Chemical Embryology, Vol. 1.
Needham, J. 1934. History of Embryology.
Nordenskiold, E. 1928. The History of Biology.
Russell, E. S. 1916. Form and Function.
Singer, C. S. 1931. The Story of Living Things.
LABORATORY MANUALS
Adamstone, F. B., and Shumway, W. 1954. A Laboratory Manual of Verte-
brate Embryology,'Zrd Ed.
Boy'den, E. A. 1933. A Laboratory Atlas of the Pig Embryo.
Harrison, B. M. 1950. Embryology of the Chick and Pig.
Lillie, F . R. 1919. A Laboratory Outline of Embryology.
Rugh, R. 1949. A Laboratory Manual of Vertebrate Embryology.
Vecchierello, H., and Worden, J. L. 1935. A Laboratory Manual of Vertebrate
Embryology.
Waite, F. C , and Patten, B. M. 1918. An Outline of Laboratory Work in
Vertebrate Embryology, Part I, "The Chick," 1925. Part I I , "The Pig."
Waterman, A. J. 1948. A Laboratory Manual of Comparative Vertebrate Em-
bryology.
Weiman, H. t . , and Weichert, C. K. 1930. A Laboratory Manual for Verte-
brate Embryology.
MANUALS O F EXPERIMENTAL EMBBYOLOGV

Adams, A. E. • 1941. Studies in Experimental Zoology.
Ha,rnburger, V. 1942. A Manual of Experimental Embryology.
Rugh, R. 1948. Experimental Embryology: A Manual of Techniques and
Procedures.
MONOGRAPHS, EMBRYOLOGICAL SERIES

Carnegie Institution of (Washington. Contributions to Embryology, Vols. 1-34.
SPECIAL V E R T E B R A T E EMBRYOLOGIES
Aniphioxus
Conklin, E. G. J932. "The embryology of Amphioxus." Jour. Morphol. 54:
69-151.
Conklin, E. G. 1933. 'The development of isolated and partially separated
blastomeres of Amphioxus." Jour. Exp. Zool. 64:303-375.
Frog
Marshall, A. M. 1893. Vertebrate Embryology.
372 Bibliography
Morgan, T. H. 1897. The Development of the Frog's Egg.
Pollister, A. W., and Moore, J. A. 1937. "Tables for the normal development
of Rana sylvatica." Anat. Rec. 68:480-496.
Rugh, R. 1951. The Frog, Its Revroduction and Development.
Shumway, W. 1940. "Stages in the normal development of Rana pipiens.
I. External form." Anat. Rec. 78:139-147. II. Identification of the stages from
sectioned material." Anat. Rec. 83:309-315.
Taylor, A. C., and KoIIros, J. J. 1941. "Stages in the normal development of
Rana pipiens larvae." Anat. Rec. 4:7-23.
Wright, A. H. 1914. North American Aniira.
Zeigler, H. E. 1902. Lehrbuch der vergleichenden Entwickelungsgeschichte der
niederen Wirbeltiere.
Chick
Hamilton, H. L. 1952. Lillie's Development oj the Chick, 3rd Ed.
Patten, B. M. 1951. The Early Embryo oj the Chick, 4th Ed.
Man
Arey, L. B. 1947. Developmental Anatomy, 5th Ed.
Hamilton, "VV. J., Boyd, J. D., and Mossman, H. W. 1945. Human Embryology.
Patten, B. M. 1946. Hitman Embryology.
Keibel, F., and Mall, F. P. 1910. Human Embryology.
Pig
Lewis, F. T. 1902. "The gross anatomy of a 12 mm. pig." Am. Jour. Anat.
2:211-226.
. Minot, C. S. 1911. A Laboratory Textbook oj Embryology, 2nd Ed.
Patten, B. M. 1948. The Embryology oj the Pig, 3rd Ed.
Wallin, E. 1917. A teaching model of a 10 mm. pig embryo. Anat. Rec.
5:17-45.
, TECHNIQUE
Belling, J. 1930. The Use oj the Microscope.
Conn, H. J. 1940. Biological Stains, 4th Ed.
Gage, S. H. 1941. The Microscope, 17th Ed.
Gray, P. 1952. Handbook oj Basic Micxptechnique.
Guyer, M. F. 193.6. Animal Micrology, 4th Ed.
Lee, A. B. 1937. The Microtomist's Vade-Mecum, 10th Ed.
McClung, C. A. 1937. Handbook oj Microscopical Technique, 2nd Ed.
Mueller, J. F. 1935. A Manual oj Drawing jar Science Students.
Norman, J. R. 1923. Methods and technique of reconstruction. Jour. Roy.
Microscop. Soc. 1923:37-56.
Index
Compound terms are iudexed under the first word, e.g., Dorsal aorta not Aorta,
dorsal. Synonyms are printed in italics and referred to the terms employed by
the authors. See also the Glossary. For details of development, see names of
organs or systems, not Chick, Frog, etc.
Abapical, see Vegetal hemisphere Amniotic cavity 106, 126

Abbe camera lucida, 347 Amniotic fluid, 129
Abdominal cavity, 197, 198, 200 Amniotic folds, 116, 317
Abducens nerve (VI), 274 Amniotic raphe, 129, 320, 323
Achromatic figure,'62 , Amphioxus, life history, 13
Acinus, 174 Amplexus, 53
Acoustic, see also headings beginning Ampulla, 288
Auditory, Otic Anal opening, 180
Acoustic ganglion, 274, 326 Anaphase, 60, 63, 65
Acoustic nerve (VIII), 276, 289, 308 Androgenesis, 148
Aodusticofacial ganglion, 274, 279, 280 Anestrum, 136, 137
Aeraniata, 117 Animal hemisphere, 33
Aerosome, 28, 45 Animal pole, 33
Adamstone, 11, 31, 170 Anterior cardinal vein, 226, 231
Adnexa, 115 chick, 319, 322
Adrenal gland, 7, 168, 212, 216, 218, 219 pig, 327, 328
Adrenahn, see Epinephrin Anterior caval vein, see Precaval vein
Aepyornis, 32 , Anterior intestinal portal, 184, 311, 315
Afferent branchial artery, 229 Anterior limb bud, 320, 324, 328, 329
Afterbirth, 145 Anterior lobe of pituitary, 172
Agglutination, 51 Anterior nar.es, 292, 293
Air chamber, 37 Anterior neuropdre, 109, 311, 314
Air sac, 192 Anterior velum, 267
Alar plate, 266, 267 Anterior vena cava, see Precaval vein
Albumen, 37 ., • Anus, 187
Albumen sac, 133 Aortic arch, 121, 228, 229
Alimentary canal, see Digestive tube chick, 319, 321, 322
Alkalinity, 167 frog, 229, 235
Allantoic artery, 230 man, 229
Allantoic fluid"l33 pig, 325, 327, 333
Allatitoic placenta, 138 i Apicol pole, see Animal pole
Allantoic vein, 230, 323 Appendages, 117, 248, 249
Allantois, 130. 131. 132, 133, 180, 188 Appendicular muscles, 255, 256
chick, 19, 20, 133, 185, 320 Appendicular "skeleton, 243, 248, 249
man, 23, 134, 219 | Appendix testis, 211, 219
pig, 140 Aqueous humor (of eye), 287
Allele, 71 | Arachnoid, 265
Alveolar glands, 260 Arbacia, 149
Alveolus, 173, 191, 192, 193 , Archencephalon, see Prechordal brain
Ambystoma, 146, 176 j Archenteron, see Gastrocoel
Ameloblasts, 173 ' ' I. Arcualia, 244
Amitosis, 59 • | Area opaca, 90
Amniocardiac vesicle, 129, 198, 311 Area pellucida, 90, 311
Amnion, 128 I Area vasculosa, 126, 133, 134, 311, 313
chick, 19, 20, 129, 131, 318, 319, 322 Area vitellina, 126
man, 23, 131 Aretynoid swellings, 193
rabbit, 132 Aristotle, 1, 8
373
374 Ind ex
Arteries. 228, 229 Blastomere, 79 •
chick, 237 Blastopore, 93
frog, 234, 235 Blastula, 82, 83
man, 238, 239 amphioxus, 13, li
Articular bone, 251 frog, 17
Artificial parthenogenesis, 6, 54, 147 chick, 20
Artificial sea water, 166 man, 21
Ascaris, 40 Blood-forming centers, 224
Aster, 61 Blood island, 222, 313, 319
Astylostemus, 188 Blood plasma, 222
Asymmetry, 151 Blood vascular system, 222
Atrium, 228 Blood vessels, 224
chick, 317, 320, 321, 322 Body formation, 19, 20, 23
frog, 303, 308 Body plan, 116
man, 238 Body stalk, 127, 324, 325, 330
pig, 325, 328, 333 Bombinator, 87, 96
Attachment region (of chromosome). Bone, 242
60, 61 Bone marrow, 224
Attraction (of sperm), 50 Bonnett, 3
Auditory, see also headings beginning Bony labyrinth (ear), 289
Acoustic, Otic Born, 151
Auditory nerve ( V I I I ) , 326 Bounoure, 41
Auditory ossicles, 289 Boyden, 192
Auditory placode, 288 Bowman's capside, 203, 329
Auricle, see Atrium Brachet, 5, 6, 9
Autonomic, see headings beginning ^Brachial plexus, 265, 328
Sympathetic VKBrain, 124, 263, 266, 267, 268, 311, 313
Autoplastic, see Homoplastic transplan- Branchiae, see External gills
tation Branchial, see aho headings beginning '
Autosomes, 68 Visceral
Auxocytes, 43 Branchial arches, 175, 247
Axial filament, 28, 44 Branchial artery, 303
Axial gradient, 151 Branchial groove, 288
Axial mesoderm, 105 Branchiomeric muscles, 271
Axial musculature. 255 innervation, 256
Axial skeleton, 243 Branchiostoma, see Amphioxus
Axon, 264 Bremer, 134
Azygous vein, 240, 241 Bridges, 71, 77
Bronchi, 192
Balfour, 80 Brpnchioles, 191, 193
Basal plate, 266, 267 Bulbourethral ((Z!owper's) gland. 220
Basalia, 248 Bulbus aortae, 328
Basilar artery, 228, 326, 333 Bulbus arteriosus, 228, 317, 318,' 319, 322
Basilar plate of skull, 246
Beak, 182, 261 Calcium-free sea water, 152
Behavior pattern. 10 .^Calcium metabolism. 176
Bellamy, 151 Calyces, 206,
Bidder's orga'n, 215 ' Camera lucida, 347
Bijtel, 122 Canada goose, 10 '
Bilaterality, 87, 151 Capillaries, 224
Bile canaliculi, 179 Carbohydrate metabolism, 179
Bile duct, 178 Cardiac plexus, 276, 277
Biogenetic law, see Recapitulation Cardinal system of veins, 230
^ theory Carothers, 61
Bipolar neurons, 264 ' • ' Carotid arteries, see External carotid
I Bisexual reproduction, 12 artery; Internal carotid artery
.Bladder muscles, 257 Carotid glands, 181
Blastemal mass (muscle), 256 Carpal bones. 249
Blastocoel, 82, 85. 90 Cartilage, 242
Blastocoel jelly, 85 Cartilage bones, 242
Blastocyst, 82, 83, 92, 105, 142 Caudal artery, 225, 229, 332
Blastodisc, 89 * Caudal bud, 117
Index 375
Caul, 145 Choroid plexus (of brain), 267, 269
Caval veins, 230, 231, 232; see aho Post- Chromatid, 63
caval vein; Precaval vein Chromatin, 25
Cavitation, 131 diminution, 40
Cecum, 187 Chromatin knot, 25
Cell, 24, 25 Chromatophores, 260
Cell division, 59 Chromidia, 26
Cell lineage, 4, 81 Chromomeres, 25
Cell theoiy, 4 Chromonema threads, 59
Cellular embryology, 4 Chromosomal aberrations, 76
Central canal, 265 Chromosomal crossing over, 71, 75
Central nervous system, 263 Chromosomal deletion, 75
chick, 279, 280 Chromosomal duplication, 75
frog, 277, 278 Chromosomal inheritance, 4, 6, 9
man; 268, 280 Chromosomal inversion, 75
Centrifuge, effects of, 165 Chromosomal non-disjunction, 76
Centriole, see Centrosome Chromosomal translocation, 75
Centromere, 60 Chromosome maps, 71, 72
Centrosome, 26, 52, 61 Chromosomes, 25, 59
Centrum, 244 amphioxus, 70
Cephalic flexure, 125 chick, 70
Cerebellum, 267 frog, 70
Cerebral hemispheres, 267, 269 man, 70, 71
Cerebral peduncle, 268 salivary gland, 71
Cerebrospinal canal, 263 Ciha, 110
Cerebrospinal ganglia, 264 Ciliary ganglion, 276, 277
Cerebrum, 269 Circular cleavage, 90
Cervical gangha, 277 Clavicle, 248
Chain gangha, 277 Claw, 260
Chalazae, 3 7 . Claw plate, 261
Chambers of eye, 287 Claw sole, 261
Changes in circulation at birth, 241 Cleavage, 79, 91
Chemical composition of environment, amphioxus, 13, 14, 84
166 chick, 20, 89
Chemical embryology, 6, 9 frog, 16, 17, 85, 86
Chemotaxis, 50 man, 91
Chen, 255 Cleavage path, 52
Chick, developmental stages, 122, 311- Cleidoic egg, 133
323 CKtoris, 212
life history, 18,''i9 Cloaca, 180, 202, 205
Child, 9 chick, 185, 217, 320
Choanae, 284 frog, 182, 214, 296, 297, 301, 306
Chondrification, 242 man, 187, 219
Chondriosomes, see Mitochondria pig, 325
Chondroblasts, 242 , Cloacal aperture, 111
Chondrocranium, 245, 248 Cloacal membrane, 220
Chorda dorsalis, see Notochprd Cloacal plate, 185
Chorda-mesoderm, 57, 98, 100, 111, 163 Cloacal tubercle, -218
Chorda-mesodermal field, If^l Closing plate, 172, 181
Chorda-neural crescent, 109 • Cochlea, 288
Chorda-neural plate, 85, 94 | Cochlear nerve, 274, 289
Chorio-allantoic placenta, 140 Coeliac artery, 230
Chorio-allantois, 133, 159 Coeliac plexus, 276, 277
Chorion, 128, 129 I ' Coeloblastula, 82, 83," 85
chick, 129, 318, 319,, 322 j Coelom, 194
man, 131, 22, 23 |" chick,^ 316, 319, 323
Myxine egg, 33, 34 i divisions, 197
Chorion frondosum, 142 frog, 304
Chorion laeve, 142 pig, 329
Chorionic placenta, 138 Coghill, 271
Choroid fissure, 286, 320 Collateral ganglia, 277
Choroid layer (of eye), 287 Collecting duct, 204
376 Index
Collecting tubules, 204, 217 Dareste, 165
Colliculi, see Corpora quadrigemina Darwin, 5, 8
Colon, 180 de Beer, 7, 151
Columella, 247, 289 Decidua basalis, 142, 145
Common bile duct, 178, 185 Decidiia capsularis, 145
Common cardinal vein, 226, 227, 231, Decidua vera, 145
319, 328 Decidual reaction, 138, 142
Communicating rami, 271, 277 Deciduate placenta, 141
Comparative embryolog}', 3, S Defect experiments, 159
Competence, 164 Deferent duct, 210, 215, 217
Concrescence, 94, 102 Delamination, 100, 101, 102, 105
Conjugation of pronuclei, 51 Deletion, 75
Conjunctiva, 287 Demibranch, 189, 192; see also Internal
Conklin, 9, 55, 56, 152 gills
Continuity of germplasm, 40 Dendrite, 264
Contractile filament (of sperm), 28 Dental papilla, 172
Coprodeum, 185 Dental ridge, 172
Copulation path, 52 Dentalium, 152
Coracoid, 245, 248 Dentary bone, 250, 251
Corium, 258 Dentine, 173
Cornea, 287 Dependent differentiation, 159
Corneum, 25S Derm bone, see Membrane bones
Cornua, 246 Dermal musculature, 254
Corona radiata, 38, 51, 210 Dermal skeleton, 243
Coronary sinus, 241 Dermatome. 195, 323
Corpora bigemina, 267, 268 Dermis. 258, 260
Corpora quadrigemina, 267, 268 Dermocranium, 245, 248
Corpus albicans, 137 Descending aorta, see Dorsal aorta
Corpus luteum, 137, 210 Determinate cleavage, 152
Corpus striatum, 269 Detwiler, 9
Corpuscles, 223 Deutencephalpn, see Epichordal brain
Cortex, brain, 269 Deutoplasm,'27; see also Yolk
egg, 150 Developmental stages, frog, 118, 119,
kidney, 205 120
Cortical cells, see Interrenal gland Diacoel, 269
Cortin, 213 Diaphragm, 197, 199, 200, 255
Cranial, see also Cerebral hemispheres; Dictyosomes. see Golgi bodies
Cerebral peduncle Didelphys, 138
Cranial flexure, 266 Diencephalon, 266, 269 ^
Cranial ganglia, 273', 322 ' chick, 318. 319, 320, 321
Cranial muscles, 255 frog, 302, 303, 308. 310 .
Cranial nerves, 272, 273 pig, 324, 325, 327
Cranium, 245 Diestrum, 136, 137
Crop, 183 Dietary defipienoies, 11
Crossing over, 71, 75 Differentiation, 153 i
Crypts, 141 fate, 161
Cultivation in vitro, 158 potency,'161
Cumulus oophorus, 209 Diffuse placenta, 140, 141
Cutaneous artery, 235 Digamety, X - 0 type, 68 '
Cutis, see Dermis X - X type. 70
Cuvierian duct, 226; see afeo Common X-Y type, 70
cardinal vein Digesti\-e tube, 116
Cynthia, see Styela chick, 184
Cytokinesis, 59, 61 -' frog, 182, 183
Cytology, 4 man, 186
Cytoplasm, 24 pig, 178
Cytosome, 26 tadpole, 183
Cytotrophoblast, 106 Diploid number (of chromosomes), 66,
Cytotrophoderm, 131, 142 67
Dipnoi, 190, 284
Daloq, 9 Direct ossification, 242
and Gerard, 100 Discoblastula, 82, 83, 90 "
Index 377
Discoglossus, 27, 87, 96 Egg tooth, 182, 261
Discoidal placenta, 141 Ejaculation, 49
Distal centrosome, 28, 44 Embedding, paraffin, 339
Donor, 157 Emboitement, 3
Dorsal aorta, 226, 228 Embryological drawings, 334
chick, 316, 318, 319, 320, 321, 322 Embryological technique, 334
frog, 304, 307 Embryologists, 1, 8
man., 238 Embryonic disc, 106, 131
pig, 325, 328, 329, 333 Embryonic form, 115
Dorsal lip of blastopore, 94, 97 Embryonic knob, 92, 126
Dorsal mesentery, 195, 198, 323 Embryonic mass, 105
Dorsal mesocardium, 195, 199, 226, 316, Embryotroph, 142
319 Enamel, 173
Dorsal mesohepar, 197 Enamel organ, 172
Dorsal ramus, 271 Encapsulated end organs, 284
Dorsal root ganglion, 271 End piece, 28
Dorsal root of spinal nerve, 271 Endocardium, 198, 313, 316
Double embryos, 155 Endocrine glands, 168
Triton, 156 Endoderm, 79, 93, 98, 99, 100, 105, 106,
Dreisch, 9, 152 111
Drosophila, 71 Endodermal derivativês, 171
Ductus arteriosus (ductus Botalii), 230 chick, 184
Ductus choledoohus, 178 frog, 182, 183
Ductus Cuvieri, see Common cardinal man, 186
^ vein pig, 178
Ductus deferens, 211, 221 Endodermal lacuna, 100
Ductus venosus, 325, 329, 333 Endodermalization, 56, 150
Duodenum, 186, 323, 325 Endolymph, 288
Duplicate monsters, 157 Endolymphatic duct, 288, 303
Duplication (of chromosomes), 75 Endotheliochorial placenta, 139
Dura mater, 265 Endothelium, 223
Dushane, 74 Enterocoel, 95, 194
Dyads, 63, 66 ' Entoderm, see Endoderm
Entypy, 128
Ear, 288 Enucleate egg fractions {Arhacia), 148
• chick, 292 Environmental factors in development,
frog, 291, 292, 306, 308, 310 164
man, 293, 294 Environmental influences on breeding,
pig, 324 . : 10
Ear drum, 181' Eparterial bronchus, 192, 328
Ect6derm, 79, 93, 100, 103 Ependyma, 264
Ectodermalization, 56, 150 Ephrussi, 5, 9
Edwards, 165 and Beadle, 73
Effectors, 263 Epiblast, 101
Efferent branchial artery, 229' Epiboly, 97
Efferent ducts of testis, 208 Epibranchial placodes, 274, 289
Efferent root of spinal nerve,, 271 Epicardium, 227
Egg, 32 ; Epichordal brain, 266
Egg albumen, 37 , Epidermal ectoderm. 111, 113
amphioxsus, 35, 36 Epidermis, 258, 313, 316, 319, 322
and environment, 34 i Epididymis, 210, 217, 219
cat, 32 Epigastric artery, 229
chick, 36 Epigenesis, 2, 3
frog, 35, 36 Epimyocardium, 226, 316
man, 37 •, | Epinephrin, 213
mouse, 32 Epiphysis, 269, 296, 302, 307
ostrich, 32
( Epithalamus, 269
Egg capsules, 34 Epithelial bodies, 176
Egg envelopes, 33 Epitheliochorial placenta, 139
Egg jelly, 34 Eponychium, 262
Egg nucleus, 32 Epoophoron, 210, 217, 219
Egg shell, 37 Erythrocytes, 223
378 Index
Esophagus, chick, 183, 322 Fixation, 334
frog, 181, 309 frog, 335
man, 186, 192 chick, 336
Estrin, 137 pig, 336
Estrous cycle, 135 Fixing fluids, Bouin's, 335
Estrus, 135 F.A.A., 336
Ethmoid bones, 251 Smith's, 335
Ethmoid plate, 246 Flexure, 123
Eustachian tube, 185, 289 Fioor plate (of brain), 266, 267, 269
Evagination, 13 FoUiole (ovarian), 215
Evans, 11 Follicle-stimulating hormone, 168
Evocation, 162 Follicular fluid, 209
Evolution, 5 Foods affecting development, 167
Excretory organs, 201 Foramen cecum, 185
Exocoel, 126, 194, 313, 316, 320 Foramen ovale, 228
Exoembryo, 167 Fore-gut, 117, 171
Exogastruk, 167, 168 chick, 183, 311, 312, 314, 315, 316, 319
Exosmosis, 94 frog, 181, 296, 297, 298, 300, 301
Experimental embryology, 5, 146 man, 114, 185
Explantation, 158 Formative cells, 105
External auditory meatus, 289 Fourth ventricle, 267
External carotid artery, 228, 229 322 Fraternal twins, 157 ,,
External genitalia, 212, 218 Free nerve ternjinations, 283
External gills, 122, 188, 189, 191, 303, 305 motor, 294
External glomerulus, 203 sensory, 284
External nares, 284, 292, 310 Freemavtin, 157 ' • •
Extraembryonic membranes, 115 Frog, developmental stages, 117, 296,
Extrauterine development, 23 310
Eve, 285, 286 life history, 15
chick, 292 Frontal bone, 250, 251
frog, 290, 291 Frontal sinus, 285
man, 293 Froriep's ganglion, 275
pig, 324 F.S.H. (follicle stimulating hormone),
Eyeball, envelopes of, 287 137
Fundulus (cell lineage), 82
• Facial muscles, 255
Facial nerve (VII),' 274 Gall bladder, 178
Falciform ligament, 200 chick, 178 -
False- amnion, see Chorion frog, 309
Fat body, 215 rnan, 186
Feathers, 259 pig, 330
Female digamety, 70 Gametes, 66 ^^^
Female pronucleus, 52 ' Gametogenesis, 39, 43 ^-' '
Female sex hormone, 210 CJanglia, 263; see also Cerebrospinal
Femur, 249
Fenestra ovale, 289 •Ganglion layer of eye, 286
Fenestra rotunda, 289 Gartner's- canal, 210, 219
Fertilization, 50 Gasserian ganglion, see Semilunar gan-
amphioxus, 13, 52 glion '
chick, 18, 53 Gastroooel, 93, 100, 116
effects on egg, 54 Gastrohepatic omentum, 200
frog, 17, 53 Gastrula, 93
man, 21, 53 amphioxus, 13, 14, 93
Fertilization cone, 51 _ > chick, 20, 100
Fertilization membrane, 51, 52, 53 frog, 16, 17, 96
Fertilizin, 51 man, 21, 105
Fetus, 23, 124 Gatenby and Aykroyd, 31
Fibula, 249 and Beams, 44
Field, 56, 150 Gene, 71, 76
Field district, 56, 150 effect on cytoplasm, 74
First aortic arch, 225 effect on differentiation, 74
First meiotic di\'ision. 63 mutation, 71 !
Index 379
Gene, theory of, 5, 9 Haldane, 70
General plan of development, 11 Half spindle fibers, 61
Genetics, 4 Haploid larvae, 147
Genie balance, 77 Haploid number of chromosomes, 66
Genie control of development, 73 Hard palate, 175
eye color, 74 Harrison, 282
feather pattern, 74 Hartman, 29, 38
Geniculate ganglion, 274 Hartsoeker, 2
Genital artery, 230 Harvey, Ethel, N., 140
Genital ducts, 210, 211 Harvey, William, 2, 8
Genital ridge, 208, 215 Hassall's corpuscle, 177
Genital tubercle, 212 Hatching, of amphioxus, 15
Genotype, 67 chick, 21
Germ, 1 frog, 18
Germ cells, 40 Head, 117
Germ layer concept, 3 Head fold, 114, 122, 125, 311
Germ layers, amphioxus, 16 of amnion, 129, 314, 315
chick, 20 jlfiadZraesenchyme, 264
frog; 17 Head of sperm, 28
man, 20 Head.process,. 105
Germ ring, 87 Heart, 224, 226, 227
Germ wall, 91, 113 chick, 236, 314, 315, 318
Germinal disc, 36, 53 coiling of, 227
Germinativum (of skin), 260 frog, 233, 234, 297, 301, 302, 303, 306,
Gill filaments, 190 307, 308
Gill plate, 411 man, 238, 239
Girdles (of skeleton), 248, 249 pig, 324, 328, 329
Gizzard, 184 Heart muscle, 257
Glands of skin, 260 Heat, 165
innervation of, 271 Hemiazygous vein, 240, 241
Glans penis, 212 Hemipenis, 212
Glomerulus, 202, 216 Hemiplacenta, 133
Glomus, 304, 309 Hemoblast, 223
Glossopharyngeal nerve ( I X ) , 274, 326 Hemochorial placenta, 139
Glottis, 191,193 Hemoendothelial placenta, 139, 142
Glycogen, 136, 170 Hemoglobin, 223
Golgi bodies, 26, 44, 62 Hemolymph glands, 233
Golgi-idiosome complex, 44 Henking, 58
Gonads, 168, 2()7,:208, 215, 217, 219 Hensen's node {or knot), see Primitive
Gonia, 42 '' node
Gotaoducts, 215, 217, 219 Hepatic cells, 179
Gonomery, 150 Hepatic ducts, 179
Graafian follicle, 137, 209 Hepatic portal vein, 178, 230, 231
Gradient, see Axial gradient Hepatic veins, 179, 231, 232
Graft, 157 Herbst, 152, 166
Granulocytes, 224 Hei'maphrodite, 215
Gravity, 165 Hermaphroditism, 12
Gray crescent, 57, 96, 98, 150, 151, 156 Hertwig, 80,-150, 165
Ground protoplasm, see Hyaloplasm Hertwig and Rock, 21, 106
Growth in length, 115 Heteroplastic transplantation, 157
Growth-promoting hormone, 168 Hind-gut, 117, 171, 180
Gudernatsch, 168 chick, 185
Gut, 330, 331 frog, 181, 296, 297, 300, 301
Gymniophiona, 189, 190 man, 187
Gynandromorph,. 77 His, 5, 9,349
Gynogenesis, .148 I
Histogenesis, of cardiac muscle, 254
striated muscle, 254
Haeckel, 5, 8 \'isceral muscle, 254
Haemal arch, 244 Histoiy, 8
Haiv, 259 Hoadley, 103
Hair papilla, 260 Holoblastic cleavage, 80
Hair sheath, 260 Holtfreter, 9, 166, 167
380 Index
Homologies of reproductive organs, Internal glomerulus, 203
221 Internal jugular vein, 231
Homoplastic transplantation, 157 Internal nares, 284
Hoofs, 260 Intcrplantation, 159 *
Hormones, 11, 167 Interrenal gland, 212
Horny jaws, 122 Intersegmental artery, 230
Host, 157 Intersexes, 76, 77
Humerus, 249 Interspecific hybrids, 150
Huxley, 151 Interstitial cells, 49, 209
Hyaloplasm, 26 Interventricular septum, 228
Hyaluronidase, 51 Intervertebral disc, 244
Hybrid vigor, 150 Interzonal fibers, 61
Hymen, 219 Intestine, 181, 304, 306, 307, 309, 310
Hyoid arch, 122, 247 Invagination, 94
Hyomandibular arch, 247 Investing bones, 243, 245
Hyomandibular artery, 234 Involution, 94, 97, 100, 101
Hyomandibular cartilage, 251 Iris, 287
Hypoblast, 90, 100 muscles, 253, 287
Hypochord, 111, 299, 304 Ischium, 248
Hypogastric plexus, 277 Islets of Langerhans, 179
Hypoglossal nerve ( X I I ) , 275 Isolation experiments, 159
Hypophysis, 172 Isolecithal egg, 33
chick, 183, 319 Isthmus of brain, 281, 320
frog, 181,297, 302, 303, 307 Isthmus of Pander, 36
man, 185 Iter (aqueduct), 269
pig, 325, 327
Hypothalamus, 269 Jacobson's organ, see Vomeronasal or-
gan
Identical twins, 157 Jaw, 172, 247, 261
Idiosome, 44 Jenkinson, 166
ileum, 180 Jensen, 2, 8
Iliac artery, 230, 237 Johannsen, 5, 9, 59
' Ilium, 248 Jugal bone, 250, 251
Implantation, 21, 135, 137, 138 Jugular ganglion, 274, 326
Incus, 251, 289 Jugular vein, see Internal jugular vein
Indeciduate placenta, 140
Indeterminate cleavage, 152 Kaestner, 165
Induction, 162 Karyokinesis, 59, 60
'Infundibulum, 172, 269 Karyolymph, 25, 59, 61
chick, 183, 320 Kajyoplasm, 24 ""
frog, 297, 302, 307 Karyosome, see Chromatin knot
man, 185 Kathariner, 150 ^f
pig, 327 Kidney, 204; see also Mesonephros,
Inheritance of acquired characters, 40 Metanephros, Pronephros
Inner ear, 288
Innervation of muscles, eyeball, 273,' 274 - Jâbia majora, 212 ^ -
pharynx, 274 Labia minora, 212
tongue, 275 ' Labial groove, 174
visceral arches, 274 Labioscrotal folds, 212 '
Inorganic elements, 167 Lactogenic hormone, 168
Innominate vein, 241 Lagena, 288
Insulin, 179, 187 Lamina terminalis, 278
Integument, 258 Lanugo, 262
chick, 261 Large intestine, 184, 187
frog, 261 Larva, amphioxus, 14, 15
I man, 261 frog, 16,18
.Intercostal muscles, 255 Larval teeth, 181
Intermediate mesoderm, 114, 203, 313, Laryngeal cartilages, 193
316 Laryngeal muscles, 255
Internal carotid artery, 228, 229, 326, Laryngotracheal groove, 191, 192
333 Larynx, 193
Interna! gills, 122, 188, 189, 191, 308 Latebra, 36
Index 381
Lateral folds of amnion, 129 Main piece (of sperm), 28
Latei-al line system, 263, 289, 292 Male pronucleus, 52
Lateral lips of blastopore, 94, 97 Male sex hormone, 209
Lateral mesocardia, 199 Malleus, 289
Lateral mesoderm, 95, 105 Malpighi, 2, 8
Lateral ramus (of nerve), 271 Mammary glands, 137, 260, 262
Lateral rectus muscle, 255 MammiJkry bodies, 269
Lateral sulci, 114, 316, 320 Mandibular arch, 122, 247
Lateral ventricles (of brain), 269 Mandibular process, 172
Laws of cleavage, 79 Mangold, 9, 155
Leeuwenhock, 2 Mantle layer (of spinal cord), 264, 265
Leg bud, 323 Margin of overgrowth, 90
Lens (of eye), 286, 308, 320, 327 Marginal belt (germ ring), 87, 159
Lens field, 238 Marginal layer of spinal cord, 264, 265
Lens pit, 286 Marginal zone, 98
Lens placode, 285 Marine eggs, 34
Lens vesicle, 286, 317, 319, 322 Marsupial yolk sac, 125
Lethal mutants, 73 Matrix, 27
Leucocytes, 224 . chromosome, 59
Lieberkind, 111 Maturation divisions, 43, 45, 63; see
Life history, see aho Ontogeny also Meiosis
amphioxus, 13, 14 Mature ovum, 46
chick, 18, 19 Maxilla, 250, 251
frog, 15, 16 Maxillary process, 172
'man, 21, 22 McClung, 59
Ligaments, 243 Meatus venosus, 237, 323
Ligation experiments, 149, 154, 155 Meckelian cartilage, 247
Light, 10, 166 Mediastinum, 193, 197
LiUie, 157 Medulla oblongata, see Myelencephalon
Limb buds, 124, 125 Medulla of kidney, 205
Limb grafts, 282 Medullary^ see also headings beginning
Limiting sulci, 130 Neural
Lingual primordia, 173 Medullary cells, 221; see also Suprarenal
Linguo-labial groove, 175 gland ''
Linkage groups, 71 Medullar}' sheath, 264
Liver, 177 Megaloblasts, 223
• chick, 179, 184, 319, 323 Meiosis, 63, 64, 65; see also Maturation
frog, 181, 296, .297, 299, 301, 302, 304, divisions
307, 309 Melanin, 260, 286
man, 186 ' Membrane bones, 242, 243
i5ig, 324, 325,329, 333 Membranous labyrinth, 288
Loeb, 6, 9, 54, 147 Mendel, 4, 8, 58
Loop (intestinal), 187 Meninges, 265
Lumbo-sacral ganglia, 277 Menstrual cycle, 135, 136, 137
Lung buds, 191 ; ' Meroblastic cleavage, 80, 165
Lungs, 188, 190 Merogony, 148
chick, 192 j Mesectoderm, 93,100,'106
frog, 192, 309 Mesencephalon, 266, 267
man, 192 I chick, 314, 315, 317, 318, 320, 321, 322
pig, 325, 329 frog, 296, 297, 301, 302, 303, 307
turtle, 191 I man, 268
Luteinizing hormone (iL.H.), 137,168 pig, 324, 325, 326
Lygaeus, 69 Mesenchyme, 93, 195, 312, 313, 316
Lymph glands, 233 Mesendoderm, 93
Lymph hearts, 232 Mesenteric artery, 230
Lymph sacs,. 232 , Mesenteric vein, -239
Lymphatic system, 232, 233 Mesenteries, 194, 195, 196
Lymphocytes, 224, 232 Mesentoderm, see Mesendoderm
Mesoblast, see Mesoderm
Macacus, 29, 38 Mesocardia, 198
MacroJecithal eggs, 33 Mesocoel, 269
Macromeres, 84, 86 Mesoderm, 79, 93, 103, 104,114, 198
B82 Index
Mesodermal crescent, 84 Monovular twins, 156
Mesodermal lacuna, 100 Monsters, 156
Mesodermal pouches, 95 Moore, 165
Mesoduodenum, 195 Morgan, 5, 150, 151
Mesogastrium, 195 Morula, 91, 142
Mesonephrio duct, 320, 323, 330, 331, Mosaic eggs, 152, 153, 161 .
332; see also WollBan duct Mossman, 139, 140, 142
Mesoaephric tubules, 203, 214, 320, 323 Motor end plate, 294
Mesonephros, 203 Motor nerve terminations, 294
chick, 217, 320 Motor neurons, 265
irog, 214, 215 Mouth, 111, 172, 181, 182, 185, 306
man, 218 Mucosa (of intestine), 177
pigs, 324, 325, 329, 332, 333 Mule, 150
Mesorchium, 208 Muller, 71, 166
Mesovavium, 208 Mullerian duct, 210, 215, 217, 219; see
Metabolic gradient, 3 3 ; see also Axial also Oviduct
gradient Multicellular glands, 260
Metabolic nucleus, 25 Muscles, 253
Metacarpals, 249 eyeball, 255, 287
Metacoel, 267 mastication, 255
Metamerism, 116, 265 Muscularis (layer of intestine), 177
head, 275 Myelencephalon, 267
Metamorphosis, 168, 169, 176 chick, 318, 319, 320, 321, 322
ambystoma, 169 frog, 302, 303, 308, 309
amphioxus, 14, 15 pig, 324, 325, 326
frog, 192 Myelin, 264, 265
Metanephric duct, 204, 219, 332 Myelocoel, 267
Metanephros, 204, 205 Myenteric plexus (of Auerbach), 277
chick, 216, 217 Myoblasts, 254
man, 218, 219 Myocardium, 198, 227
pig, 325 Myocoel, 194
Metaphase, 60 Myofibrillae, 254
Metaplasm. 27 Myosepta, 245
Metatarsals, 249 Myotome, 194, 255, 265
Metencephalon, 267 chick, 323
chick, 318, 320, 321 frog, 301
frog, 302 pig, 328
man, 268 Myxine, 34
pig, 324, 325
Metestrum, 135, 136, 137 Nails, 260
Microdissection, 157 • Nares, see Anterior nares; Posterior
Microlecithal (oligolecithal) egg, 33 nares /\
Micromeres, 84, 86, 90 Nasal, see also headings beginning Ol-
Micrometry, 346 factory •'
Micron {^), 346 Nasal bone, 247, 250, 251
Micropyle, 34 -.Nasal passage, 175 "" •
Microscope, 2 Nasal pits, 284, 305, 306, 310, 320, 322
Mid-brain,, see Mesencephalon Nasal placodes, 284, 290, 292, 293
Middle ear, 181, 288, 289 Nasolacrymal duct, 285 '
Middle piece (of sperm), 28 Neck bodies, 28
Mid-gut, 11, 117, 180 iVectums, • 188, 256
chick, 184, 313, 316, 319 Necdham, 6, 9, 133 /
frog, 181, 296, 297, 299, 302, 305 Neighborwise development, 159
m^n, 187 NeonyclVium, 261
Milkj ridges, 262 Nephric tubule, 202
' Milt, 29, 49 Nephrocoels, 194, 202
Mitochondria, 26, 45, 61, 62 Nephrogenic cord, 203, 213
Mitosis, 59, 60, 64 Nephrogenous tissue, 204, 219
Modeling wax, 350 Nephron, 203
Moenkhaus, 150 Nephrostomes, 202, 213, 214, 216, 304
Monoploid number (of chromosomes), Nephrotonies, 194
see Haploid number Nerve terminations, 283 '
Index 383
Nerve trunk, 27,1 Olfactory nerve ( I ) , 272, 285
Nerves, growth in vitro, 282 Olfactory pit, 118, 328
Nervous ectoderm, 111, 113 Olfactory placodes, 284
Nervous system, 263 Oligolecithal, see Microleoithal egg
Neural arch, 244 Ollacher, 100
Omentum, 196
Neural crest, 109, 195, 213, 263, 264, 274,
276, 316 Omphalomesenteric, see headings begin-
Neural folds, 108, H I , 113, 114, 122, 125, ning Vitelline
311 Ontogeny, 1
Neural groove, 108, 311, 313 Oocyte, 43, 45, 46
Neural plate, 100, 103, 109, 110, 111, Oogenesis, 45
Oogonium, 42, 209
263
Opercular aperture, 122; see also Spir-
Neural tube, 109, 110, 263, 296, 297, 299,
312, 314, 317, 333 acle
Neurenteric canal, 107, 109, 182 Opercular chamber, 189, 191, 192, 308,
Neuroblast, 264 .309
Neurocoel, 265 Opercular fold, 189, 191
Neurocranium, 245, 246 Operculum, 122
Neuroembryology, 282 Opossum, 128, 138
Neuromeres, 279 Oppenheimer, 82
Neurons, 264, 265 Optic capsule, 246
Neuropore, 109 Optic chiasma, 269, 273, 302, 307, 325
Neurula, 16, 17,108 chick, 317, 319, 320, 322
Neurulation, 108 frog, 301, 303
âmpliioxus, 109 man, 293
chick. 111 pig, 327
frog, 110, 112 Optic cup, 286
man, 114 Optic field, 161, 288
Nodose ganglion, 275, 327 Optic lobes, 267
Non-disjunction (of chromosomes), 76 Optic nerve ( I I ) , 272, 286
Normoblasts, 223 Optic recess, 302, 307
Nose, 284 Optic stalk, 285, 300
chick, 292 Optic vesicle, 118, 285, 296, 298, 314,
frog, 290
man, 285, 293 315
Notochord, 98, 243 Oral cavity, 172
amphioxus, 95 Oral comb, 261
Oral gland, 296, 301 .
chick, 103, 105, 111, 114, 311# Oral plate, 172
frog, 98, H I , 296f Oral sucker. 111, 118, 180, 260, 296, 298,
man, 107 302, 303
•pig, 325f Organ-forming areas, 6, 55
Nuclear membrane, 24, 25, 59 Amphibia, 57, 96, 97
Nuclear sap, see Karyolymph amphioxus, 56
Nuclei of brain, 267 i Ascidiella, 55
Nucleolus, 24, 25, 53 i chick, 57
Nucleus, 25, 148, 153 Styela, 55
of brain, 267 i Organ of Corti, 288
Nucleus pulposus, 244 Organelle37-26
Nurse cells, see FoUicle Organization, during cleavage, 153
germ layer formation, 157
Oblique vein, 240 of cytoplasm, 150
Occipital bones, 251 Organizer, 6
Occipital vertebrae, 245 Organogeny, 115, 116
Oculomotor nerve ( I I I ) , 273, 326 Ossification, 242
Odontoblasts, 173 (' Osteoblasts, 242
Oesophagus-, see Esophagus Osteoclasts, 25 •
Okkelburg, 51 Osteocytes, 242
Olfactory, see also Headings beginning Ostium tubae abdominalc, 210
Nasal Otic, see also headings beginning Acous-
Olfactory capsule, 246 tic, Auditory
Olfactory epithelium, 285 Otic bones, 246, 251, 289
Olfactorv lobes, 285 Otic capsule, 246
384 Index
Otic field, 288 Penetration path, 52
Otic ganglion, 276 Penile urethra, 212, 219
Otic pit, 118, 288, 296, 298, 319 Penis, 212, 218
Otic placode, 288, 291, 292, 294, 316 Peramcles, 138 • .
Otic vesicle, 288, 291, 292, 294 Perforatorium, see Acroaome
Otocyst, see Otic vesicle Periblast, 90
Otolith, 288 Pericardial cavity, 227
Outer ear, 288, 289 chick, 198, 315, 322
Outer peritoneal lining, 195 frog, 198, 303
Ovarian follicle, 209 pig, 329
Ovarian hormones, 137 man, 199, 200
Ovary, 47, 209, 217 Pericardial membrane, 199, 200 •
Oviduct, 215, 217; see also Miillerian Pericardioperitoneal canal, 197
duct Perichondrium, 243
Oviparous, 48 Periderm, 258
Oviposition, 48 Perilymph, 289
Ovoviviparous, 48 Periosteum, 243 ,
Ovulation, 47, 135, 137, 142 Peripheral nervous system, 279, 280,
causes of, 47 281
in man, 54 Peritoneal cavity, 197
copulation, 48 Peritoneal lining of coelom, 195
enzyme action, 48 Perivitelline fluid, 51 ,
hormone action, 48 Perivitelline space, 52, 53
muscular contraction, 47 Petrosal ganglion, 274
rupture of stigma, 48 Pfluger, 151
turgor, 48 Phaeochrome tissue, 213
Oxygen, 166 Phalanges, 249
Phallus, 212
Pacific salmon, 10 Pharyngeal pouches, see Visceral
Pacinian corpuscle, 284 pouches
Painter, 71 Pharyngeal cartilages, 203, 210
Paired limbs, 122 Pharyngeal muscles, 210
Palate, 175 Pharynx, 117,175, 190
Palatine bones, 175 chick, 318, 322
Palatine process, 175 frog, 302, 303, 305, 308
Palatine tonsil, 185 man, 186
Pancreas, 179, 181, 184, 186, 325 pig, 324, 325
Parabionts, 169 Photomicrography, 348
Parachordal cartilages, 246 Phrenic nerve, 200, 255 _~
Paradidymis, 210, 217, 219 Phylogeny, 5 .
Paraphysis, 269 > Physical vigor, 11 ' ^
Parasphenoid bone, 246, 251 Pia mater, 265 ,'.
Parathormone, 176 Pigment, 27, 260, 264
Parathyroid, 176, 181, 183, 186 of retina, 286
Parietal bones, 250, 251 Pincus, 147 _^ '
Parietal recess, 200 -Pineal gland, 269 ^
Parmenter, 147 Pinna, 288, 289
Paroophoron, 210, 217, 219 Pituitary, 137, 168, 172; see also H y -
Parotid glands, 174 pophysis
Pars nervosa (of hypophysis), 172 Pituitary hormones, 137, 168
Parthenogenesis, 54 Placenta, 135, 138, 139, 188 ;
aphid, 54 carnivores, 139
honey bee, 54; see also Artificial par- man, 23', 134, 142, 143, 145
thenogenesis marsupials, 138
Partitioning of heart, 228 ' pig, 140, 141
I Parturition, 145 Placental hormones, 137
Pasteels, 9, 96, 100 Placodes, 283
Patterson, 100 Placoid scale, 243
Pectoral girdle, 245 Plasma membrane, 26
Pelvis of kidney, 206 Plasmasome, see Nucleolus
Penetration (by sperm), 51 Plasmatrophoblast, 106 ,
Penetration cone, 51 Plasmatrophoderm, 131, 142 ,
Index 385
Plasticity, 159 Primitive streak, 93, 100, 102, 103, 105,
Plastid, 24, 25 106, 111, 311, 312, 314, 315
Pleural cavity, 192, 193, 197, 200 Primordial germ cells, 41, 42, 208
Pleural groove, 322 Primordium, 14
Pleuropericardial septum, 200 Proacrosomic granules, 44
Plough, 71 Proamnion, 114, 129, 311, 313
Point mutations, 166 Proctodeum, 111, 116, 118, 124, 180, 185
Polar axis, 33 Proestrum, 136,- 137
Polar body, 45 Progestin, 137
Polar cells, 105 Projection apparatus, 248
Polar furrow, 86 Proliferation, 136, 137
Polarity, 33, 150 Pronephric duct, 202, 213
Pole, see Polarity Pronephric shelf, 213
Polyinvagination, 100, 101 Pronephric tubules, chick, 216
Pons (of brain), 267 frog, 213
Pontine flexure, 268, 280, 281 man, 218
Portal vein, 231, 330 Pronephros, 202
Postanal gut, 180, 181 chick, 216
Postcaval vein, 232, 325, 329, 330, 331 frog, 213, 214, 301, 304, 305, 300
Postcloacal gut, see Postanal gut man, 218
Posterior cardinal vein, 226, 231 Pronucleus, 52, 53, 149, 150
chick, 235, 237, 238, 319, 320, 323 Prophase, 59
frog 237 Prosencephalon, 266
man, 239, 240 241 chick, 314, 315. 316, 317
^ i g , 329, 331 • frog, 296, 297, 298, 300, 301
Posterior .. caval vein, see Postcaval Prospective potencies, 152
vein Prospective significance, 152
Posterior chamber of eye, 287 Prostate gland, 220
Posterior limb bud, 320, 332 Protenor, 68
Posterior nares, 292, 293 Protoplasm, 24
Posterior tubercle, 297, 302, 307 Protopterus, 260
Posterior velum, 267 Prototheria, 135
Postnuclear cap, 32, 44 Proventriculus, 184
Postotic ganglion, 279, 280 Proximal centrosome, 28
Precardinal vein, see Anterior cardinal Pseudobranch, 190
vein Pterygoid'bones, 246, 250, 251
Precaval vein, 231 Pterygoquadrate cartilage, 247
Prechordal brain, 266 Puberty, 23
Prechordal plate, 98, 103, 105, 107 Pubis, 248
Precoracoid'bone, 248 Pulmonary arch, 230
Preformation theory, 2 Pulmonary artery, 230, 235, 237, 241
PremaxiUa, 246, 247, 251 Pulmonary circulation, 193, 241
Preoral gut, 172, 325 Pulmonary trunk, 228
Preotic somites, 255, 287 Pulmonary vein, 231, 232, 241
Pressure experiments, 155, 156 Pulp (of feather), 260
Presumptive germ layers, 97 Pupil (of eye), 287
Presumptive organ regions, 83, 85, 88,
159 , Quadrate bene, 250, 251, 289
Prevertebral ganglia, 277 Quadi-atojugal, 250, 251
Primary bronchi, 191, 192, ,322
Primary egg envelope, |33 Radial cleavage, 90
Primary ganglia, 277 . Radialia, 248
Primary germ layers, 93 Radium, 166
Primary oocyte, 45 Radius, 249
Primary orgaaizer, 162, Radix aorta, 228
Primary spermatocyte', 43 Rami of spinal nerve, 271
Primary spindle fiber^, 61 Rana pipiens, 35
Primary vesicles of brain, 266 Rathke's pocket, 172
Primitive groove, 313 Rauber's layer, 132
Primitive knot, 311 Recapitulation theory, 5, 8
Primitive node (Henseri's), 105, 107 Receptors, 263
Primitive pit, 107 Recessive mutants, 73
386 Index
Recombination experiments, 158, 159, Segmental muscles, 305, 307
160, 162, 163 Segmentation cavity, 85, 87; see also
Reconstruction models, 349 Blastocoel
Rectal plate, 187 Segregation of mesoderm, 95, 111
Rectum, 180, 181, 187, 207, 219 Self-differentiation, 161, 162
Reflexes, origin of, 271, 282 Self-wise differentiation, 161
Regulation eggs, 152, 153 Semicircular canals, 288, 308
Renal artery, 205, 230 Semilunar (Gasserian) ganglion, 273, 326
Renal portal circulation, 232 Seminal fluid, 29, 49
Renal pyramids, 207 Seminal vesicle, 210, 215, 219
Reproductive habits, 10 Seminiferous tubules, 208, 215
Reproductive organs, 207 Sense organs, 124, 125, 263
chick, 216 Sense plate, 110
frog, 213 Sensory layer of retina, 286, 290, 303,
man, 218 308, 310, 319, 322, 327
Respiratory organs, 188 Sensory nerve terminations, 283
chick, 192 Sensory neurons, 264
frog, 191 Sensory placode, 264
man, 192 Separation of blastomeres, 152
Retention theory, 7 Septum aorticopulminale, 228
Retina, 273, 286, 319, 322, 327 Septum transversum, 197, 198, 199, 227,
Rhinencephalon, 285 329
Rhombencephalon. 266 Serial sections, 339 '
chick, 314, 315, 316, 317 Sero-amniotic raphe, see Amniotic
frog, 296, 297, 298, 301 raphe
Ribs, 245 Serosa of intestine, 177; see also C h o - ,
Rods and cones, 286 rion
Roots (of nerves), 266, 271 . Sertoli cell, 45, 49, 209
Roux, 5, 9, 152 Sex chromosomes, 68, 69, 70
Rugh, 48 Sex hormones, 169; see also Female sex
hormone; Male sex hormone
Saceuhis (of ear), 288 Sharp, 25
Sachs' rules, 80 Shell, 37
Sacral plexus, 265 Shell gland, 217
Salivary gland, 174, 185 Shell membrane, 37
chromosomes, 71, 73 Shumway, 165
innervation of, 274 Siamese twins, 157
Scales, 259 Sinus of nose, 285
Scapula, 248 Sinus rhomboidialis, 314
Schleiden and Schwann, 4, 8 Sinus terminalis, 226 "-
Schmidt, 152 Sinus venosus, 227, 317, 321, 322, 333
Schrader, 61 Situs inversus, 151 ./
Sclera (of eye), 287 Skeletal labyrinth (of ear), 289''- -
Sclerotome, 244, 323 Skeletal muscle, 271
Scrotum, 212 Skeleton, 242
Seasonal aspect of breeding, 10 chick, 250
Sebaceous glands, 260 " frog, 249 ,
Second meiotic division, 63 man, 250
Secondary envelopes of egg, 33 Skin, 258; see also Integument/
Secondar3' oocytes, 45 Skull, 245, 246, 247, 248
Secondary sex characters, 11 Small intestine, see Ileum
Secondary spermatocyte, 43 Smooth muscle, 254, 256 '
Secondary tubules (of mesonephros), innervation of, 271, 274
204 Soma cells, 40 - "^ •
Secretion, 136, 137 Somatic layer of mesoderm, 114, 194,
(Secretion granules, 27 313
Secretory tubules, 205, 217 Somatic mitosis, 59, 60, 61, 62, 64
Sectioning, 340 Somatic (affei-ent) neurons. 270
frontal sections, 34i Somatopleure, 195, 313, 316
sagittal sections, 341 Somites, 95
transverse sections, 341 chick, 114, 122
Seessel's pocket, see Preoral gut frog, 296, 297, 302
Index 387
Somites, man,. 114 Storage granules, 27
Spawning ampliioxus, 13 Stratum corneum of skin, 258
frog, 17 Stratum germinativum of follicle,
Spemann, 6, 9, 149, 133, 154, 155, 160, 258
162, 163 Stratum granulosum of skin, 209
Sperm, abnormal, 29 Stratum intermedium of skin, 258
activity of, 29 Streeter, 106
anphioxus, 30, 31 Striated muscle, 253, 254, 255
chick, 31 Stroma of testis, 209
fertilizing power, 29 Styela, 152
frog, 30, 31 ceil lineage, SI
longevity, 29 Subcardinal vein, 232, 329, 331
man, 31 Subcaudal pocket, 122. 133
numbers, 30 Subcephalic pocket, 113, 311, 315, 316
viability, 30 Subclavian artery, 230
Spermatic vein, 240 Subfields, 164
Spermatid, 43 Subintestinal vein, 226
Spermatid transformation, 44 Sublingual glands, 174
Spermatocytes, 43 Submaxillary glands, 174
Sperniatogenesis,' 43 Submaxillary ganglion, 276
Spermatogonia, 42, 208 Submucosa (of intestine), 177
Spermatozoon, see Sperm Submucous plexus (of Meissnor), 277
Spermioteleosis, see Spermatid trans- Subnotochordal rod, see Hypochord
formation Substituting bones, 243
Sphenoid bones, 246, 250, 251 Subunguis, 260
Sphenoidal sinus, 285 Sucker (of tadpole), 297, 298, 302, 303
Sphenolateral cartilage, 246 Sudoriparous glands, 260
Sphenopalatine ganglion, 276 Sulcus limitans, 266
Spina bifida, 165 Superior ganglion, 274, 326
Spinal accessory nerve ( X I ) , 275, 326 Superior oblique muscle, 255
Spinal cord, 263, 265, 266 Supernumerary sperm, 53
chick, 316, 319, 320 Supersexes, 76, 77
frog, 304, 310 Supracardinal vein, 240, 241
pig, 327-332 Suprarenal gland, 213, 264, 277
Spinal nerves, 265, 270, 271, 327 Sustentacular^cells, see Sertoli cells
Spindle (mitotic), 60 Sutton, 9,.58
Spiracle, 190 Sweat glands, see Sudoriparous glands
Splanchnic layer (of mesoderm), 114, Swim bladder, 190 '
194, 313 Sympathetic ganglia, 264
SplanchnocoeJ, 194; see also Coelom Sympathetic nerves, 275, 276
Splanchnocranium, 245, 247 Sympathetic nervous system, 263, 280,
Splanchnopleure, 195, 313, 316 281
Spleen, 197, 233 Sympathetic trunks, 277
Spongioblast, 264 Synapse, 271
Spratt, 102, 170 Synapsis, 63
Squalus, 243, 245 Syncytiotrophoderm, see Plasmatro-
Squamosal bone, 246, 247, 250, 251 phoderm
Staining serial sections, 343 Syncytium, 26
Stains, borax carmine, 337 SyndesmoclTorial placenta, 139
haemalum (Mayer's), 338 Syngamy, see Fertilization
Heidenhain's hatmatox3'lin, 334 Systemic arch, 229
picro indigo carmine, 345 Systemic trunk, 228
Stapedial muscles, 289
Stapedial plate, 289, 292, 293 Tail, 117, 122, 124, 125
Stapes, 247, 289 sperm, 28
Stem cell, 40, 41 • Tail bud, 110
Sternum, 245 Tail fin, 306
Stigma, 48 Tail fold, 114, 122, 317
Stomach, 186, 307, 309, 329, 333 of amnion, 130
Stomodeal plate, 318 Tangential cleavage. 90
Stomodeum, 111, 116, 118, 172, 180, 182, Tapetum, 286
185, 298, 302 Tarsal bones, 249
38S Index
Taste buds, 181, 274. 283 Ultraviolet hght, 166
innervation of, 274 Umbilical artery, 133, 134, 230, 325, 331
Teeth, 172, 173, 185 Umbilical cord, 140, 144
Telencephalon, 266, 269 Umbihcal stalk, 123, 129, 130
chick, 318, 320, 321 Umbilical veins, 133, 134, 230, 331
frog, 302 Unguis, 260
pig, 324. 325, 328 Unicellular glands, 260
Telobionts, 169 Urachus, 207
.Telolecithal egg, 33 Ureter, 204, 215, 217
Telophase, 60, 61, 63, 65 Urethra, 207, 219
Temperature, 10 Uric acid, 133
Temperature gradient, 165 Urinary bladder, 182, 205, 206, 207, 215,
Temperature tolerance, 165 217, 219
Tensor tympani (muscles), 289 Urodeum, 185, 207, 217
Teratology, 78 Urogenital duets, 210
Term, 124 Urogenital organs, 201
Terminal nerve (0), 272, 285 chick, 216
Terminal ganglia, 277 frog, 213
Terrestrial egg (cleidoic), 35 man, 218
Tertiary envelopes, 34 Urogenital orifice, 187
Tertiary tubules of mesonephros, 204 Urogenital plate, 187
Testis, 49, 208 Urogenital sinus, 180, 187, 207, 219, 220
Tetrad, 63 Urogenital vestibule, 212
Thalamus, 269 Urorectal septum, 219
Thigmotaxis, 51 Uterine milk, 125
Third ventricle, 269 Uterine tubes, 211, 219
Thymus, 176, 181, 183, 186, 333 Uterus, 211, 219
Thyreoglossal duct, 175 Utriculus, 288
Thyroid, 168, 175, 176, 181, 183, 185, 303, Utriculus, prostaticus, 211, 219
322
Thyroxin, 168 Vacuoles, 27
Tibia, 249 Vagina, 219
Tongue, 173, 181, 183, 185, 325, 327 Vagina rnasculina, see Utriculus pros-
Tongue muscles, 255 taticus
Tonsil, see Palatitie tonsil Vaginal smear, 136
Tooth ridge, 182 Vagus nerve (pneumogastric) ( X ) , 274,
Torsion, 123 326, 327
Trabecula (cartilage), 246 Valves of sinus vcnosus, 328
Trachea, 190, 192, 324, 328 Vandebrock, 56
Translocation, 75 Vasa effe(;entia, 215, 217
Transplantation, 157, 158 Vascula'r system, 222, 225
Trigeminal nerve (V), 273, 326, 327 chick, 236
Triploid larvae, 147 frog, 233
Triton, 146, 148, 149, 155, 156, 160, 163, man, 238 . . * . ,-;
167 Vegetal h e m i s p h e ^ and pole, 33
Trochlear nerve (IV), 273 Veins, 230
Trophoblast, 92, 105 chick, 237
Trophoderm, 'see Trophpblast frog, 235
Tuber ciriereum, 269 man, 238, 239, 240
Tube'rculum impar, 185 Velar plate, 192, 308
Tuberculum posteriiis, see Posterior Velum transversum, 280
tubercle Vena cava, see Postcaval vein; Precaval
Tubotyn panic caivity, 183 vein
Tubular glands, 260 Vent, 111, 297
Tunica albuginea (ovarv), 210 , Ventral aorta, 225, 227, 228
Tunica of testis, 209 Ventral lip of blastopore, 94, 97
Tympnnic'cavity, 185, 289 Ventral mesentery, 195^ 198
Tympanic membrane;- 289 Ventral mesocardium, 195, 199, 226
Ventral mesohepar, 197
Ulna. 249 Ventral ramus, 271
FltimoViranehial bodies, 176, 177, 181, Ventral root, 266
183 Ventricle of brain, 267
Index 389
Ventricle of heart, 228, 303, 308 317, Vogt, 6, 9, 76, 83, 87
319, 320, 321, 325, 328, 329 Vomeronasal organ, 285, 291
Vermiform appendix, 187 Von Baer, 2, 3, 8
Vertebrae, 244
Vertebral artery, 228 Waddington, 9
Vesico-urethral primordium, 207 Waldeyer, 58
Vestibular glands, 219 Water, 166
Vestibv:l-dr nerve, Zr-i, 2S& Wax p/ate model's, 349
Vestibule, 288 Weismann, 6, 9
Villus, 140, 141, 142 Weiss, 9, 282
Villus, intestinal, 177 Whitman, 4, 9
Visceral afferent neurons, 270 Whole mounts, 337
Visceral arches, 121, 122, 247 Wilher, 163
chick, 318, 322 Wilson, 152
frog, 305 Witschi, 42, 153, 169
man, 125 Wolff, 3, 8
pig, 327 Wolffian body, see Mesonephros
Visceral clefts, 121, 122, 175, 191 317 Wolffian duct. 204, 210, 215, 217, 219
320 Wright, 17, 35
Visceral grooves, 121, 122, 124 125
319 ' ' X-chromosome, 68, 69
Visceral muscles, 256 X-rays, 166
Visceral pouches, 121, 122, 288 Xenoplastic transplantation, 157, 158,
chick, 183, 319 159, 160, 162, 163
frog, 181, 305
. man, 185 Y-ehromosome, 70
• pig, 327, 333 Yamada, 164
Visceral skeleton, 243, 264; gee also Yellow crescent (of Styela), 54, 150
Splarichnocranium Yolk, 32, 36, 126, 301, 307
Vital dyes, 87 retraction of, 134
Vitamins, 167, 170 Yolk, nucleus, 46
Vitelline artery, 225 Yolk, placenta, 138
chick, 317, 320 Yolk, plug, 97
pig, 325, 330, 331 Yolk sac, 125,126
Vitelline membrane, 27 chick, 19, 20, 113, 126, 184, 319, 322
Vitelline vein, 125, 178, 824, 2^7 230 Didelphys, 128
chick. 314, 316. 317. 319. 3$D' man, 2B, J 06, J27
.frog, 304 Yolk stalk, 125, 187
pig, 325, 331 Yolk umbilicus, 126, 133, 138
Vitreous humor, 287
Viviparous, 48 Zona pellucida, 36, 37, 38, 142
Viviparous elasmobranchs, 12§ Zone of junction, 91, 126
Vocal cords, 193 Zygote, 24

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Introduction to

New Yor^c • JOHN W I L E y & .S

All Rights Reserved

t Z ^ ^ J , f'''''^' * ' '•'^"'•'^^^ '^^'^'^'' of this material.

1. The study of Embryology 1

2. Reproductive Habits and Vertebrate Life Histories . . 10

3. The Germ Cells—^Their Structure, Origin, and Development . 24

5. The Mechanism of Heredity 58

6. Cleavage and Formation of the Blastula . . . . 79

7. Gastrulation and Neurulation . . . . . . 93

8. Embryonic Form and E.xtraembryonic JMembranes . . 115-

9. The Reproductive Cycle and Placenta of the Mammal . . 135

10. Experimental Embryology . . . . . . 146

11. Digestive System and Related Structures . . . . 171

12. Respiratory Organs . . . . . . . . 188

13. Coelom and Mesenteries . . . . . . . 194

14. The Urinogeniial System . . . . . . 201

15. Blood Vascular System 222

16. The Skeleton 242

17. Muscles . , 253

18. Integument 258

19. Nervous System 263

20. Nerve Terminations . . . . . . . 283

The Study of Embryology

Genetics and Embryology

Phylogeny and Embryology

GENERAL PLAN OF VERTEBRATE DEVELOPMENT

SOME EXPRESSIONS COMMON IN DESCRIBING EMBRYOS

Vertebrates are characterized in the first place by the bisexual

VERTEBRATE LIFE HISTORIES

Fig. 4. Development of man. A, Mature egg, unfertilized, from uterine tube,

Structure of the Cell

Fig. 5. Diagram of a composite cell {ajter Wilson).

The Cell Membrane

THE GERM CELLS

Fig. 6. Diagram of a human sperm (after Gatenby).

concerned with the production of some secretion involved in fertiliza-

Sperm of the Amphioxus

Sperm of the Frog

Fig. 7. Typical sperm. A, Amphioxus (after Ballowitz). B, Frog. C, Fowl.

Sperm of the Fowl

Fig. 9. Egg of Myxine, showing "chorion" and mioropyle {after Dean)

The Egg of the Ampkioxus (^

The Egg of the ^rog C rOoJ)e'^e.tdU^ t ^ hL<L^^HA^)

The Egg of the Chick (_ f e Z « / C^^^^J

Fig. 11. Diagram of sectioned hen's egg {after Adamstone).

Fig. 12. Human egg (ovarian), X200 {.a\tex TFaZde^yer),

The Human Egg

Comparison of the Egg and the Sperm

COMPARISON OF THE VERTEBRATE EGG AND SPEEM

Cell structures Ovum Sperm

Fig.'13. Diagram of gametogenesis: male on left, female on right {after Wilson).

T H E GONIA. There^ are two opinions concerning the fate of the

only to organize the overlying peritoneal epithelium to form the defini-

Spermatogenesis General Oogenesis

At the end of the two maturation divisions the mifochondria and

Fig. 21. Section tlirougb-part of frog testis, X200.

Fig. 22. Diagram to show fertilization of the egg. A, Fertilization cdne: B,

Fertilization of the Amphioxus Egg

Fertilization of the Frog's Egg

Fertilizgjion of the Hen's Egg

Fertilization of t^e Human Egg

Effects of Fertilization on the Egg Cell . *