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Evolving Form and Function:
Fossils and Development
Proceedings of a symposium honoring
Adolf Seilacher for his contributions to paleontology,
in celebration of his 80th birthday

Derek E. G. Briggs, Editor

April 1– 2, 2005
New Haven, Connecticut

A Special Publication of the

Peabody Museum of Natural History
Yale University
New Haven, Connecticut, U.S.A.
December 2005
 Evolving Form and Function: Fossils and Development
Proceedings of a symposium honoring Adolf Seilacher
for his contributions to paleontology, in celebration of his 80th birthday
A Special Publication of the Peabody Museum of Natural History, Yale University
Derek E.G. Briggs, Editor
These papers are the proceedings of Evolving Form and Function: Fossils and Development,
a symposium held on April 1–2, 2005, at Yale University.

Yale Peabody Museum Publications

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Design by Rosemary Volpe • Index by Aardvark Indexing
Cover: Fossil specimen of Scyphocrinites sp., Upper Silurian, Morocco (YPM 202267).
Purchased for the Yale Peabody Museum by Dr. Seilacher. Photograph by Jerry Domian.
© 2005 Peabody Museum of Natural History, Yale University. All rights reserved.
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Evolving form and function : fossils and development : proceedings of a symposium honoring Adolf
Seilacher for his contributions to paleontology, in celebration of his 80th birthday : April 1-2, 2005, New
Haven, Connecticut / Derek E.G. Briggs, editor.
p. cm.
Includes bibliographical references and index.
ISBN-10: 0-912532-72-6 (alk. paper)
ISBN-13: 978-0-912532-72-1
1. Evolutionary paleobiology--Congresses. I. Seilacher, Adolf. II. Briggs, D. E. G.
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∞ This paper meets the requirements of ANSI/NISO Z39.48-1992 (Permanence of Paper).

Growth and Form in Echinoids:
The Evolutionary Interplay of
Plate Accretion and Plate Addition
Andrew B. Smith
Department of Palaeontology, The Natural History Museum
Cromwell Road, London SW7 5BD United Kingdom
E-mail: a.smith@nhm.ac.uk

Abstract
There is a marked change in the nature of disparity between Paleozoic and post-Paleozoic echi-
noids. Paleozoic echinoids are rather similar in overall shape but differ noticeably in the num-
bers of columns of plates that make up their test, whereas post-Paleozoic echinoids have
diversified into a great variety of shapes, but retain a fixed number of columns of plates in their
test. This difference is explained as the outcome of two major evolutionary changes in growth
strategy. In Paleozoic echinoids growth is achieved almost exclusively by plate addition, with
little or no subsequent accretionary growth of individual plates. Tests enlarge simply by adding
more plates and more columns of plates. The first clear evidence of sustained growth and re-
modelling of individual plates is found in late stem group archaeocidarids, and this innovation
resulted in a striking reduction in the number of plates and columns needed to build a large
test. This archaeocidarid growth strategy, combining plate addition and plate accretion, was in-
herited by all post-Paleozoic echinoids. The second major innovation involved shifting plate
production to a much earlier stage in ontogeny, so that the final (adult) positions of plates be-
come established immediately after metamorphosis. Plate accretion then becomes the domi-
nant mode of test growth. This trend is first seen in primitive irregular echinoids and is at its
most pronounced today in the Atelostomata and Clypeasteroida. Both have therefore been able
to diversify in shape and have developed regional specialization of spines and tube feet, thereby
arriving at higher levels of morphological diversity than other echinoids.
Keywords
Sea urchins, ontogeny, skeletal growth, evolutionary trends, growth trajectories.

Introduction

From their very first appearance in the Late Ordovician, echinoids have had a distinctive skeleton.
This is constructed of many individual plates that interlink to form a typically subglobular frame
or test. Like that of all echinoderms, the echinoid skeleton is formed in the mesoderm and is cov-
ered externally by epidermis, and each plate is composed of calcite with a very distinctive mi-
croarchitecture, termed stereom. In the great majority of echinoids the plates abut and are bound
together by collagenous fibers to form a rigid structure. This skeleton provides protection to the
internal organs, and a firm foundation for the attachment of the jaw apparatus and the various
articulated appendages, together with their associated muscles.
There is, however, a striking difference in the appearance of Paleozoic and post-Paleozoic
echinoids and the way in which their tests are constructed. In all post-Paleozoic echinoids the
skeleton is built following a very conservative plan. There is an apical zone of genital and terminal

© 2005 Andrew B. Smith. All rights reserved.

From Evolving Form and Function: Fossils and Development: Proceedings of a symposium honoring Adolf Seilacher for his contributions to
paleontology, in celebration of his 80th birthday. D.E.G. Briggs, ed. New Haven: Peabody Museum of Natural History, Yale University.
ISBN-10: 0-912532-72-6; ISBN-13: 978-0-912532-72-1. © 2005 Peabody Museum of Natural History, Yale University. All rights reserved.
Figure 1. Representative post-Paleozoic and Paleozoic echinoids showing the range in body plans. A, Tem-
nocidaris (Stereocidaris); Upper Cretaceous, England (Cidaroida). B, Echinosigra; Recent, Atlantic (Holas-
teroida). C, Rotula; Recent, West Africa (Clypeasteroida). D, Aceste; Recent, South Atlantic (Spatangoida). E,
Bromidechinus; Upper Ordovician, USA. F, Bothriocidaris; Upper Ordovician, Estonia. G, Lepidesthes; Lower
Carboniferous, USA. H, Pholidechinus; Carboniferous, USA. I, Myriastriches; Silurian, Wales. J, Aulechinus;
Upper Ordovician, Scotland. Abbreviations: amb, ambulacral zone; Ia , interambulacral zone.
 Growth and Form in Echinoids • Smith 183

plates at one pole, and a peristomial membrane, which is usually plated, at the opposite pole, sur-
rounding the mouth. The corona, which lies between these two plated zones, makes up the vast
bulk of the skeleton and is formed of just 20 columns of plates arranged as pairs of ambulacral
and interambulacral columns (Figure 1A). The shape of the test, though often subglobular, is
highly variable, particularly in irregular echinoids where bottle-shaped (Figure 1B), discoidal
(Figure 1C) and heart-shaped (Figure 1D) morphologies have evolved.
Paleozoic echinoids are much more variable in the number of columns that make up the
corona, in both interambulacral and ambulacral zones. This variation is evident right from the
start of their fossil record, in the Late Ordovician. Bromidechinus (Figure 1E) has 25 columns of
plates, each fifth of the test comprising two columns of interambulacral plates and three columns
of ambulacral plates: Bothriocidaris (Figure 1F) has only 15 columns of plates, all ambulacral;
while Aulechinus (Figure 1J) has narrow ambulacral zones composed of two columns of plates
and wide interambulacral zones with six or seven columns of plates. This marked variation in the
composition of the test continues to occur throughout the Paleozoic. The Carboniferous Lepides-
thes (Figure 1G) has very wide ambulacral zones and narrow interambulacral zones, whereas the
contemporaneous Pholidechinus (Figure 1H) has just the opposite, wide zones of interambulacral
plates and narrow ambulacral zones. The Permian–Carboniferous Cravenechinidae have up to
eight columns of plates in each ambulacral zone, but only a single column of plates in each inter-
ambulacral zone (for additional illustrations see Jackson 1912; Kier 1965; Smith 2005). Yet de-
spite this variation all Paleozoic echinoids remained basically subglobular in form. This marked
difference between Paleozoic and post-Paleozoic echinoids is striking and well known. Surpris-
ingly, it has never previously been investigated or explained. Seilacher (1991) developed a me-
chanical– constructional model of echinoid shape based on the pneu concept to explain diversity
of form. However, this was concerned only with overall adult shape and took no account of
plating or its ontogenetic development (see also Phillipi and Nachtigall 1996). Here I take a dif-
ferent approach, one that focuses on the evolution of echinoid growth strategies.

Test Growth in Extant Echinoids

The echinoid test grows by a combination of two processes, plate addition and plate enlargement
or accretion. Plates that make up the adult skeleton start to form in the imago during metamor-
phosis. The very earliest plates to form are those of the apical disc (Gordon 1926, 1927, 1929) and
these are in part derived from the larval skeleton (Emlet 1985, 1989). By the time the metamor-
phosing larva settles to the sea floor, the first few plates of each ambulacral and interambulacral
column have already appeared. Then, as the individual grows, new ambulacral and interambula-
cral plates are added and are initiated at the distal edge of the five terminal plates (Jackson 1912;
Figure 2). As a consequence plates progressively shift adorally away from the apical disc as in a
conveyor belt, with the earliest formed plates found closest to the mouth on the lower surface. In-
dividual plates, once formed, are subsequently enlarged by accretion of stereom, which is added
both around the plate periphery and across the inner surface, thickening the plate and creating
concentric growth lines (Smith 1980b; see Figure 2). There may also be some resorption of the
earliest plates adjacent to the peristomial margin.
The relative emphasis given to the processes of plate addition and plate accretion during on-
togeny is fundamental to the adult form eventually achieved by the skeleton, and has changed sig-
nificantly over geological time. The evolutionary trend in echinoids has been to switch from growth
by plate addition to growth by plate accretion. The aim of this paper is to document when this shift
took place, and to explore the history and consequences of this important change in growth strategy.

Growth in the Earliest Echinoids

Echinoids first appeared in the Late Ordovician (Smith and Savill 2001) and grew by plate ad-
dition at the apex. Aulechinus (see Figure 1J) and Eothuria have two columns of ambulacral
184 Evolving Form and Function: Fossils and Development

Figure 2. Test of the sand dollar Dendraster ventruraensis Kew (Upper Pliocene, Las Posas Hills, Camavilla,
California). A, Test in apical view; the plate boundaries show up clearly as dark lines. B, Detail of test (as in-
dicated in A) showing terminal plates (tp) of apical disc and adapical portions of ambulacral (amb) and
interambulacral (Ia) zones. Note the growth lines visible in the plates. C, Detail of one interambulacral plate
showing distinct concentric growth banding (arrow).

plates, but multiple columns of thin interambulacral plates. A small terminal plate is present at
the summit of each ambulacral column and was presumably the initiation point for new inter-
ambulacral and ambulacral plates. Plates in the vicinity of the terminal plate are smaller than
those slightly more adoral in position. However, at least in Aulechinus, just two columns of
interambulacral plates were initiated adapically, one on either side of the terminal. There is a re-
 Growth and Form in Echinoids • Smith 185

gion close to the apex where, immediately after formation, the interambulacral plates become
reorganized into four or five irregular columns. MacBride and Spencer’s (1938) original draw-
ings showed a few smaller interambulacral plates interspersed among larger ones. This, together
with the lack of a clear terminal plate, presumably was what led Mooi and others (1994) to infer
that primitive echinoids lacked true interambulacra. However, in well-preserved material it is
clear that the interambulacral plates are rather uniform in size and semiregularly arranged into
columns, and that the irregularity illustrated by MacBride and Spencer (1938) reflects breakage
and postmortem distortion of the fragile skeleton. In all of these forms plates were added at the
apex and moved adorally during growth.
In another Late Ordovician echinoid, Bromidechinus (see Figure 1E), the earliest formed
interambulacral plates (that is, those closest to the peristome) are uniserially arranged (Smith and
Savill 2001), but during ontogeny this quickly changed to the generation of two regular columns,
as in post-Paleozoic echinoids. Unusually, in this taxon there are three ambulacral columns, a me-
dian imperforate one flanked on either side by a column of perforate plates.
The individual plates of these primitive echinoids are thin sheets of calcite only a few layers
of stereom thick. None show any sign of accretionary growth and, except in close proximity to the
apex, plates remain broadly similar in size irrespective of the size of the body and their position
on the test. Unfortunately, because most species are known from just fragmentary or distorted
material, it is not feasible to plot their growth trajectory. However, it seems reasonable to conclude
that body size increased by addition of new plates that formed rapidly, and that there was little or
no subsequent accretion or enlargement of elements.
By the Silurian a rather regularized pattern of growth had been adopted by the Lepidocen-
tridae, involving simple rhomboidal elements arranged in horizontal and vertical series. In Ap-
tilechinus plates continued to be added to each column as the test grew. A specimen 14.5 mm in
test height has about half the number of interambulacral plates in a column compared to a spec-
imen 30 mm in test height (specimens illustrated in Kier 1973). In addition, the number of
columns reduces approaching the peristome, showing that fewer columns of plates were gener-
ated at the apex during the earlier ontogenetic stages. This style of growth reached an extreme in
Myriastiches (see Figure 1I) where vast numbers of very small, identical plates built up the inter-
ambulacral zones.
A detailed description of the growth of a Carboniferous echinoid was given by Kesling and
Strimple (1966, pl. 154), who studied a range of different-sized individuals of the lepidesthid Lep-
idesthes (Figure 1G). They identified a periapical zone in which ambulacral plates were initiated,
grew and became relocated into multiple columns. During growth the number of ambulacral
columns in Lepidesthes increases from four to eight, while the number of interambulacral
columns increases from four to five. Furthermore, as new plates are added adapically the more
adoral regions with fewer columns zones do not increase in size, indicating that there was little or
no subsequent growth of these plates.
In summary, all these Paleozoic echinoids grew by the continuous addition of simple, iden-
tical elements that underwent little or no subsequent modification or differentiation after an ini-
tial phase of growth and relocation. Such growth is simple to program developmentally, but very
limiting, because no specialization of elements is possible as growth proceeds.

The Appearance of Growth by Plate Accretion

Most Paleozoic echinoids conform to a simple conveyor belt model of growth, in which plates re-
main unspecialized and undifferentiated as they move from aboral to oral surface during on-
togeny. However, by the Carboniferous a simple oral–aboral differentiation is evident in one clade,
and we see the first evidence of sustained accretionary plate growth.
Oral–aboral differentiation is weakly developed in the Proterocidaridae where it affects only
the ambulacral plating. In this family the ambulacral plates on the oral surface are larger and bear
larger pore pairs (and presumably larger tube feet) than those of the aboral surface (Kier 1965).
Figure 3. Interambulacral plate of Archaeocidaris from the Lower Carboniferous. A, NHM E42228, external
surface and detail of two of the bands of denser stereom radiating from the primary tubercle to each scro-
bicular tubercle. These bands mark lines along which stereom resorption has occurred as the scrobicular tu-
bercles have shifted outwards during growth of the plate. B, NHM E31015, internal surface and detail of
stereom. Stereom here shows a zonation in pore size, with larger-pored stereom sandwiched between two
zones of smaller-pored stereom (indicated by black and white lines). Insert, Archaeocidaris rossica (Buch) in
oral view, after Jackson (1912, pl. 11, fig. 1).
 Growth and Form in Echinoids • Smith 187

The difference is slight in Hyattechinus, where only the first 14 or so plates are enlarged, but is
more pronounced in others such as Proterocidaris and Pronechinus. Because no growth series is
available for Hyattechinus it is not clear whether pore pairs and tube feet become differentiated as
they move into an oral position, or whether there is early specification of oral and aboral plates
with minimal migration of elements from aboral to oral side. In Pronechinus, however, the two
forms of pore pairs and tube feet co-occur on the oral surface on alternate plates in the same
columns, and in Proterocidaris the number of oral ambulacral plates continues to increase as test
size increases (compare juvenile and adult illustrated by Kier 1962). Both observations suggest
that these forms did not have a determinate number of oral plates and that tube feet become dif-
ferentiated as they move onto the oral surface.
Archaeocidarids are the only Paleozoic group to have evolved large interambulacral spines.
They also show a corresponding increase in the size of interambulacral plates. Furthermore, in
Archaeocidaris interambulacral plates show signs of growth banding internally, and evidence of
remodelling on the external surface. Growth banding on the internal surface takes the form of a
zoning of stereom, expressed by a difference in pore size and trabecular thickness (Figure 3B).
However, such growth banding is unusual, and in most cases the stereom is uniform over the en-
tire plate. Presumably, as the plate grew new layers of stereom were added over the entire inner
surface of the plate. The outer surface of interambulacral plates commonly displays a pattern of
stripes of modified stereom leading radially outwards from the primary tubercle towards each
surrounding secondary tubercle (see Figure 3A). A similar pattern is seen in modern echinoids,
the result of outward migration of scrobicular tubercles (the secondary tubercles supporting the
spines that form a protective ring around the muscle field of the primary spine) through simul-
taneous resorption of calcite on the inner side and deposition on the outer side as the central pri-
mary tubercle enlarges (Smith 1980a). This provides direct evidence that the primary tubercles
in Archaeocidaris grew in size as the plates enlarged. Here, therefore, is the first evidence for a sig-
nificant switch in growth strategy from plate addition to plate accretion and remodelling.
Archaeocidarids represent the advanced stem group Echinoidea, on the line leading to all
modern echinoids. Kier (1968) noted several important evolutionary trends along this line, in-
cluding the increasing size of interambulacral plates and the decrease in the number of interam-
bulacral columns, both of which mark the switch in emphasis from growth by plate addition to
growth by plate accretion. Earlier archaeocidarids, such as Deneechinus, Lepidocidaris and Nor-
tonechinus, have plates composed of a rather uniform stereom meshwork and show no evidence
of a similar stereom remolding. Compared to Archaeocidaris they also have many more interam-
bulacral plates that are each individually much smaller.
At the same time, a major change in spine morphology was taking place. Early archaeoci-
darids, such as Deneechinus, had only small, slender spines and poorly differentiated primary tu-
bercles. The spines are stouter and the primary tubercles have a distinct areole in the more derived
Lepidocidaris, but the spines remain short. Archaeocidaris is the first echinoid to have massive
spines at least as long as the test diameter, which attach to large well-developed primary tubercles.
The need to have a larger base for muscle attachment may have been the driving force behind the
switch to extended and sustained plate growth.
By the end of the Paleozoic, echinoids such as Miocidaris connorsi Kier 1965 had returned to
a plate arrangement very similar to that in the earliest echinoid Bromidechinus, with just two
columns of interambulacral plates. However, unlike Bromidechinus, individual plates in mioci-
darids grew to a much larger size and underwent modification and remolding during ontogeny.

Growth in Post-Paleozoic Echinoids

The echinoid crown group was in existence by the end of the Paleozoic, and had already split into
the Cidaroidea and the Euechinoidea (Kier 1984; Smith and Hollingworth 1990). Test growth in
crown echinoids involved a mixture of plate addition and plate growth. In cidaroids relatively few
new plates were added through life and plates remained undifferentiated. Regular euechinoids
 A

Figure 4. Growth trajectories. A, Psammechinus miliaris, a regular echinoid; B, Holectypus depressus, a stem
group irregular echinoid; C, Echinocardium cordatum, a spatangoid echinoid. Chart labels: (a), total number
of interambulacral plates in a column; (b), number of interambulacral plates from the peristome to the am-
bitus; (c), number of plates in ambulacrum III inside the internal fasciole; (d), number of pore-pairs in petal;
(e), number of plates in posterior interambulacrum; (f), number of plates in interambulacrum I to ambitus.
 Growth and Form in Echinoids • Smith 189

usually have considerably more plates and continue to add new plates throughout growth. Their
plates also generally show a well-developed seasonal banding, recording how each has enlarged by
incremental accretion. Plates migrate from a supra-ambital to a subambital position as growth
proceeds, as Seilacher (1979) observed. A typical growth pattern for this group is shown by Psam-
mechinus (Figure 4). Although plate addition slows down as maximum size is approached, it never
ceases completely and plates are continuously moving around the ambitus onto the oral surface.
Irrespective of size, approximately half the total number of plates in an interambulacral column
are always on the oral surface. Consequently, regular echinoids never develop any strong differen-
tiation between the plates of the oral and aboral surfaces.
A similar growth style occurs in the earliest and most primitive stem group irregular echi-
noids, where plate addition and plate migration onto the oral surface continue throughout life.
Loriolella (Smith and Anzalone 2000), for example, shows continuous addition of plates, with
those on the oral surface rising from six plates per column at 17 mm diameter to 12 plates at 55
mm diameter. However, in slightly more advanced irregular echinoids, migration of plates around
the ambitus effectively ceases above a certain size. Holectypus (Figure 4) starts with seven oral
plates per column at 9.6 mm diameter reaching 11 or 12 by about 25 to 30 mm in diameter. Al-
though adapical plates continue to be added and the test can almost double further in size, there
is no further migration of plates around the ambitus (see Figure 4). Thus, growth can be divided
into two phases: an early phase dominated by plate addition, with plates migrating from aboral to
oral surface; and a later phase when plates continue to be added adapically, but with no migration
of plates around the ambitus. Growth of the oral surface during this second phase is accomplished
purely by accretion to the existing plates.
Primitive irregular echinoids such as Holectypus record the beginnings of an important shift
towards early specification of oral plates, and a marked switch in emphasis from growth by plate
addition to growth by plate accretion. As a consequence, oral–aboral differentation of the plates
and their appendages became feasible. This trend was subsequently taken to extremes in two
groups, the Atelostomata and the Clypeasteroida.

Atelostomates
Spatangoids, holasteroids and their common stem group the disasteroids together make up the
clade Atelostomata. Their style of growth differs from that of regular echinoids and was carefully
documented for the spatangoid Echinocardium (see Figure 4) by Gordon (1927). She was able to
show that all of the plates that form the oral surface are laid down in position in the imago prior
to metamorphosis. Indeed, all plates up to the base of the periproct form in the posterior inter-
ambulacrum before metamorphosis is completed. Following metamorphosis the periproct starts
to migrate away from the apex and additional interambulacral plates are added between it and the
apical disc. By the time the animal has reached a length of about 5 mm petals have begun to form;
by 8 mm there is a well-formed internal fasciole and all of the adult pore pairs of the petal are pre-
sent. At this stage in development the addition of new interambulacral plates effectively ceases (see
Figure 4) and all subsequent growth outside the interior fasciole occurs solely by plate accretion.
However, not all growth ceases. Inside the inner fasciole new plates continue to be added to am-
bulacrum III as the test enlarges, which greatly increases the numbers of tube feet in this region.
These are the tube feet responsible for funnel building and food harvesting from the sedi-
ment–water interface. Most of the plates in Echinocardium are formed and already in their adult
position relative to the ambitus within a few weeks of metamorphosis, the test has more or less its
full adult complement of interambulacral plates, and all subsequent test enlargement occurs pri-
marily by plate accretion.
Other spatangoids, such as Meoma and Plagiobrissus, show a similar pattern of growth
(Chesher 1970; Kier 1975). In Meoma, the adult position and arrangement of plates outside the
peripetalous fasciole is established by the time the individual is 6 to 7 mm long and the oral
plating is established by 5 mm (and probably earlier; no information is available on younger
stages). The peripetalous fasciole appears at around 7 mm test length, after which only a very few
190 Evolving Form and Function: Fossils and Development

interambulacral plates are added. However, ambulacral plates continue to be added, significantly
increasing the length of petals and the number of plates and pore pairs that they contain.
This early specification of plating in spatangoids extends at least as far back as the Early Cre-
taceous. David (1980) described the ontogeny of Toxaster granosus and showed that the smallest
individuals of about 8 mm already have nine out of the 12 or 13 adult plates of the posterior in-
terambulacrum. Even by this size the periproct is already more or less in its adult position and sep-
arated from the apical disc by three interambulacral plates. Toxaster has no aboral fasciole, yet it
is clear that oral and aboral plating was established from a very early stage in ontogeny. There is
no information on the early postmetamorphic stages of atelostomates that originated earlier: dis-
asterids or collyritids. However, Disaster by 10 mm is exactly like the adults in its shape and plate
position. Thus, in all of these atelostomates, it seems that oral plating is fixed at metamorphosis,
that test growth is achieved by plate enlargement and that there is no migration of plates from the
aboral to the oral surface after the very initial stages of growth. Some plate addition continues
adapically in later stages of ontogeny, but affects only the relative lengths of the petaloid zones.
Early fixation of plate position in ontogeny made several evolutionary innovations possible
in the Atelostomata.
1. Because the plates that make up the test remain in basically the same position throughout
postmetamorphic growth, regions of the test can start to differentiate in function and structure.
This is most pronounced in the morphological and functional differentiation of spines and their
tubercles that develops progressively within the atelostomates. The Jurassic atelostomate stem lin-
eage shows little in the way of regional differentiation of plates and their spines, but there is a pro-
gressive differentiation and regional specialization of spines within both holasteroids and
spatangoids during the Cretaceous and Tertiary. By the Eocene modern levels of spine differenti-
ation and regionalization had been achieved. In this case it would appear that spine differentia-
tion followed and was made possible by plate fixation.
2. Fascioles are bands of specialized spines that generate water currents and a mucous sheath,
and which enable spatangoids to burrow into fine sediments. Their positions on the test are ob-
viously critical from a functional point of view and ideally must not shift during growth. Yet they
form on specific plates early in ontogeny and do not migrate or undergo remodelling (Kier 1975;
Smith and Stockley 2005). Consequently, the evolution of fascioles only became feasible when the
position of plates making up the test became more or less invariant through ontogeny. Within
clades individual fasciole pathways have tended to switch onto earlier and earlier forming plates
during evolution, as the oral surface has become composed of fewer and fewer plates (Smith and
Stockley 2005). The earliest fasciole appears in a late stem group atelostomate, and fascioles have
played a major role in allowing spatangoids and holasteroids to diversify ecologically.
3. With growth achieved almost exclusively by plate accretion, differential growth of indi-
vidual plates becomes the major factor driving diversity in form. Plates in specific regions can ex-
pand at faster rates to make up a proportionately larger area of the test, as for example in the
expansion of the sternal plates of the spatangoid plastron. Expanding individual plates in different
directions at different rates allows divergence from the spherical body plan and enabled irregular
echinoids to adopt a wide range of test shapes.

Clypeasteroids
The early development of sand dollars was first documented by Agassiz (1872–74) and later de-
scribed in great detail by Gordon (1929). In Echinarachnius the test at 2 mm, immediately post-
metamorphosis, is subglobular like that of a regular echinoid. By the time it reaches 3 mm it has
laid down its full complement of oral plates, after which flattening of the test takes place. By 5 mm
most of the adult interambulacral plates have formed and are in their final position. As in most
spatangoids, ambulacral plates continue to be added adapically in later growth, thereby enlarging
the petals. Development in Encope and Mellita is even more extreme, with all plates up to the base
of the petals formed and the test already flattened by the time it reaches 2 mm. Again, subsequent
growth is almost entirely by plate accretion with only minimal addition of plates in interambula-
 Growth and Form in Echinoids • Smith 191

cral zones and to petals. The presence of a single large interambulacral plate in laganinids suggests
that interambulacral plate addition ceased at a comparable stage, although there is no direct ob-
servational evidence.
The shift of plate formation largely to the initial stages of ontogeny must have occurred early
in clypeasteroid history, since it is common to both major clades of the crown group (the Clypeas-
terina and Scutellina). The Oligopygidae represent the immediate extinct sister group to clypeas-
teroids. A growth series of Oligopygus kugleri shows that there is some migration of
interambulacral plates around the ambitus, because the periproct shifts progressively adorally in
larger individuals. However, an individual 1.6 mm in length already has 10 plates per column in
the posterior interambulacrum, and an individual 3.2 mm long has 11 plates. By 4.3 mm the first
six pore pairs of the petal are developed and there are 12 interambulacral plates. In a fully grown
adult of 25 mm there are 16 plates so, as in Echinarachnius, the bulk of the interambulacral plates
are established and in their adult position before reaching a 5 mm test diameter. Cassiduloids lie
further down the stem group leading to clypeasteroids, but unfortunately their skeletal ontogeny
remains unstudied. The growth of Echinoneus (Westergren 1911) seems much closer to Holec-
typus than to Oligopygus and the clypeasteroids. Less than half of the adult interambulacral plates
are present by 6 mm, and there is continued migration of plates around the ambitus during
growth. In flatter cassiduloids with a well-developed ambitus such as Clypeus, the number of oral
plates remains relatively static during later growth while aboral plates continue to be added, as in
Holectypus. Kier (1974) noted that there was a trend within cassiduloids for a decrease in the
number of plates through time, and this may reflect a general trend towards fewer and earlier
formed plates.
The line leading to modern clypeasteroids therefore independently evolved a growth strategy
similar to that of atelostomates, in which most of the adult plates were laid down, and in their
adult position, extremely early in ontogeny. Immediately postmetamorphosis clypeasteroids have
all the interambulacral plates up to the petals. Subsequent plates are added adapically, so that the
petals increase in length and pore pair number, but oral and supra-ambital plates are fixed in rel-
ative position almost from the start. As in atelostomates, this fixed plate architecture allowed
clypeasteroids to evolve regionally differentiated spine canopies and to diverge from a basically
globular test shape. However, clypeasteroids evolved two additional and unique innovations: (1)
internal buttressing, binding plates on the upper surface to those on the lower surface, thereby
strengthening the test (Seilacher 1979); and (2) lunules, perforations that pass right through the
test, which increase the stability of the test in currents (Telford 1981), increase the area over which
food can be collected and transported to the mouth (Smith and Ghiold 1982), or both. Although
these structures always appear in the same positions on the test, they form in different ways and
have evolved independently in different clades (Seilacher 1979).
Both innovations became possible only once the plates on the upper and lower surfaces be-
came fixed in position relative to one another through ontogeny. In the more primitive clypeast-
eroids there are no lunules and buttressing is relatively simple, restricted to the marginal zone. In
these forms plate addition still causes some shifting of position of the more adapical plates rela-
tive to the more adoral plates. However, in sand dollars, where almost all interambulacral plates
are formed right at the start of ontogeny, internal buttressing can extend well into the petal zone.
Once upper and lower surfaces are connected by solid calcite walls, lunules can be created easily
by resorption or differential plate growth (Seilacher 1979).

Discussion

How echinoids grow, whether by adding new plates, or enlarging existing plates, has played a key
role in determining evolutionary trends, and has directly influenced the form that morphological
disparity has taken over time (Figure 5). Paleozoic echinoids are notable for the variation that they
display in numbers of ambulacral and interambulacral columns, although in terms of overall
shape they all remain relatively conservative in form. Paleozoic echinoids were not able to enlarge
Figure 5. Summary cladogram of echinoid evolution. The Mesozoic to Recent crown group echinoids all
have tests constructed of 20 columns of plates (alternately two ambulacral and two interambulacral), but
show great variation in shape. Members of the Paleozoic stem group all have a similar spheroidal or oblate
spheroidal shape, but the tests are constructed of a variable number of ambulacral and interambulacral plate
columns. There has been a marked shift in growth strategy through time, from growth primarily by plate ad-
dition to growth primarily by plate accretion.
 Growth and Form in Echinoids • Smith 193

and modify their plates to any great extent after an initial growth phase, and so they were restricted
to growing in width by adding more columns of plates. Some achieved this by adding interam-
bulacral columns, others by adding ambulacral columns, and still others by adding both.
A breakthrough came in the late Devonian to Carboniferous archaeocidarids when a signifi-
cant switch took place from growth by plate addition to growth by plate accretion, possibly be-
cause of the need to support ever larger spines in the arms escalation against predators. Growth
became an interplay between plate addition at the apex, and accretion and remoulding of the ex-
isting plates throughout life. No longer was it necessary to add new columns of plates as the test
enlarged to fill space: the plates themselves could be periodically enlarged and the test composed
of just a small number of columns.
This mode of growth was inherited by all crown-group echinoids and, as a result, post-Pale-
ozoic echinoids have evolved several quite different morphologies within a very restricted test-
plating “bauplan.” This change in growth strategy, by itself, was not enough to lead to extensive
morphological differentiation. Cidaroids, which retain an identical growth strategy to the Per-
mian miocidarids, are among the most highly conserved echinoids in terms of their skeletal mor-
phology. Increasing skeletal complexity and differentiation only became possible when growth by
plate accretion became dominant over plate addition and the adult position of individual plates
became fixed at an extremely early developmental stage. The catalyst for this change seems to have
been the need to develop oral–aboral functional differentiation of spines and tube feet in infaunal
echinoids. Whereas growth in regular echinoids involves the continuous addition of new plates
and their migration from aboral to oral surface, early specification of oral, ambital and supra-am-
bital plates in ontogeny allowed irregular echinoids to develop regional patterns of spination that
were fixed in position throughout life. With the switch to plate accretion as the predominant
means of test enlargement, differential growth of individual plates became feasible and provided
a mechanism for shape change.
In an important paper, Eble (2000) examined the evolution of morphological disparity in
spatangoids and holasteroids using landmark-based morphometrics for the first time. He parti-
tioned disparity into plastronal (that is, oral) and nonplastronal (that is, aboral) components, and
showed that the two followed different trajectories over time. Whereas disparity of the plastron
features increased steadily during the Jurassic and Cretaceous, disparity of the upper surface
peaked early and then plateaued. Eble distinguished plastronal features as being more develop-
mentally entrenched and less functionally important than aboral features. However, the evidence
of growth patterns documented here suggests a more important difference: oral plating is already
laid down by the end of metamorphosis and landmark points evolve only through differential
growth of individual plates, whereas the position of aboral landmarks (such as petal length and
the position of the apical disc) are affected by plate addition during the later stages of ontogeny.
Eble’s results (2000) seem to show that growth by plate elaboration (accretionary growth) pro-
vides a greater opportunity for morphological innovation, whereas modifications that involve
greater or lesser amounts of adapical plate addition quickly lead to saturation of morphospace.
The diversity of form in today’s irregular echinoids has arisen largely because the rules by
which growth is specified have become more complex. The evolution of echinoids can be seen as
a transformation from a simple modular growth of many identical elements to a highly differen-
tiated pattern of growth in which individual plates of the test each have their own specific devel-
opmental pattern, growing at different rates and in different directions. In terms of diversity, early
specification of plates in ontogeny has been a highly successful strategy: 40% of extant echinoids
today have the bulk of their interambulacral plates formed and in adult position within a few
weeks of metamorphosis.
While nothing is known as yet about the genetic specification of growth in echinoids, it is
clear that it has increased in complexity through the Phanerozoic. The ability to remodel signifi-
cantly and to grow individual plates evolved only some 350 million years ago, and a highly speci-
fied pattern of growth in sea urchins emerged only some 100 million years ago. Both were
profoundly significant in the evolution of morphological diversity.
194 Evolving Form and Function: Fossils and Development

Acknowledgments.

I should like to acknowledge the contribution of Dolf Seilacher, whose paper on the construc-
tional morphology of sand dollars set me thinking about the evolution of echinoid growth strate-
gies through the Phanerozoic. I am indebted to Derek Briggs, Steve Donovan, Charlotte Jeffery
and Jim Sprinkle for their helpful reviews and constructive criticisms of an earlier version of this
paper.
 Growth and Form in Echinoids • Smith
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