A M . ZOOLOCIST, 12:159-171 (1972).

When? Why? and How?: Some Speculations on the Evolution of the

Vertebrate Integument
PAUL F. A. MADERSON

Biology Department, Brooklyn College, Brooklyn, New York 11210

SYNOPSIS. The basic structure of the vertebrate integument is briefly reviewed. The
system is either scaled, non-scaled, or a mixture of the two. Scales are not appendages
of the integument, but are patterned folds in which the dermal and/or epidermal
components may be elaborated. An appendage is the product of specialized patterns of
cell differentiation localized within the dermis and/or epidermis. Scales, and appendages (whether borne within scaled or non-scaled integuments), can only be correctly
defined with reference to the chemical or molecular nature of the end-products of
dermal and/or epidermal cell differentiation. Truly homologous integumentary
structures probably do not exist above the class level in modern vertebrates.
Anatomical, developmental, neurological, and paleontological data are presented in
support of a model for the origin of mammalian hair. It is suggested that hairs arose
from highly specialized sensory appendages of mechanoreceptor function which facilitated thermoregulatory behavioral activity in early synapsids. Specialization of cellular
differentiation within these units led to the appearance of dermal papillae. A chance
mutation led to subsequent multiplication of the originally sparsely, but spatially
arranged papillae, causing the induction of a sufficient density of "sensory hairs" to
constitute an insulatory body covering. The insulatory properties of this "prolopelage"
were the subject of subsequent selection, but the sensory function of mammalian hairs
remains important.

INTRODUCTION

The papers presented at this symposium

have indicated the wide scope of currently
available data on the vertebrate integument, which greatly facilitates an evolutionary review. We can now turn away
from those treatments of the past century
which have tended to focus on anatomical
and embryological differences, and rarely,
if ever, considered the problems of function or natural selection with reference to
the origin of specific integumentary structures.
Initial emphasis will be placed upon
denning certain fundamental terms which
are important to any discussion of the existence or non-existence of general trends.
Then follows a consideration of the problem of deciding whether apparently similar
structures have been retained throughout
evolution the conservative interpretation or whether the known developmenThe author's studies on the reptilian integument
have been supported by N. I. H. Grants CA 10844 and 1-PO1-AM-15515. Mrs. Una Maderson
kindly typed the manuscript.

tal plasticity of the integument has permitted the repeated appearance of analogous specializations in convergent response
to functional demands the radical view.
Finally, the evolution of hair is discussed
to illustrate the parameters which should
be considered in dealing with the origin of
apparently unique integumentary modifications.
FUNDAMENTALS

While
the
"mixed"
ectodermalmesodermal nature of the vertebrate integument is well-known, less emphasis is
placed on the fact that of all the major
phyla, only the vertebrates have a multicellular epidermis. This is significant
when we recall that the vertebrate integument never forms a confining exoskeleton
comparable to that of Arthropods, Molluscs, or Echinoderms. Freedom from direct association with locomotory muscle action has not meant, however, that the vertebrate integument does not reflect locomotory needs. Indeed, it is more likely
that the most fundamental patterns of or-

159

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PAUL F. A. MADERSON

ganization of the vertebrate integument

are responses to problems posed by the
basic locomotory patterns.
Whatever the actual protovertebrate
looked like (Berrill, 1955), the small softbodied creature probably possessed an integument similar to that of Amphioxus.
Millions of unrecorded years of evolution
separate this ancestor from the profusion
of early Paleozoic fish forms, but we know
that during this period, increase in body
size was accompanied by a mechanical
strengthening of the body surface. While
the reasons for this are debatable (see discussion, Moss, 1968a), the question presents itself as to how the integument could
be strengthened at all in an animal
whose fundamental locomotory pattern depended on free lateral flexure of the body
(Gray, 1968). Easily envisaged intermediates, with obvious selective advantages, at
least for mechanical protection, lead eventually to either a partial abandonment of
the body mobility "the turtle strategy"
or else folding. As a result of the
latter, any one segment of the body axis
became covered by two or more units
which could move relatively freely over
one another. Since either the epidermal
and/or dermal components of such units
could thereafter be strengthened, this
offered possibilities for mechanical strengthening while retaining the fundamental
functional requirement of lability of the
organ system in toto. We recognize these
folds as "scales," which can therefore
be defined as serial, patterned folds of the
integument in which the epidermal and/
or dermal components may be variously
elaborated so that one or the other type of
tissue may be present in greater quantity,
or be superficially more obvious, than the
other.
Within the definition of a scale given
above, we can describe the integument of
any vertebrate as being "scaled," "nonscaled," or a mixture of the two. In the
case of those forms which definitely do not
have scaled integuments, e.g., cyclostomes,
elasmobranchs, holocephalans, anguilliform teleosts, most modern amphibia,

birds, and most mammals, it is most probable that they are derived from ancestral
stocks whose integument was scaled. Furthermore, the integument of each of these
taxa is characterized by the presence of
complex derivatives various multicellular glands, dermal denticles, hairs, and
feathers. These structures are fundamentally localized centers of specialized epidermal and/or dermal cell proliferation and
differentiation, within an otherwise generalized integument, of which they may
properly be described as "appendages."
Analagous structures may be found within
scaled integuments, in which case the appendages are borne upon (epidermal specializations) (Maderson, 1971), or contained within (dermal ossifications) (Moss,
1972), individual scales. Thus, if a "scaled
integument" is made up of scales, logically
any individual scale is a part of the integument, and cannot therefore be regarded as
an appendage. This distinction is pertinent
to any discussion of integumentary evolution. Where the adult integument is
scaled, the epidermal-dermal cell populations over the embryonic body surface were
originally sub-divided into developmental
fields. Within these fields, appendages
may subsequently differentiate. As will be
discussed later, the evolution, embryogenesis, and adult distribution of hairs and
feathers (Maderson, 1972a) can only be
understood by relating them to such developmental fields.
Vertebrate integumentary structures can
only be defined accurately if one combines
the descriptive terms mentioned above
with a reference to the chemical or molecular nature of the material synthesized by
the constituent cell populations (Table I).
The term "dermal scale," so often used to
describe integumentary structures in piscine vertebrates, has little meaning unless
one refers to the specific end-product of
the interaction between dermis and epidermis in any particular taxon (Moss, 19686,
1972). Similarly, the term "reptilian scale"
has no exact meaning since the differential distribution of keratinaceous proteintypes across the lepidosaurian and ar-

VERTEBRATE INTEGUMENTARY EVOLUTION

161

TABLE 1. A general characterization, of the integument of extant vertebrates following the terminology
and definitions discussed in the text.
Taxon

General
description1

Appendages2

Most conspicuous features3

Unicellular epidermal mucous glands

Denticles*
Dermal ossification with superficial COSMINE layer*
Dermal ossifications with a variety of superficial
mineralizations*
Weak epidermal keratinization: dermal ossifications
No
Amphibians
Unsealed
in some scaled apodans
No
Chelonia
Scaled*
Varied horizontal distribution of epidermal keratin
types
No
Archosauria
Scaled
Horizontal alternation of a- and /3-epidermal keratin
types: dermal ossifications in many regions
No
Lepidosaurs
Scaled
Vertical alternation of a- and ^-epidermal keratin
types: dermal ossifications in many lizards
Yes
Birds
Mixed
Feathers of j3-keratin* arising from a-synthesizing
general epidermis: horizontal alternation of a -and
Yes
Unsealed
Mammals
j9-keratin types on leg scales
Hairs of o-keratin* arising from a-synthesizing general epidermis: dermal ossifications in some forms
1
Applies to the great majority of species in the taxon cited.
3
Only those appendages are mentioned which are usually cited as primary diagnostic features of the
group.
a
Structures or features which are known to involve dermal-epidermal interactions arc marked thus *.
4
The body is primarily scaled, but the development of the carapace, with its associated dermal ossifications, obviously inhibits flexibility. Data from: Alexander (1970); Baden and Maderson (1970);
Moss (1968a,6); Quay (1972); Spearman (I960).
Cyclostomes
Chondrichthyes
Sarcopterygians
Actinopterygians

Unsealed
Unsealed
Scaled
Scaled

Yes
Yes
Yes
Yes

chosaurian scale surfaces (Baden and

Maderson, 1970) makes these units as different in their own way as are feathers and
hairs.
The integumentary morphology of piscine fossils is usually clearly demonstrated
by impressions in the surrounding matrix,
but we need some "rule-of-thumb" for tetrapod fossils. Many extant squamates have
scales which do not contain dermal ossifications. However, with the exception of
Dermochelys (the leatherback turtle), I
know of no living tetrapod which normally
has a wide-spread distribution of dermal
ossifications which does not have a visibly
scaled integument. While this does not
necessarily indicate a 1:1 relationship between externally recognizable units and
individual ossification centers (Zangerl,
1969), it does suggest that in those systems
where developmental fields exist in the
embryonic integument and produce a pattern of dermal ossification, similar fields
influence the topography of the entire integument. Therefore, I suggest that if
paleontologists describe "scales" (dermal

ossifications) in their material, the forms

concerned probably had scaled integuments in the sense defined earlier.
Was the primitive tetrapod epidermis
keratinized? Spearman (1966) indicated
that the potential for keratin synthesis is
widespread among vertebrates, and the reports on the ultrastructure of epidermal
cells (Flaxman, 1972) show that all epidermal basal cells contain the 70-80A wide
filaments which are associated with a-keratin. However, it is also known that in
those tissues where the /?-protein is synthesized (characterized by 30A wide filaments) , the 70A filaments occur first, and
the 30A units appear later and eventually
fill the cells. To me, this implies that the
/?-protein is a later phylogenetic development than the a-form, and this is supported by the distribution of epidermal protein
types in extant amniotes (Baden and
Maderson, 1970). It appears that those
lower Pennsylvanian captorhinomorphs
which gave rise to synapsids and mammals
possessed only the capacity to synthesize
a-keratin. The remainder of the cap-

162

PAUL F. A. MADERSON

FIG. 1. Sagittal section through ventral body scales

of the gekkonid lizard Eublcpharis macularius
just before skin-shedding. The ^-layers of the outer
(/So) and inner (fii) epidermal generations are
thick on the outer scale surface (OSS) , but are
reduced to a single layer of cells on the inner
surface and in the hinge region (ISS, H) . Ddermis; sc- sub-cutaneous tissue.

torhinomorphs, which gave rise to all the

other reptilian groups and birds (Carroll,
1969(1$/:), possessed an additional capacity for /3-protein synthesis in their epidermis, which was variously expressed in different lineages (Table I). What then of the
paleozoic amphibia? Romer and Witter
(1941), Colbert (1955), and Kitching
(1957) described ossified units suggesting a
scaled integument (see above) which was
secondarily modified in their lissamphibian
descendents (Cox, 1967). Findlay (1968a)
suggested that haematite deposits around
the matrix of the lower Triassic Uranocentrodon resulted from the decomposition of sulphur-containing epidermal proteins. While this intriguing interpretation
suggests the presence of keratin, it does not
reveal whether it was of the a- or /J-variety!
Microscopic and ultrastructural studies
indicate that the epidermal tissues on the
inner surface and hinge region of amniote
scales tend to be thinner, less compact, and
more lamellate in their organization than
those on the outer scale surfaces. Different
fluorescent properties of different regions
of amniote scales (Cane and Spearman,
1967; Spearman, 1964, 1966, 1967) cannot
be explained by reference to the presence
of a- or /J-keratins alone (Baden and Maderson, 1970). However, they may reflect
differences in inter-cellular bonding, which
endow the different epidermal regions

with different mechanical properties, and

these originally augmented the flexibility
of the entire integumentary system. This
end is still extremely important in squamates where numerous subtle differences
in patterns of cell production and differentiation modify the basic epidermal generation pattern (Maderson, 1965, 1966;
Maderson and Licht, 1967) over the inner
scale surface and hinge (Fig. 1). However,
the persistent a-protein in these regions in
crocodiles and birds (Baden and Maderson, 1970) and centers of granular layer
formation in mammalian tail scale
"hinges" (Spearman, 1964, 1966) should
be interpreted as relics of the ancestral
functional modifications.
TRENDS IN VERTEBRATE INTEGUMENTARY
EVOLUTION

Raising the question of the possible homology between feathers, hairs, and scales,
Cohen (1964) wrote: "If by homology we
mean that the organs concerned, may, we
believe, be traced back along lines of ancestors until a comparable structure is
reached in the common ancestor, then the
assessment is always made more difficult by
more facts." This conclusion is germane
to the entire topic of integumentary evolution. On the basis of the facts presented
above and their combination with the most
conservative possible deductions regarding
possible integumentary anatomy in fossil
forms, we are forced to conclude that no
two integumentary features in two major
assemblages can be strictly considered to be
homologous. This concept must be restricted to such examples as pelage hair and
spines in mammals, or climbing setae and
the normal Oberhautchen in lizards
(Maderson, 1970). Even the recognition of
general anatomical trends is of limited
value. While piscine vertebrates tend to
have scaled integuments or conspicuous
elaborations of dermal skeletal structures
or both, attempts to define the degree of
homology therein are important only insofar as they lead to consideration of whether dermo-epidermal interactions have or

VERTEBRATE INTEGUMENTARY EVOLUTION

163

phological diversity.
THE EVOLUTION OF HAIR

FIG. 2. An epidermal "Haareorgane" from the dorsal body scales of the gekkonid lizard Gekho gecko.
The epidermis shows a stage 4 condition of the
shedding cycle (Maderson and Licht, 1967) and
shows that the "hair" derives from a modified
Oberhautchen cell (SpOb) . In a sense organ of this
type, although the structure of the epidermal
generation is modified, the subjacent germinal cells
(sg), closely resemble those of the adjacent
non-specialized epidermis. Note the cluster of cells
in the dermis (X) beneath the sense organ here
and in Figures 4 and 5. The /3-layer of the outer
epidermal generation is not seen in the photograph. Other abbreviations, here and in Figures 4
and 5: oo o-layer of the outer generation;
/3i /3-layer of the inner generation; clo clear
layer of the outer generation; lto lacunar tissue
of the outer generation; mi mesos layer of the
inner generation; Obi Oberhautchen of the inner
generation; Obis spinules of the unspecialized
Oberhaulchen cells.

have not changed during evolution. The

question "Are tetrapod scales retained
from the piscine ancestors?" has no meaning except to emphasize that there is a
general capacity for patterned integumentary structure in different taxa with varying degrees of phyletic affinity. Whatever
general trend we define or recognize, it is
always subject to major or minor revision
of execution. In short, I favor the "radical" view of integumentary evolution to
such a degree that I would suggest that in
any instance, a functional question should
be asked, a functional investigation should
follow, and any subsequent detailed anatomical study should be expected to
demonstrate yet another example of mor-

This problem has a number of facets.

First, we must ask, is hair a unique mammalian characteristic? Second, are there
other structures which resemble mammalian hair in other vertebrates, or indeed in
other animals? Third, have hairs always
served an insulatory function, and if not,
what other functions could they have
served? Finally, is it possible to present a
model for the steps in the phylogenetic
development of hair, with plausible explanations for the accompanying selective
pressures?
Recent reviewers (Hopson, 1969; Hopson and Crompton, 1969; Jenkins, 1970)
suggest a monophyletic origin for mammals in the late Triassic - early Jurassic.
Hopson (1969) concluded: ". . . (anatomical, physiological and neuroanatomical
studies) strongly suggest that the common
ancestor of monotremes and therians was
also mammalian in a majority of essential
features e.g. hair, lungs, diaphragm, heart,
and kidneys, to name a few." How many of
these features might have characterized
the early Triassic cynodonts which Hopson
and Crompton (1969) proposed as mammalian ancestors? Reference to possible integumentary structures of therapsids is so
common-place that we may tend to forget
that there is no direct information available. Watson (1931), Brink (1956), and
Findlay (1968ft) interpreted depressions in
skull bones as probably having housed vibrissae or "skin glands of a sweat gland
nature" (Brink, p. 87). These interpretations were extrapolated to suggest pelage
hairs and normal sweat glands over the
rest of the body. Repeated associations between these "extrapolated interpretations"
and actual mammal-like osteological features in support of suggestions of endothermy in therapsids have produced a
situation so close to circuitous argument
that it is time to seek a new approach to
the problem of the origin of hair.
No extant vertebrates have integumen-

164

PAUL F. A. MADERSON

tary appendages which anatomically resemble hairs. The structures seen in many
lizards (Fig. 2), once invoked as "ancestral
hairs" (Elias and Bortner, 1957), are sensory units (Miller and Kasahara, 1967) derived from individual cells of the Oberhautchen (Schmidt, 1920; Maderson and
Licht, 1967; Maderson, 1971), which layer
is a unique constituent of the lepidosaurian epidermis (Maderson, 1968a). While
the anatomy of the individual units is certainly not homologous with that of any
vertebrate epidermal derivative, a number
of insects have a "pelage" (Heath, 1968).
Although the pelage plays a primary
role in insulation in most mammals (Ling,
1970) and in some insects, various vertebrates, e.g., lizards, or man, manifest endothermic regulatory mechanisms of varying degrees of "perfection," but do not possess a continuous body covering of this
type. Conversely, the presence of a covering pelage does not necessarily indicate an
absolutely constant internal temperature
throughout life (Heath, 1968). There is
therefore no a priori reason for assuming
that therapsid thermoregulation could not
have evolved in the absence of a pelage.
Indeed, the physical laws which govern the
functioning of a pelage indicate that each
constituent unit must have a certain minimum length, and there must be a certain
minimum density per unit area of the body
before any selective advantage accrues
with regard to insulating function (Ling,
1970). It seems most unlikely that a "preadapted proto-pelage," upon which selection could act, could have appeared via a
steady accumulation of "neutral traits"
affecting epidermal morphogenesis over
several thousand generations. A more
plausible hypothesis is that the insulating
function of hair is secondary and became
possible only after completely different selective advantages had favored suitable
morphogenic changes in the epidermis.
These primary selective pressures can be
identified if we consider the probable ecology of the extinct forms concerned, and
thence deduce the obligatory minimal
functions of their integument.

Studies of Pennsylvania reptile fossils

(Carroll, 1964, 1969a,bjC, 1970a,b) suggest
that they were small, highly terrestrial, forest-dwelling forms. Carroll (1970&) writes
of the captorhinomorph Hylonomus lyelli:
"in size and general form it resembles a
medium-sized lizard. It may have had similar habits as well." I suggest that functionally the integument of such forms would
have resembled that of modern lizards.
The epidermis would have possessed a
well-developed outer cornified region
which would have provided a degree of
protection against dessication (Maderson
et al., 1970). Carroll's (1964) descriptions
of osteoscutes suggest a scaled integument
(see above), so that both dermal and epidermal components probably contributed
to mechanical protection. Since holocrine
secretion is a very important function in
modern lizards (Maderson, 1970), this may
have been true for the earliest reptiles.
However, in most modern amniotes,
odoriferous sources are localized on the
body surface: the pheromonal function of
sweat-glands in some mammals is probably
secondary. My own observations on a
great variety of modern lizards suggest that
if behavioral thermoregulation characterized the earliest reptiles, this would not
have necessitated any particular morphological structure of the integument, except
perhaps with regard to the distribution of
pigment cells (Porter, 1967). If the integument of primitive reptiles manifested other
secondary functions (e.g., climbing claws,
poison glands, sexual or territorial warning appendages), comparative observations
on modern amniotes indicate that associated structural modifications would have
been localized on the body surface.
Apart from the "primary barrier function" of physiological and mechanical protection which influences the fundamental
morphology of the entire integument
(Maderson, 1971), there is only one secondary integumentary function which potentially involves the entire organ system
that of sensory reception. Two quite
different types of sensory stimulus have
always impinged upon the terrestrial in-

VERTEBRATE INTEGUMENTARY EVOLUTION

<?/*.

FIG. 3. Schematic representation of a mammalian

tylotrich hair follicle modified after Straile (1969) .
1 - hair shaft; 2 - internal root sheath; 3 - external
root sheath; 4 - germinal region of the tylotrich follicle; 5 - dermal papilla; 6 - connective
tissue sheath; 7 - annular complex; 8 - epidermal
pad complex; 9 - neurons associated with slowadapting mechanoreceptors; 10 - mouth of sebaceous gland (body of gland not shown) ; 11 venular complex associated with tylotrich unit (arteriolar complex not shown) .

165

tegument temperature
and
touch.
These categories can be further subdivided since gradual changes in ambient
temperature, or casual contact with the
substrate during locomotion, are interpreted by the brain quite differently than
are sudden temperature changes, or sharp
pressures. Any or all of any variety of
types, or levels, of stimulation might challenge any part of the body surface. It is
therefore predictable that there would be a
spatial pattern of functional differentiation across the integument, which might be
reflected anatomically in patterns of nerve
distribution and/or the morphology of
the receptor-transducer units.
I propose that mammalian hairs are derived from complex epidermal modifications of mechanoreceptor function, which
were originally "sparsely," but regularly,
distributed over the surface of the body. At
some stage in the evolution of the therapsid integument, the competence of the developmental fields centered around the
original units changed, resulting in a multiplication of basically similar morphogenic events. These events produced a sufficient density of "sense organs" per unit
area of the body to produce a "pelage," the
insulative properties of which were the focus for subsequent selection. The sensory
function of hair in modern mammals does
not exactly resemble that of the original
units, but this does not affect the morphological model which will be presented. The
data supporting this hypothesis will now
be discussed.
Straile (1969) proposed "repeating vertical units" in the mammalian integument
containing epidermal, neural, and vascular
elements arranged around a "tylotrich"
hair follicle (Fig. 3). The tylotrich is associated with two innervated regions, an annular complex surrounding the upper
third of the follicle, and an adjacent epidermal pad complex. Although the exact
construction of the vertical unit varies
across the body, and between taxa, tylotrichs have been observed in monotremes
and many therian mammals (Mann, 1968).
While there is some disagreement as to

166

PAUL F. A. MADERSON

tween the two conditions.

There is an impressive variety of epidermal sensory modifications in reptiles (Miller and Kasahara, 1967) (Figs. 2, 4, 5).
There are no systematic investigations of
any single type available, but the distribution of "Haareorganes" suggests a function
of monitoring inter-scale contact (Maderson, 1971). Bailey (1969) demonstrated
fast and slow-adapting mechanoreceptors
by electro-physiological techniques, but
did not provide an anatomical correlation.
The anatomy and functioning of the infra-red sensitive cutaneous pit organs in
snakes have been extensively studied (Barrett, 1970; Meszler, 1970). Although the
mm 4
data are sparse, we can say that cutaneous
FIG. 4. Sense organ from a labial scale of the
sensory reception does occur in reptiles,
iguanid lizard Iguana iguana. The epidermis is in
and the diversity of associated morphologithe resting phase of the shedding cycle (Maderson
cal specializations suggests that it is an exand Licht, 1967) . In this type of sense organ, the
tremely important function.
associated germinal cells are always columnar and
have vesicles at their distal tips. The mature kerElias and Bortner's (1957) morphologiatinized elements of the outer epidermal genercal
schema of hair phylogeny rests on the
ation are indicated by dotted lines. /So - /3-layer o
premise of a direct relationship to the lathe outer generation.
certilian "Haareorgane" which is no longFIG. 5. Sense organ from a lateral body scale of
er acceptable (see above). While the
the xantusiid lizard Xantusia vigilis. The epidermis
morphogenic events in hair development
is in stage 4 of the shedding cycle, and we note
are difficult to relate to any possible evoluthat although this type of sense organ does not
protrude above the general level of the skin
tionary sequence, if one ignores the details
surface, it is associated with a modification of the
involved, one can derive a useful, simplyhistogenesis of the inner generation which produces
stated overview. A portion of the germinal
mature elements (dotted outlines) analagous
population becomes specialized so that its
to those seen in Figure 4.
daughter cells stick together as a rod which
how the electro-physiological data should projects above the skin surface, while the
be related to the anatomical data (see dis- daughter cells of adjacent, unspecialized
cussion, Straile, 1969), there is good evi- inter-follicular epidermis do not stick todence that both rapid and slowly adapting gether so tightly and therefore desquamechanoreceptors are represented within mate. The process of initial specialization
repeating vertical units so that: "The de- and adult homeostasis involves mesoderm
tection of a tactile stimulus moving from cells ("the dermal papilla"), and the two
point to point probably involves the inter- cell populations influence one another via
pretation of a complex series of nerve im- a sequence of inductive processes which we
"epithelial-mesenchymal
interacpulses that are received by the brain" term
tions"
(see
Kollar,
1972).
The
elegant
(Straile, 1969). My own familiarity with
the scaled reptilian integument, where complexity of the hair follicle, which at
even cursory examination reveals a pleas- first sight seems so difficult to explain in
ing geometric order, has long made me evolutionary terms, may be readily explained. It permits a "good rod" to grow
suspicious of the apparent heterogeneity of
from a "good hole," a mere refinement
the mammalian system. Straile's "re- which could have occurred quite late in
peating vertical unit" seems to me to the phylogeny of hair. It should be noted
provide the required conceptual link be-

VERTEBRATE INTEGUMENTARY EVOLUTION

16?

age (Carroll, 1964, 1969a,b,c, 1970a,6; Clemens, 1970; Hopson, 1969; Hopson and
Crompton, 1969; Jenkins, 1970) indicate
that the creatures concerned were of small
size less than 18" total length. However,
throughout the geological eras concerned,
related forms and other amphibian and
reptilian groups radiated to produce genera of considerable size. The mammalian
grade of organization with its attendant
morphological characteristics, e.g., hair,
was perfected over a period of 200 million
years by small animals, possibly crevice
dwellers, who probably attained their evolutionary destiny by exploiting nocturnal
niches, following gradual refinement of
thermoregulatory mechanisms.

FIG. 6. Suggested model for the sequence of morphological changes in the evolution of mammalian
hair, a - suggested integumentary structure of a
primitive cotylosaur; b - suggested integumentary
structure of a cotylosaur associated with synapsid
lineage; c - suggested integumentary structure of a
pelycosaur associated with the therapsid/mammalian lineage; d - e - magnified views of suggested
evolutionary changes in the original "hinge" region
of c (outlined) . Medium dense fine stipple epidermis showing basic a-protein synthetic capacity;
dense fine stipple epidermis where cell maturation involves keratohyalin; sparse fine stipple dermis; clusters of fine stipple dermal papilla;
dashed lines neurons associated with fast-adapting mechanoreceptors; heavy dotted lines neurons
associated with slow-adapting mechanoreceptors;
cross-hatching dermal ossification. For explanation, see text.

that holocrine secretion from lacertilian

pre-anal organs (Maderson, 19686, 1970,
1971, 19726) frequently produces a durable "rod" of mature cells which may protrude a considerable distance from the skin
surface. However, there are no specializations comparable to the various layers of
the inner and outer root sheath seen in a
hair follicle.
Before we consider the model, it should
be mentioned that all recent accounts of
the amphibian-reptilian-mammalian line-

A possible structure of the early cotylosaurian integument is shown in Figure

6a. The epidermis contained only a-keratin, and the tissue was thinned on the
inner scale surface and hinge region. A
plausible suggestion for the differential
distribution of mechanoreceptors would
place fast-adapting units on the outer scale
surface. These monitored transient environmental contact during normal locomotion. Locomotory activities involving
stretching or compression of the integument (e.g., twisting of the body into small
crevices and hiding) could have been monitored by slow-adapting receptors in the
hinge region. Dermal ossifications were
present and possibly played some mechanical protective role.
In those cotylosaurs associated with the
basic synapsid stock and the derived forms,
certain modifications characterized the integument (Fig. 6b). I propose that the
involvement of keratohyalin in the keratinization process, at first confined to the
hinge region (Spearman, 1964, 1966), enhanced the overall flexibility of the integument and permitted a reduction of scale
overlap. This additional protein could
have resulted from a single gene change,
since similar proteins exist in the epidermis of modern reptiles (Maderson et al.,
1972) and birds (Alexander, 1970). Reduction of scale overlap is suggested by the
scarcity, or absence, of dermal ossifications

168

PAUL F. A. MADERSON

in synapsid material. The modified pat- depends upon the cooling influences at the
tern of protein synthesis may have per- skin surface. Any animal which could monmitted a thickened epidermis on the outer itor such influences, and accordingly adscale surface to provide mechanical protec- just its position in the environment, could
tion and perhaps decrease percutaneous achieve more subtle temperature regulawater-loss. The groups of fast-adapting tion. More importantly, it could take admechanoreceptors probably became local- vantage of "heat availability situations"
ized within regions of hypoplasia. The re- which would be beyond the sensory analytduction of scale overlap diminished the ical capacities of other forms.
original function of the slow-adapting reFigure 6c is a suggested skin structure of
ceptors in the hinge region for monitoring a pelycosaur at the base of the therapsidinter-scale contact. However, the function mammalian lineage. Certain general trends
of providing sensory data during hiding described earlier have continued, i.e., recould have been maintained if the nerve duction of scale overlap, spread of the
endings became associated with a small ep- granular layer, epidermal thickening. The
idermal papilla which protruded to a level slow-adapting mechanoreceptors originally
just beneath the general level of the outer seen in the hinge region are now associscale surfaces during normal locomotion.
ated with a longer papilla, the primary
The widespread occurrence of thermo- function of which is still monitoring enviregulatory behavior patterns in modern ronmental contact during hiding activity.
reptiles (Bellairs, 1969) implies that they When the body is still during sun-basking,
arose very early in reptilian evolution. If, these papillae protrude above the general
indeed, Triassic therapsids did manifest body surface. Their mechanoreceptor acsome degree of homeothermy (Heath, tion could detect displacement of their dis1968), we might postulate that the coty- tal tips by air-movements. Figures 6d-f suglosaur-synapsid lineage possessed some spe- gest how further selection might have imcial feature permitting the precocious de- proved the functioning of this levervelopment of this grade of organization activated mechanoreceptor.
relative to other reptilian lineages. Bailey's
Figure 6f shows a rod of cells which
(1969) data suggest that cutaneous ther- grows out from a follicle; movement of the
moception in lizards is insufficiently sensi- distal tip of the rod distorts the entire
tive to facilitate thermoregulatory behav- structure leading to activation of the neuior. Heath (1968) indicated that while rons which are now associated with the
peripheral temperature receptors modulate upper third of the follicle. The daughter
hypothalamic responses to environmental cells arising from the germinal region of
temperature change in mammals, he the follicle form a tightly adhering mass,
stated: "The cold-blooded terrestrial ani- and specialization of the outermost cell
mals may rely largely on internal recep- layers would endow this "rod" with specific
tors." Such receptors can only provide in- mechanical properties associated with
formation regarding heat energy after it flexibility. These patterns of cellular activhas been absorbed; they cannot critically ity are sufficiently distinct from those of
examine possible differential heat-sources surrounding "interfollicular" epidermal
in the environment on a "minute-by- cells to imply the presence of a distinct
minute basis." For this reason, the ther- morphogenetic mechanism responsible for
moregulatory behavior patterns of modern their control. At this stage in evolution,
lizards involve quite sudden movements the dermal papilla appeared. It does not
from one type of exposure to another, fol- matter whether this structure arose initiallowed by equally rapid increases or de- ly as an embryonic or an adult "inducer,"
creases in deep body temperature (McGin- since its fundamental role maintenance
nis and Dickson, 1967). The amount of of a specialized sequence of differentiative
heat absorbed by the deep body tissues events for a circumscribed germinal/

VERTEBRATE INTEGUMENTARY EVOLUTION

169

-.** M
FIG. 7. Sagittal section through rat tail scale
showing a hair follicle growing from the "hinge
region." The restriction of the granular layer to

the follicle mouth area is indicated by arrows.

H hair shaft.

daughter cell population within an otherwise homogeneous epidermal system is

the same at all stages of the life cycle.
The model to this point suggests that
although the postulated specialized mechanoreceptor which should be compared
to the tylotrich hair follicle (Fig. 3)
did not evolve from a scale, it was
initially associated with a morphogenic
field surrounding a scale and eventually
superseded it in size and importance. This
premise receives support from the following data. First, tylotrichs develop first in
the embryo (Mann, 1968). Second, tylotrichs are more numerous dorsally than
ventrally (Mann, 1969) a similar condition is seen with regard to scales in most lizards. Third, recalling that the sequence of
events under discussion concerned small
animals, we note that Mann (1969) stated:
"The larger the mammal, the fewer the
tylotrichs per unit surface area of the
skin." Fourth, the described sequence of
events accounts for hair distribution across
the scaled caudal integument of some
modern mammals (Spearman, 1964, 1966)
(Fig- 7)
The integumentary structure shown in
Figure 6f might have characterized a small
early therapsid with a highly sophisticated
thermoregulatory behavior pattern. However, the function of the spatially dis-

tributed "eotylotrichs" was exclusively

mechanoreceptive, and such structures
could not have served an insulatory function. I suggest that this secondary function
arose following the multiplication of follicular units within the original "scale morphogenic field" surrounding the eotylotrich.
The model suggests an association between a certain level of morphologic complexity and the evolutionary appearance of
a dermal papilla. Cohen (1964, 1969) has
emphasized the similarity in organization
of hairs and feathers, and Maderson
(1972a) has proposed the origin of the
dermal papilla of feathers for similar morphogenic reasons to those presented here.
Ede et al. (1971) investigated the failure
of feather development in the talpid3 mutant chick embryo and demonstrated a defect of dermal papilla formation. While
comparable detailed ontogenic analyses are
lacking, Mann (1969) listed recessive
point mutations in mice which disturbed
normal tylotrich development. I submit
that it is equally possible that multiplication of follicular units could have occurred
as the result of a single gene change in
our therapsid ancestors. The only question
is, what selective advantage accrued which
favored the survival and spread of such a
gene change? There are two possibilities,

170

PAUL F. A. MADERSON

which are not mutually exclusive. The increase in number of units reached or surpassed the minimum density per unit area
necessary to provide insulatory benefits.
Alternatively, since secondary hair follicles
in modern mammals are associated with
rapidly adapting touch receptors (Straile,
1969), one could argue that the "leveractivated" receptor associated with the
slow-adapting receptors (the eotylotrich)
was so successful that selection favored the
incorporation of the fast-adapting units
into secondarily derived similar structures.
I favor the second of these explanations
since it does not necessitate quantum
changes in anatomical structure and does
offer possible successive levels of cutaneous
organization, culminating in an insulatory
pelage.
The model which has been presented
here is highly speculative, but this is inevitable due to the nature of the subject. The
premise of a mechanoreceptor origin for
mammalian hair is not new, but it has
never before to my knowledge been considered in detail with reference to a series of
selective pressures. I would like to emphasize in conclusion, that if the level of
mechanoreceptor organization shown in
Figure 6f were typical of most cynodonts,
enlarged units could have formed the facial vibrissae discussed earlier. If we accept
Heath's (1968) and Bailey's (1969) statements with reference to deep and cutaneous thermoreception in mammals versus
reptiles, we might even suggest that it was
only in the phyletic line leading to mammals that peripheral modulation of hypothalamic temperature responses developed. This could have been that last
subtle refinement in endothermy which ensured the success of the lineage.
Right or wrong, this discussion will have
served its purpose if it stimulates further
interest in mammalian cutaneous reception, but even better, it should lead to
comparable studies on modern lizards, the
epidermis of which is, after all, the zenith
of amniote integumentary evolution.

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