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Geol. Mag. 144 (2), 2007, pp. 333–359.
c
!
2007 Cambridge University Press 333
doi:10.1017/S0016756806003001 First published online 19 December 2006 Printed in the United Kingdom
Phylogeny and origin of Jurassic irregular echinoids
(Echinodermata: Echinoidea)
TH OM AS SAUC
`
ED E
∗
§, RICH M OO I‡ & BRUNO DAV ID
∗
∗
UMR CNRS 5561 Biog
´
eosciences, Universit
´
e de Bourgogne, 6 bd Gabriel, F-21000 Dijon, France
‡California Academy of Sciences, San Francisco, California, USA
(Received 26 September 2005; accepted 17 May 2006)
Abstract – A phylogenetic analysis of Jurassic irregular echinoids is realized to explore the origin
and early evolution of this important subset of echinoids. The phylogeny is based on 39 characters
and considers data from apical system architecture, the corona including tuberculation and spines,
Aristotle’s lantern, and general test shape. Results corroborate the monophyly of Irregularia, and
clarify the phylogenetic interrelationships existing between the main groups of irregular echinoids.
Specializations of the Aristotle’s lantern, spines, tubercles and phyllodes constitute the apomorphies
for different taxa, as for the whole of Irregularia. The phylogenetic signal yielded by these
characters highlights the importance of the environmental context of the origin and diversification
of irregular echinoids. The definition of ‘irregularity’ is re-examined, rejecting exocyclism and
characters of the apical system as appropriate synapomorphies, and stressing the importance of
other characters, particularly the high density and small size of tubercles and spines. A new
clade name, Infraclypeidae [P], and phylocode designations (stem-based diagnoses) are proposed
for the clades Irregularia, Eognathostomata, Microstomata, Neognathostomata and Atelostomata.
Other groupings formerly used (Pygasteroida, Galeropygidae and Menopygidae) are considered
paraphyletic.
Keywords: Irregularia, Echinoidea, phylogeny, systematics, Jurassic.
1. Introduction
1.a. Irregular echinoids
The mass extinction that took place at the end of
the Permian deeply affected echinoid diversity. Only
two lineages survived the event (Kier, 1965, 1968,
1974, 1977, 1984; Fell, 1966; Smith, 1984; Smith
& Hollingworth, 1990). Once past the ‘Palaeozoic’
crisis, echinoid diversity recovered through significant
evolutionary radiation and rapid morphological diver-
sification (Kier, 1974, 1982; Smith, 1978b, 1984). The
echinoids therefore played a much more prominent
role in Mesozoic echinoderm diversity than they
did previously (Erwin, 1993). Diversity increased
from the Early Jurassic (Sprinkle, 1983) with the
appearance of a large and important g roup of echinoids:
the irregular sea urchins, recognized as the clade
Irregularia Latreille, 1825 (Kier, 1977, 1982; Smith,
1984, 1988). This clade includes forms as diverse
as the present-day lamp urchins, heart urchins and
sand dollars, and constitutes nearly 60 % of extant
and extinct species of echinoids (calculated after
Kier, 1974). The appearance of irregular sea urchins
thus contributes greatly to the general recovery and
expansion of echinoid diversity that occurs within the
global context of the ‘Mesozoic Marine Revolution’
(MacLeod, 2003; Vermeij, 1977, 1995).
§Author for correspondence: thomas.saucede@u-bourgogne.fr
The establishment of an anterior–posterior axis
of secondary bilateral symmetry in the otherwise
pentaradial tests of the Irregularia distinguishes them
from the other globose sea urchins (sometimes referred
to as ‘regular’ urchins), and places the radiation of
irregular sea urchins among the most significant events
in the evolution of echinoids. The establishment of
secondary bilateral symmetry is associated with the
migration of the periproct (the area which surrounds
the anus) from the summit of the test toward the
posterior margin. This migration accompanies other
morphological innovations such as the anteriorly placed
mouth, the single-direction locomotory systems with
spines specialized to produce an efficient power-
stroke, the sophisticated particle-picking mechanism
that provides continuous access to fresh and abundant
supplies of food, and the miniaturization of almost all
external appendages such as spines and podia. All these
morphological innovations are strongly linked with
the colonization and the adaptation to new ecological
niches, determined by the nature of the sea bottom
where ir regular sea urchins live. Ir regular echinoids
are exclusively microphagous species that can only
ingest small nutrient-bearing particles (De Ridder &
Lawrence, 1982). This feeding behaviour implies a
specialization of the body form and appendages for
feeding and moving upon or inside soft sediments (Kier,
1974; Smith, 1981; Kanazawa, 1992; Telford & Mooi,
1996).
334 T. SAUC
`
EDE , R. M OO I & B. DAVI D
Figure 1. According to the Extraxial–Axial Theory, the echinoid test is constructed almost entirely from axial elements organized into
five growth zones. In regular echinoids, the periproct is enclosed within the apical system, a composite structure that gathers ocular
(axial elements) and genital (extraxial elements) plates that surround the periproct (extraxial elements) (a, from David & Mooi, 1999).
Conversely, in irregular echinoids, the migration of the periproct leads to a breaking of the extraxial region into two distinct units: the
genital plates that stay in an apical position, and the periproct that move towards the margin of the test (b).
David & Mooi (1996) have proposed a new system
for interpretation of the body wall components among
echinoderms (David & Mooi, 1998, 1999; David, Mooi
& Telford, 1995; Mooi & David, 1997, 1998). This new
system (the Extraxial-Axial Theory, or EAT) bases the
recognition of homologies on the embryology and the
ontogeny of structures (David & Mooi, 1996, 1998;
Mooi, David & Marchand, 1994). It identifies two
major body wall categories in the Echinodermata:
axial and extraxial. The identification of these two
distinct body wall regions permitted the establishment
of new homologies pertaining to all echinoderms. In
some cases, it also led inexorably to drastic challenges
of previous phylogenetic hypotheses (David & Mooi,
2000; Mooi & David, 1998).
Echinoids are unique among the echinoderms
because the entire coronal part of the test consists of
axial body wall (Mooi, David & Marchand, 1994). The
extraxial region is restricted and indeed constricted to
the scales present on the periproctal membrane and
to the genital plates (Fig. 1). The axial region of the
corona is organized into five growth zones that form
and continue to grow in accordance with the ‘Ocular
Plate Rule’ (OPR). Following this mechanism, each
growth zone is closely associated with an ocular plate
and consists of an ambulacrum surrounded by two half-
interambulacra, one on each side of the ambulacrum.
New ambulacral and interambulacral plates are formed
next to the ocular plate. Plates are shifted away from
the apical system and the ocular plate as new plates are
added at the edge of the oculars between the oculars
and the rest of the plate column.
The apical system is a composite structure that
associates ocular (axial element) and genital (extraxial
element) plates that surround the periproct (extraxial)
in ‘regular’ echinoids (Fig. 1a). In irregular echinoids,
the migration of the periproct leads to a ‘breaking’
of the apical system as the periproct moves out of
the circle formed by the genital and ocular plates.
This phenomenon is called exocyclism. Exocyclism
entails a disruption of the echinoid’s small remaining
extraxial region into two distinct units: (1) genital plates
that remain in the apical position; (2) the periproct
and its associated scales that move toward the margin
(and in some cases all the way to the oral surface)
of the test (Fig. 1b). Therefore, the diversification of
irregular echinoids is associated with exocyclism that
corresponds to a disruption of the extraxial part of the
body into two separate areas.
1.b. Previous works and systematics
According to Melville & Durham (1966), irregular
echinoids constitute a morphological (and not taxo-
nomic) group or grade that can be distinguished from
‘regular’ forms by the position of the periproct outside
the apical system (exocyclism), by the predominance of
bilateral symmetry in test outlines, and by the absence
of the Aristotle’s lantern in many of them. Variation
in expression of test outline and the Aristotle’s lantern
implies that these characters cannot constitute absolute
criteria for establishment of a natural group of irregular
echinoids. In addition, Durham & Wagner (1966) use
the ter ms ‘irregular’ and ‘exocyclic’ as synonyms.
These terms refer to tests with the periproct located
outside the apical system and supposedly contrast with
‘regular’ and ‘endocyclic’ which refer to tests with
the periproct located within the apical system. Finally,
Phylogeny and origin of Jurassic irregular echinoids 335
irregular, or exocyclic, groupings are recognized to
be polyphyletic, the subclass rank of the group is
abandoned, and ‘irregular echinoid’ is retained only
as an informal division (Melville & Durham, 1966).
At the same time, Jesionek-Szymanska (1959)
and Mintz (L. W. Mintz, unpub. Ph.D. thesis, Univ.
California Berkeley, 1966) showed that the boundary
between regularity and irregularity is not so definite.
The morphological changes from the regular to
the irregular condition occurred in stages, so that
many Jurassic irregular echinoids display intermediate
morphologies between regularity and fully manifested
irregularity (Jesionek-Szymanska, 1963; Mintz, 1968).
Therefore, according to these authors, some Jurassic
irregular echinoids are still endocyclic (the periproct
is located within the apical system), and exocyclism
and irregularity are not good synonyms. If we consider
restriction of the concept of irregularity (exocyclism in
which the periproct moves significantly away from the
centre of the apical system so that it eventually loses
contact with it) to the clade that we now consider the
Irregularia, we are still left with evidence suggesting
that some form of exocyclism (that is, at least some
movement of the periproct away from the center of the
apical system in the direction of interambulacrum 5)
occurred at least seven times in independent lineages
of ‘regular’ echinoids (Sauc
`
ede, Mooi & David, 2003).
Consequently, exocyclism is not a sufficient criterion
to define irregularity. Repeated movements of the
periproct toward and into interambulacrum 5 could
be seen as supporting the plural origin of irregular
echinoids, as suggested by Melville & Durham (1966).
As a morphological character of irregular echinoids,
exocyclism was given great taxonomic weight in the
19th and the beginning of the 20th century, but the ques-
tion of the origin of the group, whether unique or plural,
was not necessarily tackled. Some authors considered
exocyclism to be of major taxonomic importance and
placed irregular echinoids in a unique category (Desor,
1855–1858; Wright, 1855–1860; Zittel, 1876–1880;
Gregory, 1900). For others, the presence or absence of
the Aristotle’s lantern was of paramount importance,
and echinoids were divided accordingly into those
that lack a lantern (the atelostomes) and those that
possess one (the gnathostomes). Even in cases when
irregular echinoids were recognized, they were split
within two distinct groups according to the presence
or absence of the Aristotle’s lantern (Pomel, 1869,
1883; Lambert & Thi
´
ery, 1909–1925). Finally, certain
authors (e.g. Duncan, 1889) did not make a distinction
between regular and irregular forms, and species that
we now recognize as irregular taxa were scattered
among widely disparate groups.
The position favouring the plural origin of irregular
echinoids prevailed for most authors of the 20th
century. Hawkins (1922) was the first to tackle the
question of the origin of irregular echinoids. He
derived them from ‘regular’ echinoids through two
independent lineages and two possible ancestors: (1)
the Microstomata (sensu Smith, 1984) through the
genus Pseudopygaster Hawkins, 1922 (= Loriolella
Fucini, 1904) on the one hand, and (2) the Eo-
gnathostomata (sensu Smith, 1981) through the genus
Plesiechinus Pomel, 1883 on the other hand.
Mortensen (1948) proposed independent origins for
the two families composing the Eognathostomata: the
Pygasteridae Lambert, 1899 and the Holectypidae
Lambert, 1899. His assumption relied on the absence
of tubercle crenulation in certain species of Pygas-
teridae (as in the ‘regular’ Pedinidae Pomel, 1883),
contrasting this condition with the crenulate tubercles
of Holectypidae (as in the ‘regular’ Diadematidae
Gray, 1855). However, he maintained both families,
Holectypidae and Pygasteridae, in the same order, and
all irregular echinoids in a unique subclass. Later,
Jesionek-Szymanska (1970) and Rose & Olver (1984)
showed that Pygasteridae have primitive crenulate
tubercles, and that crenulation tends to disappear in
derived species of Pygaster Agassiz, 1836.
In spite of this, the hypothesis of irregular polyphyly
has especially been supported by studies of the
Aristotle’s lantern. These studies followed initial work
by Jackson (1912), and the first observations on the
Aristotle’s lantern and associated structures in irregular
echinoids were published on the Eognathostomata
(Hawkins, 1934). Durham & Melville (1957) used lan-
tern and tooth morphology to derive irregular echinoids
from aulodont and stirodont regular ancestors through
three distinct lineages: (1) the Pygasteroida Durham
& Melville, 1957, (2) the Gnathostomata Zittel, 1879
(holectypoids and clypeasteroids) and (3) the Ate-
lostomata Zittel, 1879. They concluded that the group
Irregularia is polyphyletic and should be abandoned, a
position which prevailed in the widely followed Treat-
ise on Invertebrate Palaeontology (Durham, 1966).
The independence of pygasteroids and holectypoids
was also supported by Melville’s work (1961) on
tooth shape. He compared the apparent triangular
shape of teeth in the genus Pygaster (pygasteroid)
to the keeled teeth of the genus Holectypus Desor,
1842 (holectypoid). Consequently, he derived the
pygasteroids from regular aulodont echinoids (the
Pedinidae), and all other irregular echinoids from
stirodonts. Mintz (L. W. Mintz, unpub. Ph.D. thesis,
Univ. California Berkeley, 1966) derived pygasteroids
from among the Pedinidae, and proposed a stirodont
ancestor for the Microstomata in which the lantern
is absent (Mintz, 1968). Hess (1971) also classified
the keeled teeth of Holectypus as of stirodont affinity,
but Philip (1965) suggested an aulodont origin for the
lantern of holectypoids, which he derived from the
Diadematidae. However, Philip (1965) did not give
an opinion on the origin of other irregular echinoids.
M
¨
arkel (1978) presented independent origins for the
three irregular orders that possess a lantern, namely: the
Cassiduloida Claus, 1880, the Holectypoida Duncan,
336 T. SAUC
`
EDE , R. M OO I & B. DAVI D
1889, and the Clypeasteroida Agassiz, 1872. Jensen
(1981), founding her position on the study of teeth
microstructure and ambulacral composition, grouped
the orders Pygasteroida and Pedinoida Mortensen,
1939 (aulodont regular echinoids) into the superorder
Pedinaceae. She made this the sister group of all
other irregular echinoids, which then constitute a
monophyletic assemblage.
The hypothesis of the polyphyletic origin of irregular
echinoids was first challenged by Kier (1974), who
showed that the morphology of the lanter n and teeth
is similar in the genera Pygaster and Holectypus,
but he did not draw any conclusions about their
origin. Smith (1981) showed that all irregular echinoids
possess the same type of lantern with diamond-
shaped teeth, a type already present in a ‘regular’
species (Eodiadema aff. minutum (Buckman, 1845)
in Strickland & Buckman, 1845) which was in turn
related to aulodont echinoids. He also considered the
genera Pygaster and Holectypus to be closely related
and to constitute the sister group of all other Irregularia.
Smith’s view has been followed by successive authors
(Rose, 1982; Rose & Olver, 1988; Anzalone, Teruzzi
& Smith, 1999; Smith & Anzalone, 2000; Solovjev &
Markov, 2004).
Basically, all previous works on the origin of irregu-
lar echinoids rely on the study of the four following
characters: (1) the position of the periproct with
respect to the apical system; (2) the Aristotle’s lantern;
(3) tubercle crenulation; and (4) the organization of
ambulacral plates. Depending on each author and
their views of a character’s relative importance, these
characters have fomented arguments both for and
against the unique origin (that is, the monophyly)
of irregular echinoids. However, Kier’s (1974) and
Smith’s (1981, 1982) findings that the irregulars are
monophyletic based on lantern morphology are seldom
questioned.
Even if the monophyly of Irregularia is no longer
challenged, a broader definition of irregularity taking
into account all of the above-mentioned features
is needed. In addition, phylogenetic relationships
among irregular taxa as well as the relationship with
regular echinoids remain imprecise. Clarification of
phylogenetic relationships is an essential stage of
understanding the processes by which irregularity is
achieved. Through this understanding, a much better
picture will develop of the most important radiation of
post-’Palaeozoic’ echinoids.
2. Materials and methods
2.a. Taxon selection
Fossil taxa are of extreme interest when trying to
resolve phylogenies because they bear mor phological
information of phylogenetic significance that is often
absent in extant taxa (Benton, Wills & Hitchin, 2000;
Wagner, 2000; Smith, 2001). Moreover, extant taxa
are sometimes so different morphologically, when
evolution has been rapid enough to accumulate large
numbers of apomorphies along a given lineage,
that comparisons only among extant forms can
be misleading. Uncovering phylogenies necessitates
the study of intermediate morphologies, and these are
often inherent in the fossil record (Rieppel, 1994).
In the Lower Jurassic, the very earliest irregular
echinoids, such as ‘Plesiechinus’ hawkinsi Jesionek-
Szymanska, 1970 (Sinemurian of Nevada) and
Loriolella ludovicii Meneghini, 1867 (Pliensbachian
of Italy), still display the pattern observed in regular
echinoids, namely a periproct enclosed by the genital
and ocular plates (Jesionek-Szymanska, 1970; Smith
& Anzalone, 2000). However, the periproct becomes
displaced from the centre of the apical system (becomes
more eccentric) during growth and tends to ‘stretch’
the genital plate in interambulacrum 5 and adjacent
ambulacral oculars of the apical system in which the
periproct is enclosed. By definition, these genital and
ocular plates become posterior elements of the apical
system. In later forms, such ‘stretching’ culminates
in disruption of the ring of apical plates and actual
migration of the periproct away from the apical system.
This trend appears to be progressive over a large span
of time ranging from Early Jurassic to Late Jurassic
times, and exocyclism therefore appears to have been
achieved gradually in irregular echinoids (Jesionek-
Szymanska, 1963; L. W. Mintz, unpub. Ph.D. thesis,
Univ. Califor nia Berkeley, 1966). By contrast, in Recent
irregular echinoids, periproct migration begins during
early ontogeny before the closure of the apical system,
and posterior plates show little or no evidence of
elongation (Gordon, 1926). Therefore, apical structures
of the first irregulars are very informative; they display
the intermediate patterns lacking even in the early
ontogeny of extant forms, and are therefore essential
to the comprehension of the processes of periproct
migration, and to determine if these processes are
homologous in all irregulars.
Homoplasy in morphological characters is a
common feature of invertebrate phylogenies (Moore
& Willmer, 1997; Wills, 1998). They sometimes
constitute evidence for the adaptation of species to
similar habits and habitats (Stewart, 1993; Suter, 1994).
At other times, they are evidence that hypotheses of
homology among the characters in question require
reassessment. Phylogenies of echinoids are no excep-
tion, and parallel evolution in apical structure has
been stressed by several authors (Jesionek-Szymanska,
1963; L. W. Mintz, unpub. Ph.D. thesis, Univ. California
Berkeley, 1966; Kier, 1974; Sauc
`
ede, Mooi & David,
2003; Solovjev & Markov, 2004), and more generally
for numerous traits within the Cassiduloida (Kier, 1962,
1966; Suter, 1994; Smith, 2001; Wilkinson, Suter &
Shires, 1996). The probability of homoplasy increases
if too many fossil taxa are selected over too long
Phylogeny and origin of Jurassic irregular echinoids 337
Table 1. List of species used for character coding
Taxon Stratigraphic range Collection
Caenocidaris cucumifera (Agassiz, 1840) Upper Toarcian–Upper Bajocian Gras, Sauc
`
ede
Acrosalenia hemicidaroides Wright, 1851 Bajocian–Lower Callovian Sauc
`
ede
Farquharsonia crenulata Kier, 1972 Bathonian
Diademopsis bowerbankii Wright, 1851 Hettangian–Sinemurian
Eodiadema minutum (Buckman, 1845) in Strickland
& Buckman, 1845
Upper Sinemurian–Lower Pliensbachian
Atlasaster jeanneti Lambert, 1937 Sinemurian Collignon
‘Plesiechinus’ hawkinsi Jesionek-Szymanska, 1970 Upper Sinemurian
Plesiechinus ornatus (Buckman, 1845) in Strickland
& Buckman, 1845
Aalenian–Bajocian Clavel, Lambert, UB
Pygaster gresslyi Desor, 1842 Middle Oxfordian–Upper Tithonian Clavel, Cotteau, Courville, UB, Lambert
Pileus hemisphaericus Desor, 1856 Oxfordian Lambert, Votat
Holectypus depressus (Leske, 1778) Bathonian–Callovian CAS, Cassel, UB, Votat
Loriolella ludovicii (Meneghini, 1867) Lower Domerian
Eogaleropygus microstoma (Lambert, 1933) Middle Toarcian
Galeropygus agariciformis (Wright, 1851) Upper Toarcian–Bathonian UB, UCMP
Hyboclypus caudatus Wright, 1851 Bajocian–Bathonian Courville, Dailly, Dudicourt, UB
Centropygus petitclerci Lambert, 1901 Upper Aalenian Clavel
Clypeus plotii Leske, 1778 Upper Bajocian–Lower Callovian CAS, Courville, Dudicourt, Mooi, UCMP
Pygurus depressus Agassiz in Agassiz & Desor, 1847 Bathonian–Upper Callovian Collignon
Nucleolites clunicularis (Phillips, 1829) Bathonian–Lower Callovian Courville; UCMP
Pseudosorella orbignyana Cotteau, 1855 Middle Oxfordian–Lower Tithonian Lambert
Menopygus nodoti (Cotteau, 1859) Bathonian Clavel, Collignon, Cotteau, Dudicourt
Pyrinodia guerangeri (Cotteau, 1862) Bajocian
Infraclypeus thalebensis Gauthier, 1875 in Cotteau,
P
´
eron & Gauthier, 1873–1891
Tithonian Courville, Enay, Clavel
Desorella elata (Desor, 1847) in Agassiz & Desor, 1847 Upper Oxfordian Lambert
Pachyclypus semiglobus (M
¨
unster, 1829) in Goldfuss,
1826–1844
Lower Kimmeridgian Lory
Orbigniana ebrayi (Cotteau, 1874) Upper Bajocian Clavel, Lambert
Pygorhytis ringens (Agassiz, 1839) Upper Bajocian–Middle Callovian UCMP, UP
Cyclolampas kiliani (Lambert, 1909) Upper Bajocian Fournier
Pygomalus ovalis (Leske, 1778) Upper Bajocian–Middle Bathonian Thierry
Collyrites elliptica (Lamarck, 1791) in Brugui
`
ere, 1816 Upper Bathonian–Upper Callovian Gras, UB
Disaster moeschi Desor, 1858 Callovian
Metaporinus sarthacensis Cotteau, 1860 Upper Bathonian–Middle Callovian Votat
Tithonia praeconvexa Jesionek-Szymanska, 1963 Upper Callovian Clavel, UCMP
Location of consulted collections: Caillet – Claude Bernard University, Lyon; Collignon – Bourgogne University, Dijon; Cotteau – Claude
Bernard University, Lyon; Courville – University of Rennes; Dailly – Claude Bernard University, Lyon; Dudicourt – University of Rennes;
Enay – Claude Bernard University, Lyon; Fournier – Joseph Fourier University, Grenoble; Gras – Museum of Grenoble; Lambert – Museum
National d’Histoire Naturelle (MNHN), Paris; Lory – Museum of Grenoble; Sauc
`
ede – Joseph Fourier University, Grenoble; Thierry –
Bourgogne University, Dijon; Votat – University of Rennes; CAS – California Academy of Sciences, San Francisco; UB – Bourgogne
University, Dijon; UCMP – University of California Museum of Paleontology, Berkeley; UP – University of Poitiers.
an inter val of time (Sanderson & Donoghue, 1989;
Suter, 1994; Smith, 2001) or if the selected terminal
taxa are too distant from the origination time of the
group. These problems foster the phenomena of long
branch attraction and character exhaustion (Wagner,
1995, 2000). The alternative is a careful selection of
taxa relevant to the question and from key time intervals
(Stewart, 1993; Smith, 2001).
Taxa used in the present study were chosen
exclusively from the Jurassic. In fact, they originate
as close as possible to the lowermost Jurassic, the
supposed earliest occurrence of irregular echinoids.
Therefore, representatives of the orders Spatangoida
Claus, 1876, Holasteroida Durham & Melville, 1957
(sensu Smith, 1984), Clypeasteroida, Oligopygoida
Kier, 1967 and Neolampadoida Philip, 1963 were not
considered in the analysis, as they originated in the
Early Cretaceous and the Palaeogene (Kier, 1962, 1974;
Smith, 1984, 2004; Eble, 1998, 2000; Mooi, 1990;
Jeffery, 2001; Villier et al. 2004). In a recent study
(Barras, in press), certain Jurassic irregular echinoids
are included within the orders Spatangoida and Holas-
teroida. Pending further investigations, we will follow
herein the definition of these orders as formulated by
Smith (1984).
Taking into account the taxonomic level of the
analysis, we selected 33 species representative of 32
genera covering the morphological range expressed
during the Jurassic part of the radiation (Table 1). The
selection was performed according to availability of
material, quality of preservation (with the intention of
minimizing missing data), and stability of taxonomic
nomenclature. Poorly known genera or those judged to
be so similar as to be almost synonymous with other
genera were not included.
To resolve the origin of irregular echinoids and to
test their monophyly, four species have been selected
among ‘regular’ echinoids to represent the possible
stem groups of irregular echinoids as suggested by
previous authors. Diademopsis bowerbankii Wright,
338 T. SAUC
`
EDE , R. M OO I & B. DAVI D
Table 2. Data matrix
Characters 1 /6 /11 /16 /21 /26 /31 /36
Caenocidaris cucumifera 00000 00000 00000 00000 00020 01000 00010 0000
Acrosalenia hemicidaroides 00010 00100 01000 00210 00000 00000 00010 2000
Farquharsonia crenulata 00010 00000 01000 00200 00000 00000 000?0 1000
Diademopsis bowerbankii ??0?0 00?00 0?000 00100 00000 00010 10000 1000
Eodiadema minutum ??0?0 00?00 00000 00100 00000 00000 00000 3100
Atlasaster jeanneti 00010 00000 01000 00110 00000 00010 100?0 ??00
‘Plesiechinus’ hawkinsi 11010 00?00 01010 00101 00000 00120 001?0 3101
Plesiechinus ornatus 11021 00011 01010 10300 00000 00120 01110 3101
Pygaster gresslyi 11021 00011 03010 10301 00000 00120 01110 3102
Pileus hemisphaericus 10021 00011 13010 10301 00000 00220 111?0 3100
Holectypus depressus 10021 00011 13012 00301 00000 00120 01100 3101
Loriolella ludovicii ?10?? 00??0 01010 11000 10011 01100 00001 ??01
Eogaleropygus microstoma ?101? 00??0 01000 10011 1002? 00221 ??1?1 3111
Galeropygus agariciformis 01011 00110 01000 21011 1011? 10221 02101 3112
Hyboclypus caudatus 01011 00110 01000 21011 10022 10221 02101 3121
Centropygus petitclerci 11111 00111 02000 21012 1012? 10221 02101 3101
Clypeus plotii 11111 00001 03000 21012 1012? 10221 02101 3102
Pygurus depressus 10121 00001 13002 11012 10122 10221 02101 3102
Nucleolites clunicularis 11111 02011 13000 21022 1012? 10221 02101 3121
Pseudosorella orbignyana 11121 00001 13000 21022 1012? 00221 02101 3111
Menopygus nodoti 01011 00110 01000 20000 00012 00221 021?1 ??01
Pyrinodia guerangeri 000?1 00111 13000 0?000 000?? 00221 0?1?1 ??21
Infraclypeus thalebensis 000?1 01111 12002 11001 00121 00221 021?1 ??01
Desorella elata 000?1 01111 12001 11000 00111 00221 0?1?1 ??21
Pachyclypus semiglobus 000?1 00011 13001 0?00? 00??? 00221 021?1 ??21
Orbignyana ebrayi 01011 10110 02100 21010 1002? 10221 02101 ??21
Pygorhytis ringens 01111 00100 02101 11011 10021 10221 02101 ??21
Cyclolampas kiliani 01111 20100 02101 01010 1002? 11221 02101 ??22
Pygomalus ovalis 11111 20010 02100 10020 10022 10221 02101 ??20
Collyrites elliptica 11111 21011 12101 01021 11022 10221 02101 ??21
Disaster moeschi 11111 00000 03101 00000 1102? 11221 02101 ??21
Metaporinus sarthacensis 10111 00001 12101 00021 1102? 10221 02101 ??20
Tithonia praeconvexa 01111 00000 02101 00020 11021 10221 02101 ??20
Character states are described in the text.
1851 was chosen as the earliest representative of the
Diadematacea Duncan, 1889. The genus appeared as
early as the end of the Triassic (Bather, 1911; Kier,
1977; Smith, 1988) and is considered a representative
of the stem group from which all the Irregularia and
Stirodonta Jackson, 1912 originated (Smith, 1981). The
Aristotle’s lantern of D. bowerbankii was precisely
described by Hawkins (1934), and is among the
oldest known of the aulodont type (Kier, 1974;
Jensen, 1981). The species Acrosalenia hemicidaroides
Wright, 1851 was selected as the representative of
the Stirodonta, which has been considered a possible
ancestor for certain groups of, or for all, the irregular
echinoids (Durham & Melville, 1957; Melville, 1961;
Durham, 1966; Jesionek-Szymanska, 1963; Mintz,
1968). The genus Acrosalenia Agassiz, 1840 appeared
as early as the Early Jurassic (Jensen, 1981), and
is thought to contain the first stirodonts. The family
Acrosaleniidae Gregory, 1900 is characterized by an
eccentric periproct and the presence of one or several
supplementary plates in the apical system (Fell, 1966).
Farquharsonia crenulata Kier, 1972 belongs to the
family Diadematidae, which has been considered the
possible stem group of holectypoids (Mortensen, 1948;
Philip, 1965), pygasteroids (Hawkins, 1912, 1922),
galeropygoids (L. W. Mintz, unpub. Ph.D. thesis, Univ.
California Berkeley, 1966) or of all the Irregularia
(Jesionek-Szymanska, 1963; Smith, 1981). F. crenulata
is characterized by an eccentric periproct within the
apical system. Finally, E. minutum has been placed
as the sister group of the Irregularia (Smith, 1981,
1984). Caenocidaris cucumifera (Agassiz, 1840), a
representative of Cidaroidea Claus, 1880, was chosen
as outgroup to root the trees. The Cidaroidea diverged
from other post-’Palaeozoic’ echinoids as early as the
end of the Triassic (Kier, 1974, 1977; Smith, 1981,
1990).
2.b. Character coding
The high taxonomic level of the analysis required a
selection only of characters relevant to the question
under consideration (as recommended by Stewart,
1993), that is, early evolution of the major irregular
taxa. Therefore, selected characters deal with general
structures of the test common to all taxa in the analysis,
and are not subject to variation at the species level.
A set of 39 characters was coded (Table 2) and
organized into the following four main categories,
which are themselves broken down into subcategories
that deal with specific features within some of these
categories. (1) The first 16 characters concern the apical
system, the periproct and the relationships between
both structures. Character coding relies partly on
Phylogeny and origin of Jurassic irregular echinoids 339
the interpretation of apical disruptions and periproct
migration according to the Extraxial-Axial Theory
(e.g. character 3), a model that is general enough
to allow comparison between morphologically distant
taxa (such as regular and irregular echinoids). (2) The
next 18 characters (17–34) deal with structures of
the corona, including the ambulacra, interambulacra,
peristome, tuberculation and spines. (3) Three charac-
ters (35–37) concern the Aristotle’s lantern. (4) The last
two characters (38, 39) deal with the overall shape of
the test.
2.c. Tree computing methods
We used the software PAUP 4.0b10 (Swofford, 2000)
to perform a parsimony analysis. Because of the
large size of the data matrix (Table 2), trees were
computed using the heuristic search algorithm and
the ACCTRAN optimization criterion. Character states
were unordered. One hundred replicates with random
taxon addition sequences were performed to make
sure that the taxon addition order used by software
PAUP 4.0b10 does not hinder the discovery of other
trees of shortest length. Parsimony indices were
also obtained with PAUP 4.0b10, and indices of
stratigraphic congruence were computed with the
software GHOSTS 2.4 (Wills, 1999b). Three indices of
stratigraphic congruence were calculated: Stratigraphic
Consistency Index (SCI: Huelsenbeck, 1994), Relative
Completeness Index (RCI: Benton, 1994), and Gap
Excess Ratio (GER: Wills, 1999a) tests for index
values were computed by randomization according to
the procedure described in the software GHOSTS 2.4
(Wills, 1999b).
2.d. Character analysis
2.d.1. Genital and ocular plates (characters 1–5)
Plate columns and, in some cases, even individual plates
making up the test of a given sea urchin can be homologized
to those of any other urchin. A numbering system based on the
cycle of radii and interradii around the peristome was devised
by Lov
´
en (1874) as summarized in David, Mooi & Telford
(1995) to refer precisely to specific plates and plate columns.
We use this system to identify specific plates in the apical
system and the coronal skeleton. Also, to save space, we often
omit the term ‘plate’ in reference to a specific element. For
example, ‘genital plate 2’ can be abbreviated to ‘genital 2’.
Genital 2 (which contains the madreporite) is dif-
ferentiated from other genital plates by the pres-
ence of tiny, often numerous, pores (the hydropores)
(Fig. 2a) that lead to the stone canal and thereby to the ring
canal of the water vascular system. In ‘regular’ echinoids,
genital 2 is roughly the same size as other genital plates
(Fig. 2b). In irregular echinoids, genital 2 tends to increase
in size in correlation with the degree to which hydropores are
developed (Fig. 2c) (Kier, 1974). Finally, in some irregular
echinoids, genital 2 expands so much that it completely
separates oculars I and II and genital 1 on one side from
oculars III–V and genitals 3 and 4 on the other (ethmolytic
apical systems) (Durham & Wagner, 1966) (Fig. 2d).
In some for ms, periproct migration is accompanied by
a stretching of posterior apical plates, namely genital 5 and
ocular plates I and V (Fig. 2e). Posterior oculars are stretched
considerably to maintain contact between the periproct
and the apical system, but they regain something close to
their original shape in taxa whose periproct is completely
dissociated from the apical system (Fig. 2a). Genital 5 is the
most distorted plate as the periproct moves away from the
apical system. In the first irregulars, this extraxial plate is
crushed between the posterior rim of the periproct and the
axial plates of interambulacrum 5 (Fig. 2e). Subsequently, the
plate is progressively incorporated into the periproctal area,
and it finally atrophies and almost disappears in more derived
forms (Jesionek-Szymanska, 1959, 1963). Gordon (1926)
showed that in some extant irregulars, genital 5 is present b ut
extremely reduced in size among the scales of the periproctal
membrane.
According to previous authors, the apical system of
pygasteroids should be distinguished from that of other
irregular echinoids by non-elongated posterior oculars and
by the absence of genital 5 incorporated to the posterior
rim of the periproct (Hawkins, 1912; Jesionek-Szymanska,
1963; Smith, 1981, 1984). However, this is contradicted
by personal observations of different species (Plesiechinus
ornatus (Buckman, 1845) in Strickland & Buckman, 1845;
Pygaster trigeri Cotteau, 1857 in Cotteau & Triger, 1855–
1869; Pygaster laganoides Agassiz, 1839; Pygaster joleaudi
Besairie & Lambert in Lambert, 1933a; Pygaster umbrella
Agassiz, 1839 and Pygaster gresslyi Desor, 1842) showing
that posterior oculars are really elongated in these species
(Fig. 2f), and that genital 5 can be present on the posterior
rim of the periproct, as observed in a juvenile specimen of
P. trigeri (Bathonian of Sarthes, France; collection of Votat).
This supports Gordon’s (1926) hypothesis that genital 5 is
incorporated into the periproctal area in all irregular echin-
oids. Perforated by a gonopore in regular echinoids, genital
plate 5 loses the gonopore in the first irregulars (but it is still
present in ‘P.’ hawkinsi) when the plate begins to be distorted.
A fifth gonopore reappears several times in the evolutionary
history of irregular echinoids: in the Cretaceous holectypoids
and in at least three separate clades in the Cenozoic
clypeasteroids.
In endocyclic echinoids, whether ‘regular’ or irregular,
posterior ocular plates are separated by the periproct and
genital plate 5 (Fig. 2b). In exocyclic echinoids, periproct
migration out of the apical system leaves a ‘free space’ within
the apical ring, which is filled either by additional plates or
by the rearrangement of standard apical plates according
to various patterns that depend on the taxa considered.
Posterior oculars are separated by supplementary plates in
stem irregulars (Fig. 2g), but are brought closer and finally
contact each other in more derived taxa (Fig. 2h). However,
in ethmolytic apical structures, posterior oculars do not come
into contact because genital plate 2 is extended posteriorly
between them (Fig. 2d). The extension of genital plate 2 is
independent of periproct migration. Therefore, the separation
of posterior oculars was coded in different ways depending
on whether they are separated by supplementary plates or by
genital plate 2.
1. Development of the genital plate 2: 0, all genital plates of
nearly the same size; 1, genital 2 enlarged.
2. Elongation of posterior ocular plates: 0, posterior ocular
plates short; 1, posterior ocular plates elongated (much
longer than wide).
340 T. SAUC
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EDE , R. M OO I & B. DAVI D
Figure 2. Characters involving genital and ocular plates. ( a) Pachyclypus semiglobus: hydropores are not widespread and genital
2 is approximately of the same size as other genital plates; posterior oculars do not contact the periproct and are not elongated.
(b) Acrosalenia hemicidaroides: all genitals have the same size, genital 5 excepted. (c) Metaporinus sarthacensis: hydropores are
widespread and genital 2 is the largest genital plate. (d) Pseudosorella orbignyana: in ethmolythic apical systems, apical plates are
separated by the significant extension of genital 2. (e) ‘P.’ hawkinsi: posterior oculars and genital 5 are elongated, and genital 5
is ‘crushed’ between the axial plates of the corona and the periproct. (f) Pygaster gresslyi: posterior ocular plates are elongated.
(g) Hyboclypus caudatus: posterior oculars are separated from each other by the periproct and supplementary plates. (h) Clypeus plotii:
posterior ocular plates are in contact with each other.
3. Contact between posterior ocular plates: 0, ocular plates
completely separated by the periproct or by supplement-
ary plates; 1, ocular plates in contact (or separated by
genital plate 2 in ethmolytic apical structures).
4. Development of genital plate 5: 0, genital plate 5 well
developed and not deformed; 1, genital plate 5 crescent-
shaped, lying at the lower side of the periproct; 2, genital
plate 5 lacking or reduced.
5. Perforation of genital plate 5: 0, genital plate 5 bearing a
gonopore; 1, genital plate 5 not bearing a gonopore.
2.d.2. Supplementary plates (characters 6–9)
In all Jurassic ir regular taxa, the breakout and migration of
the periproct is associated with formation of supplementary
(or complementary) plates inside the apical system. Supple-
mentary plates first appear in the fossil record in the genus
Galeropygus Cotteau, 1856 (the earliest, known species of
Galeropygus is Galeropygus lacroixi Lambert, 1924 from
the Upper Pliensbachian, but the type specimen appears to
be missing from Lambert’s collections; the earliest, preserved
apical system is from G. agariciformis (Wright, 1851)
from the Upper Toarcian), and they progressively disappear
in all taxa during the Late Jurassic, once the periproct
and the apical system are completely separated (except
in holectypoids). Contrary to some previous descriptions
(Jesionek-Szymanska, 1963; Fell, 1966), and in spite of
their infrequent preservation, we have found supplementary
plates in pygasteroids (Hawkins, 1944) and in holectypoids
(Fig. 3a). The apical system of Holectypus has long been
interpreted to be composed of five genital plates, the fi fth
genital plate lacking a gonopore in the Jurassic (Wagner &
Durham, 1966). However, considering the apical disruptions
induced by periproct migration, and the presence of two
or three supplementary plates in the species Holectypus
hemisphaericus Desor in Agassiz & Desor, 1847, it seems
more likely that the fifth imperforate ‘genital’ plate of
Holectypus and Pileus Desor, 1856 is a supplementary plate.
The term ‘genital’ used by most authors actually refers to a
function recovered by Cretaceous holectypoids (the plate is
again perforated by a gonopore (Wagner & Durham, 1966)),
and does not refer to a homology with the posterior genital 5
of other taxa. Supplementary plates are also present in some
‘regular’ taxa (e.g. Acrosaleniidae) characterized by a very
eccentric position of the periproct within the apical system
(Fig. 3b).
Supplementary plates are formed inside the apical system.
They do not originate in contact with ocular plates, they
generally present no precise structural pattern, and they
Phylogeny and origin of Jurassic irregular echinoids 341
Figure 3. Characters involving supplementary plates. (a) Holectypus depressus: genital plate 5 is replaced by a supplementary plate.
(b) Acrosalenia hemicidaroides: the ‘regular’ family Acrosaleniidae is characterized by the presence of several supplementary plates in
the anterior part of the apical system. (c) Hyboclypus caudatus: supplementary plates fill the space created by periproct migration. (d)
Pygorhytis ringens: in the first Atelostomata, the apical system is broken into an anterior part (trivium) and a posterior part (bivium).
(e) Orbigniana ebrayi: a supplementary rupture is present within the trivium. (f) Collyrites elliptica: catenal (supplementary) plates
are present between the trivium and the bivium as well as between the bivium and the periproct.
are variable in size and number irrespective of specimen
size. In view of their pattern and position with respect to
other apical plates, we consider supplementary plates as
elements of the extraxial skeleton. They are present either
in the anterior or posterior part of the apical system, and
generally fill the free space created by the departure of the
periproct (Fig. 3c). In Jurassic Atelostomata, the stretching
of the apical system results in breakage into an anterior sub-
unit, the trivium (composed of three ocular and four genital
plates), and a posterior sub-unit, the bivium (composed
of two ocular plates) (Fig. 3d). These two sub-units are
connected by a row of supplementary plates, called catenal
plates (Durham & Wagner, 1966), and aligned along the
III-5 axis in cer tain taxa (Orbigniana ebrayi (Cotteau, 1874)
in Gotteau, P
´
eron & Gauthier, 1873–1891; Cyclolampas
kiliani (Lambert, 1909)) (Fig. 3e). Supplementary plates
may also link posterior oculars to the periproct (e.g. in
Infraclypeus Gauthier, 1875 in Cotteau, P
´
eron & Gauthier,
1873–1891 and Collyrites Desmoulins, 1835). In this
case, we assign the term catenal to these plates as well
(Fig. 3f).
6. Supplementary plates between the bivium and the trivium:
0, no supplementary plates between the bivium and the
trivium; 1, supplementary plates in continuous row of
catenal plates between the bivium and the trivium; 2,
supplementary plates in irregular plating between the
bivium and the trivium.
7. Supplementary plates between the posterior ocular plates
and the periproct: 0, no supplementary plates between the
posterior ocular plates and the periproct; 1, supplementary
plates forming a catenal row between the posterior ocular
plates and the periproct; 2, supplementary plates in
irregular plating between the posterior ocular plates and
the periproct.
8. Supplementary plates between the anterior ocular plates:
0, no supplementary plates between the anterior ocular
plates; 1, supplementary plates present between the
anterior ocular plates.
9. Supplementary plates between the posterior ocular plates:
0, no supplementary plates between the posterior ocular
plates; 1, supplementary plates present between the
posterior ocular plates.
342 T. SAUC
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EDE , R. M OO I & B. DAVI D
Figure 4. Relationships between the periproct and the apical system. (a) ‘Plesiechinus’ hawkinsi: the periproct is still enclosed within
the apical system, but posterior apical plates are stretched by the onset of periproct migration. (b) Pygaster gresslyi: posterior ocular
plates are elongated but do not contact genital 5, the apical system is exocyclic. (c) H. hemisphaericus: the periproct is isolated within
the axial plates of the corona. (d) Clypeus plotii: posterior oculars still contact the periproct but the anterior apical plates are already
grouped together. (e) Nucleolites clunicularis: posterior oculars do not contact the periproct and the apical plating forms a compact
structure. (f) Pyrorhytis ringens: the apical plating of the trivium forms an intercalary structure. (g) Caenocidaris cucumifera: the
apical plating forms a dicyclic structure. (h) Acrosalenia hemicidaroides: the apical plating forms a hemicyclic structure.
2.d.3. Relationships between periproct and apical system
(characters 10–13)
In ‘regular’ echinoids, two distinct patterns in apical structure
can be recognized: (1) they are said to be dicyclic when gen-
ital and ocular plates form two concentric circles around the
periproct, with no ocular joining the periproctal rim (Fig. 4g),
and (2) they are monocyclic or hemicyclic when at least
some ocular plates form part of the inner circle around the
periproctal rim (Fig. 4a, h) (Durham & Wagner, 1966).
Durham & Melville’s (1966) definition of exocyclism (that
is, tests with the periproct located outside the apical system)
is not precise enough to be applied to early irregular echinoids
which are characterized by apical structures intermediate
between the common endocyclic and exocyclic systems.
Therefore, we refine Durham & Melville’s (1966) definition
of exocyclism as the contact between the periproct and the
axial plates of interambulacrum 5. This contact is made
possible by the breaking of the apical rim (between posterior
oculars and genital 5) and the periproct’s movement out of
the apical circle (as suggested by the term exocyclism).
Exocyclism is realized progressively in many taxa
(Jesionek-Szymanska, 1963), first by the breakage between
the posterior oculars and genital 5, then by the progressive
movement of the periproct away from posterior oculars
which stretch before losing all contact with the periproct
(Fig. 4c, d). Once they lose this contact, apical plates begin
to g roup together and fill the space created by periproct
removal. Therefore, apical plates begin to group together in
the anterior part of the apical system, even when the periproct
is still in contact with posterior ocular plates (Fig. 4e). This
pattern is present in Cassiduloida and basal Atelostomata.
Then, posterior ocular plates tend to group together with the
anterior part of the apical system once they lose contact with
the periproct (Jesionek-Szymanska, 1963; Thierry, 1974)
(Fig. 4e). Finally, exocyclism results in the isolation of
Phylogeny and origin of Jurassic irregular echinoids 343
the extraxial periproct embedded within a growth zone
boundary, between the axial plates of interambulacrum 5 and
distant from other extraxial elements (that is, the genitals)
(Fig. 4c).
The grouping of apical plates is achieved in two different
ways, leading to two types of apical patterns: (1) the
intercalary (or elongate) structure (Fig. 4f) in which genital
plates 1 and 4 are not in contact with the periproct, and genital
plate 2 does not contact genital plate 4; and (2) the compact
structure (Fig. 4d, e) in which genital plates 1 and 4 are not in
contact with the periproct, and genital plate 2 contacts genital
plate 4.
10. Endo- and exocyclism: 0, periproct not in contact with
interambulacrum 5 (endocyclic state); 1, periproct in
contact with the interambulacrum 5 (exocyclic state).
11. Contact between the posterior ocular plates and
the periproct: 0, periproct in contact with the pos-
terior ocular plates (or with the posterior gen-
ital plates when the ocular plates are exsert);
1, periproct not in contact with the posterior ocular
plates.
12. Structure of the apical system: 0, apical system dicyclic,
genital and ocular plates forming two concentric circles
around the periproct, no ocular joining the periproctal
rim; 1, apical system monocyclic or hemicyclic, at least
some ocular plates participate in the inner circle around
the periproctal rim; 2, apical system intercalary, genital
plates 1 and 4 not in contact with the periproct, and
genital plate 2 not in contact with genital plate 4; 3,
apical system compact, genital plate 2 in contact with
genital plate 4.
13. Disjunction of the apical system: 0, posterior ocular
plates and genital plates 1 and 4 in contact; 1, posterior
ocular plates and genital plates 1 and 4 disjunct.
2.d.4. The periproct (characters 14–16)
The periproct is large in pygasteroids and holectypoids, as
well as in L. ludovicii (Smith & Anzalone, 2000) (Fig. 5a, b).
In these taxa, it occupies a much larger surface than the rest of
the apical disc. In contrast, the periproct is relatively smaller
in all other irregular echinoids, with a surface area nearly the
same size as the rest of the apical disc (Jesionek-Szymanska,
1963) (Fig. 5c, d).
In numerous Jurassic irregulars, the periproct remains
on the apical side of the test. This position is described
as supramarginal. However, in the majority of menopygids
and Atelostomata, the periproct migrates posteriorly to the
margin of the test, and is said to be marginal. It can even reach
the oral side (as in Holectypus, Pygurus Agassiz, 1839, and
Infraclypeus Gauthier, 1875 in Cotteau, P
´
eron & Gauthier,
1873–1891) and become inframarginal.
In ‘regular’ echinoids and holectypoids, the periproct is
flush with the test, whereas it is depressed in pygasteroids,
in L. ludovicii and Eogaleropygus microstoma (Lambert,
1933b) (Jesionek-Szymanska, 1978; Smith & Anzalone,
2000). The periproct is vertical and located at the bottom
of a deep anal groove in galeropygoids, cassiduloids and
early atelostomates.
14. Size of the periproct: 0, surface of the periproct smaller
than or of nearly the same size as the apical disc; 1,
surface of the periproct much larger than the apical disc.
Figure 5. Characters of the periproct. In (a) (‘Plesiechinus’
hawkinsi) and (b) (Holectypus hemisphaericus), the periproctal
area exceeds the area filled by apical plates. In (c) (Clypeus plotii)
and (d) (Orbigniana ebrayi), the periproctal area is smaller or
approximately equals the area filled by apical plates.
15. Position of the periproct: 0, periproct supramarginal; 1,
periproct marginal; 2, periproct inframarginal.
16. Attitude of the periproct: 0, periproct flush with the test;
1, periproct in a slight anal groove; 2, periproct vertical
and in a steep anal groove.
2.d.5. Ambulacra (characters 17–21)
Kier (1974) reviewed the evolution of plate compounding
throughout the Mesozoic. Originating in Late Triassic
cidaroids, plate compounding diversified gradually during
the Mesozoic and corresponds to an increase in the
number of elementary ambulacral plates. Kier interpreted the
evolution of plate compounding as a mechanism by which
echinoids could increase the number of tube feet (sensation,
locomotion and food collection), while maintaining the
size of ambulacral tubercles and spines (protection against
predation). Because of miniaturization of their spines,
most irregular taxa are distinguished by simple ambulacral
plating, except in pygasteroids and holectypoids which
344 T. SAUC
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EDE , R. M OO I & B. DAVI D
retain plate compounding of the plesiechinid type. Jensen
(1981) distinguished between the plesiechinid type of plate
compounding in Pygasteroida (which she related to the early
diadematoid type), from the pattern present in Holectypoida
(the holectypid type). This was an argument to make
Eognathotomata polyphyletic, but in designating these as
separate types and therefore essentially as autapomorphies
for each of these groups, Jensen obviated the possibility
that they could contain phylogenetic information. Herein,
we follow Kier (1974) in considering that holectypoids
and pygasteroids share the same type of compounded
plates.
Petaloids are absent in the earliest irregular
echinoids, although ambulacral pores are slightly elongated
in ‘P.’ hawkinsi, pygasteroids and holectypoids (Jesionek-
Szymanska, 1970). Petaloid ambulacra became strongly
developed in cassiduloids (and especially in the genera
Clypeus Leske, 1778 and Pygurus) as early as the Middle
Jurassic, with the outer pore of the pore pairs elongated
into a narrow slit. Petals were slightly developed later on
in Atelostomata, but to a lesser extent. Pore morphology
and tube foot morphology are closely linked (Smith, 1978a,
1980a). Petaloid evolution corresponds to a specialization
of aboral tube feet that allows irregular echinoids to conduct
gas exchange more efficiently, especially in relation to new
living habits such as burrowing, a more intense activity than
grazing (Kier, 1974) that also results in reduced exposure to
ambient water flow.
The appearance of phyllodes corresponds to an increase in
number, specialization and enlargement of adoral ambulacral
pores. The function of phyllodes is to enhance efficiency of
tube feet for food gathering (particle picking) in irregular
echinoids (Telford & Mooi, 1996) or for attachment in
‘regular’ echinoids. Whatever the function, phyllodes were
considered homologous structures in ‘regular’ and irregular
echinoids by Kier (1974). Phyllodes are present in ‘regular’
echinoids as early as the Early Jurassic (in pedinoids). In
pygasteroids, phyllodes are very similar to those of pedinoids.
In galeropygoids and first cassiduloids, phyllopodia became
larger and arranged in arcs of three. This increase in
size and number is correlated with a modification of
adoral ambulacral plating (demi-plates and reduced plates)
that allows crowding of the pores in the region near the
peristome. Phyllode arrangement is used in systematics.
For example, the families Clypeidae Lambert, 1898 and
Nucleolitidae Agassiz & Desor, 1847 are distinguished
according to their phyllopodial patterns (Kier, 1962). Phyl-
lodes are also differentiated in the first Atelostomata which
inherited the arrangement of phyllopodes in arcs of three
(Jesionek-Szymanska, 1963). However, menopygids have
been distinguished from galeropygoids mainly by the absence
of phyllodes (L. W. Mintz, unpub. Ph.D. thesis, Univ.
California Berkeley, 1966; Rose & Olver, 1988).
17. Depression of ambulacra: 0, ambulacra not depressed
on the oral side; 1, ambulacra depressed on the oral
side.
18. Compounded plates (ambulacral units composed of
several elemental plates bound together by a single
large primary tubercle): 0, simple ambulacral plating,
ambulacra composed throughout of simple plates; 1,
compound plating of diadematoid type, unit of three
plates bound together; 2, compound plating of acros-
aleniid type, a simple plate alternates with two plates
bound together; 3, compound plating of plesiechinid
type, each plate overlained by two tubercles that bind
it to two different units.
19. Structure of the adoral part of the ambulacra: 0,
ambulacra composed only of primary plates adorally,
that is plates with an adradial (contact with the
interambulacral column) and a perradial suture (contact
with the neighbouring ambulacral column); 1, ambu-
lacra composed adorally of reduced plates intercalated
between primary plates, and pore pairs arranged in
triads; 2, ambulacra composed adorally of reduced plates
intercalated between primary plates, and pore pairs not
arranged in triads.
20. Petals: 0, petals not differentiated, partitioned isopores
aborally; 1, petals slightly developed, enlarged and
specialized pore pairs aborally; 2, petals well developed,
enlarged and elongated anisopores, outer pores in a
narrow slit.
21. Phyllodes: 0, phyllodes not differentiated, ambulacral
pores not specialized near the peristome; 1, phyl-
lodes with specialized ambulacral pore pairs near the
peristome.
2.d.6. Interambulacra (characters 22, 23)
Atelostomata are distinguished from other irregular echin-
oids by differentiation in the size of their adoral interam-
bulacral plates (Devri
`
es, 1960; Kier, 1974). However, the
earliest Atelostomata (O. ebrayi, C. kiliani, Pygomalus ovalis
(Leske, 1778) and Pygorhytis ringens (Agassiz, 1839)) still
lack this differentiation (Jesionek-Szymanska, 1963; Kier,
1974). Such a differentiation first appeared in the Upper
Bathonian (as in Collyrites elliptica (Lamarck, 1791) in
Brugui
`
ere, 1816) by the enlargement of the first plate of
interambulacrum 5, thereby forming the labrum (Jesionek-
Szymanska, 1963; Mintz, 1968). For Kier (1974), this
differentiation was related to the evolution of heart-shaped
tests with wide peristomes in Atelostomata. Very early in
ontogeny, the relative positions of interambulacral plates
become nearly fixed on the oral side so that test and
peristomial growth is almost exclusively accommodated by
the enlargement of adoral plates.
Galeropygoids and cassiduloids evolved an outward
bulging of the basicoronal interambulacral plates to form
the so-called bour relets. Bourrelets are present, although
slightly developed, in certain menopygids as well. As early
as the Middle Jurassic, bourrelet development is particularly
significant in cassiduloids in which bourrelets intrude into the
peristome (e.g. Clypeus), and might have been involved in
food gathering. These structures are covered by many small
tubercles and tiny spines which some have hypothesized were
used to push particles up into the peristome (Kier, 1962; L. W.
Mintz, unpub. Ph.D. thesis, Univ. California Berkeley, 1966).
However, Telford & Mooi (1996) observed no such function
of the bourrelets in extant Cassidulus Lamarck, 1801, in
which podia were the sole agents of food transfer into the
mouth. Spines were never employed in food manipulation,
and bourrelet spination was actually moved out of the way to
admit particles being manipulated by the phyllopodia.
22. Differentiation of oral interambulacral plates: 0, ba-
sicoronal interambulacral plates not differentiated; 1,
enlarged basicoronal interambulacral plates.
23. Bourrelets (doming of the interambulacra near the
peristome): 0, bourrelets absent; 1, bourrelets present.
Phylogeny and origin of Jurassic irregular echinoids 345
2.d.7. Peristome (characters 24–27)
Buccal notches and the perignathic girdle are structures
internal to the peristome and associated with the function of
the Aristotle’s lantern (Melville & Durham, 1966). They are
present in ‘regular’ echinoids (buccal notches are absent in
cidaroids) and in the irregular pygasteroids and holectypoids
(Kier, 1974) but disappear as the lantern is lost in the
Microstomata. The earliest Microstomata retain relics of
buccal notches and of a perignathic girdle as marks of their
‘regular’ origin. Relics can be found in menopygids (Rose
& Olver, 1988), in L. ludovicii (Smith & Anzalone, 2000),
and in some Atelostomata and galeropygoids (Kier, 1962;
Jesionek-Szymanska, 1963).
In Microstomata, the anterior displacement of the
peristome accompanies the appearance of bilateral symmetry
of the test. Anterior shifting of the peristome can be related
to the adoption of burrowing and infaunal living habits
that necessitated an exclusive forward motion of echinoids
to facilitate the ingestion of particles gathered from the
sediment (Kier, 1974).
24. Buccal notches: 0, buccal notches well
developed; 1, small residual buccal notches; 2,
buccal notches absent;
25. Perignathic girdle (internal processes for attachment of
muscles supporting the lantern): 0, perignathic girdle
complete; 1, perignathic girdle atrophied, no longer
functional; 2, perignathic girdle absent.
26. Position of the peristome: 0, peristome close to a central
position; 1, peristome anterior.
27 Depression of the peristome: 0, peristome depressed; 1,
peristome flush with the test.
2.d.8. Tubercles and spines (characters 28–34)
Kier (1974) and Smith (1981) observed a trend toward
the reduction in size and increase in number of tubercles
and spines in the evolution of post-‘Palaeozoic’ echinoids.
The greatest decrease in size of spines occurs with the
appearance of irregular echinoids. In the earliest irregular,
‘P.’ hawkinsi, tubercles of the oral side are of the same
size in ambulacra and interambulacra, whereas the later
L. ludovicii still retains large interambulacral tubercles
and spines (Smith & Anzalone, 2000). Nevertheless, in
succeeding irregular echinoids, tubercles and spines are of
the same size in ambulacra and interambulacra. The decrease
in tubercle size and their correlated increase in number
became more pronounced in Microstomata as early as the
Pliensbachian, and is noticeable in the genus Galeropygus in
which there are many more tubercles than in Plesiechinus
(Kier, 1974, 1982; Smith, 1978b). In pygasteroids and
holectypoids, tubercles are ordered in concentric rows all
over the test. The areoles, depressions around the tubercles
for attachment of muscles controlling movement of spines,
are asymmetrical around tubercles of the oral side. The
asymmetry is radially arranged all over the oral side, so that
there is no specialization to accommodate the power stroke
by the muscle during movement in a particular direction
(Smith, 1980b). Conversely, the increase in tubercle number
in Microstomata goes along with an unordered arrangement
of tubercles on the test, but the asymmetry of areoles is
organized in accordance with the bilateral symmetry of the
test and is a specialization for forward and unidirectional
movement of echinoids. It is related to the adaptation of
Microstomata to moving upon or within the sediment in a
single direction (Smith, 1978b, 1980b).
Crenulation, the ribbing or lobation of the perimeter of
the tubercle’s platform below the mamelon, evolved once
but has been lost several times in the evolution of regular
echinoids (Lewis & Ensom, 1982). In the Introduction to
the present work, it was noted that Mortensen (1948) used
the crenulation of tubercles as a criterion to argue for
the independent origin of holectypoids and pygasteroids,
whereas Jesionek-Szymanska (1970), as well as Rose &
Olver (1984), showed that crenulation could not be used to
demonstrate the independent origin of these groups. In fact,
tubercles are originally crenulated in irregular echinoids, and
all the Microstomata have crenulated tubercles (L. W. Mintz,
unpub. Ph.D. thesis, Univ. California Berkeley, 1966).
The internal structure of spines differs among echinoids
but is constant in a given species (Hyman, 1955) or even at
higher taxonomic levels such as genera or families (Melville
& Durham, 1966). The internal structure of spines is used
in the systematics of ‘regular’ echinoids. In particular,
some ‘regular’ taxa evolved solid spines, whereas they are
hollow in others as well as in irregular echinoids, excepted
in pygasteroids. Hence, pygasteroids possess solid spines,
whereas spines are hollow in holectypoids (Smith, 1981).
28. Density of primary tubercles on ambulacral plates: 0,
one single large primary tubercle on each ambulacral
plate (or compound plate); 1, two or three ‘primary’
tubercles on each ambulacral plate near the ambitus; 2,
numerous ‘primary’ tubercles on each ambulacral plate
near the ambitus.
29. Density of primary tubercles on interambulacral plates:
0, one single large primary tubercle on each interam-
bulacral plate; 1, two or three ‘primary’ tubercles on
each interambulacral plate near the ambitus; 2, numerous
‘primary’ tubercles on each interambulacral plate near
the ambitus.
30. Ordering of primar y tubercles: 0, primary tubercles
ordered in concentric rows all over the test; 1, primary
tubercles not ordered in concentric rows.
31. Crenulation of primary tubercles (tubercles with ribbed
periphery): 0, primary tubercles crenulate; 1, primary
tubercles smooth.
32. Symmetry of areoles (depression for attachment of
muscles supporting and controlling movement of
spines): 0, areoles with a radial symmetry on the oral
side; 1, areoles with bilateral symmetry, the long axis
arranged radially on the oral side; 2, areoles with
bilateral symmetry, the long axis arranged anterior to
posterior on the oral side.
33. Size of spines: 0, large primary spines; 1, short and
slender primary spines.
34. Internal structure of spines: 0, hollow primary spines; 1,
solid primary spines.
2.d.9. Aristotle’s lantern (characters 35–37)
The importance of the Aristotle’s lanter n for the systematics
of irregular echinoids was discussed in the Introduction.
Smith (1981, 1982) showed that irregular echinoids and E.
minutum evolved diamond-shaped teeth from the aulodont
type (grooved teeth) by paedomorphosis (McNamara, 1982).
Similarly, E. minutum, the holectypoids and juvenile cassid-
uloids (cassiduloids lose the lantern as adults) have wide
346 T. SAUC
`
EDE , R. M OO I & B. DAVI D
pyramids derived from the narrow pyramids of aulodont
echinoids (e.g. Diademopsis Desor, 1855).
35. Presence of the lantern: 0, Aristotle’s lantern p resent in
adults; 1, Aristotle’s lantern absent in adults.
36. Type of teeth: 0, teeth of cidaroid type; 1, grooved teeth;
2, keeled teeth; 3, teeth diamond-shaped in cross-section.
37. Type of pyramids: 0, narrow pyramids; 1, wide pyramids.
2.d.10. Shape of the test (characters 38, 39)
The choice of coding characters linked to the shape of
the echinoid test (profile and outline) in a phylogenetic
analysis may seem questionable. Indeed, at a species level,
such characters are known to be ‘sensitive’ to environmental
variations (N
´
eraudeau, 1995), and their significance for taxa
discrimination may be reproved. For example, in several
Cretaceous irregular groups (such as archiaciids, holectyp-
oids and hemiasters), the shape of the test appears related
to sediment granulometry, to the depth of burrowing, and to
water depth (Nichols, 1959; Smith & Paul, 1985; Zaghbib-
Turki, 1989; N
´
eraudeau & Moreau, 1989). However, because
of the taxonomic level of the present analysis along with
the antiquity and the originality of first irregular echinoids,
it seemed relevant to consider the possible phylogenetic
significance of test shape. Furthermore, Kier (1974) noted
a change in the general shape of the echinoid test with
the appearance of irregular echinoids. He correlated this
change to the migration of the periproct outside the apical
system. Indeed, tests of irregular echinoids can be elongated
and display a bilateral symmetry that distinguishes them
from ‘regular’ echinoids (Smith, 1981). However, in earliest
irregular echinoids, tests are wider than long and the bilateral
symmetry is not so conspicuous (e.g. ‘P.’ hawkinsi and
G. agariciformis). Elongated tests did not appear before
the Middle Jurassic in Microstomata. The elongation and
bilateral symmetry of the test are related to the adaptation of
irregular echinoids to a unidirectional mode of locomotion
(Kier, 1974; Smith, 1978b, 1981, 1984). Irregular echinoids
also evolved flattened tests, particularly pronounced in the
cassiduloids Clypeus and Pygurus (Kier, 1974).
38. Marginal outline of the test: 0, circular outline, length
and width of the test more or less equal; 1, widened
outline, test wider than long; 2, elongated outline, test
longer than wide.
39. Profile of the test: 0, high, rounded test; 1, low, rounded
test; 2, low, flattened test.
3. Results
3.a. General results
The parsimony analysis found 156 shortest trees
with a length of 151 steps. Completion of 100
replicates with random taxon addition sequences
did not reveal the existence of other trees of
equal shortest length. We used a majority-rule con-
sensus tree to summarize this set of trees (Fig. 6).
Phylogenetic relationships among taxa are almost all
resolved, with the exception of two polytomies: one
involves the ‘regular’ echinoids A. hemicidaroides
Wright, 1851 and F. crenulata Kier, 1972 and the
other concerns the derived irregular taxa Clypeus plotii
Leske, 1778, Pygurus depressus Agassiz in Agassiz
& Desor, 1847, Nucleolites clunicularis (Phillips,
1829) and Pseudosorella orbignyana Cotteau, 1855.
Most of the nodes are well supported (Fig. 6);
the uncertainties (4 nodes out of 28) lying within the
relationships among crown cassiduloids (one node)
and atelostomates (three nodes). Parsimony indices
(CI = 0.391, RI = 0.738, RC = 0.288, HI = 0.609)
fall within the ranges of values obtained in previous
cladistic analyses carried out on irregular echinoids
(Suter, 1994; Smith & Anzalone, 2000; Smith, 2001,
2004; Villier et al. 2004). These recurrent and relatively
low values reveal the importance of homoplastic state
changes in these phylogenetic analyses of primitive
fossil forms (Suter, 1994; Villier et al. 2004).
The overall aspect of the majority-rule consensus
tree is clearly asymmetric, with a paraphyletic as-
semblage constituted by stem ‘regular’ taxa, and a
monophyletic group corresponding to the Irregularia
(clade 1). The question of whether to include E.
minutum in the Irregularia or not is discussed below.
This monophyletic assemblage is organized into four
sub-units corresponding to the four main recognized
groups of Jurassic irregulars: the Eognathostomata
(clade 2), the menopygids (excluding Menopygus
nodoti (Cotteau, 1859)) (clade 4), the Neognathosto-
mata Smith, 1981 (clade 5), and the Atelostomata
(clade 6). The last three clades are themselves united
to form a sixth grouping, the Microstomata (clade 3).
The monophyly of Irregularia is well-supported (decay
index ≥ 3, bootstrap value = 90 %), and departs from
Jensen’s analysis (1981) but agrees with all other, more
recent cladistic works (Smith, 1981, 1984; Rose &
Olver, 1988; Smith & Anzalone, 2000; Solovjev &
Markov, 2004).
3.b. Main clades
3.b.1. Clade 1
All recognized irregular taxa in the analysis are strongly
related and form the clade Irregularia (Fig. 6). The clade
is supported by the following synapomorphies: relatively
large size of the periproct (character 14), high density
of primary tubercles on ambulacral and interambulacral
plates (characters 28 and 29), shortening of primary spines
(character 33), L. ludovicii excepted (characterized by
large primary spines attached to a primary tubercle, one
to each interambucral plate), and a relatively low test
camber (character 39). The relatively large surface area
of the periproct is seen in the very first irregulars (‘P.’
hawkinsi and L. ludovicii), as well as in the Eognathostomata
(Clade 2). However, all other irregulars possess a relatively
small periproct. Similarly, a low test profile characterizes
basal taxa, but presents numerous reversions in more
derived groups. On the contrary, characters related to
appendages, namely the increased number of primary
tubercles and shortened primary spines (characters 28, 29
and 33), exhibit relatively low levels of homoplasy and
are shared both by all basal and terminal irregular taxa
(L. ludovicii excepted).
The diamond-shaped teeth (character 36) and narrow
pyramids (character 37) are states shared by E. minutum and
Phylogeny and origin of Jurassic irregular echinoids 347
Figure 6. Fifty per cent majority-rule consensus tree of the 156 equally parsimonious cladograms computed from the data matrix of
Table 2. Caenocidaris cucumifera is the outgroup. Clades discussed in the text are designated by encircled numbers. Four nodes are
not fully supported; their support is given as percentage values in squares. Bootstrap values are indicated in bold on the left of each
branch; Bremer support values are in italics on the right of each branch.
lantern-bearing irregulars (Smith, 1981), and are features that
led Smith (1984) to include E. minutum in the Ir regularia. E.
minutum shares two other characters with irregular echinoids:
the elongation of posterior ocular plates (character 2) and the
development of genital plate 2 (character 1). However, these
two characters show important homoplastic changes within
the Irregularia (Fig. 7).
‘P.’ hawkinsi shares the apomorphic characters of other
irregular taxa: a relatively large periproct (character 14),
and specialization of appendages (characters 28, 29 and
33). Previous authors (Jesionek-Szymanska, 1970; Smith,
1981; Kier, 1982) also considered ‘P.’ hawkinsi to be the
first representative of irregular echinoids on the basis of
its morphological affinities (overall shape and plesiechinid
type of compound plating) with pygasteroids (Plesiechinus,
Pygaster, and Pileus). However, ‘P.’ hawkinsi differs from
pygasteroids and other early irregular taxa in three character
states: the perforated genital plate 5 (character 5), the absence
of supplementar y plates (character 9) and a periproct that is
not depressed (character 16).
Atlasaster jeanneti Lambert, 1937 is discussed herein
because Lambert (1931, 1937) considered this taxon to be an
early irregular representative on the basis of what turns out to
be an erroneous interpretation of its apical system. A. jeanneti
possesses none of the apomorphic characters of ir regular
echinoids, and in the consensus tree, it is placed close to
the regular echinoid D. bowerbankii, with which it shares
smooth primary tubercles (character 31) and the presence of
two primary tubercles on interambulacral plates (character
29). More investigations are needed to determine the precise
phylogenetic position of A. jeanneti, but the present results
indicate that it should be considered an early representative of
the ‘regular’ Diadematacea, lacking any phylogenetic affinity
with irregular echinoids.
3.b.2. Clade 2
Clade 2 (Fig. 6) is fairly well-supported (decay index ≥
3) and corresponds to the superorder Eognathostomata as
described by Smith (1981), the sister group of all other
irregular echinoids (‘P.’ hawkinsi excepted). Apomorphies
of the clade are: genital plate 5 reduced or lacking (character
4), exocyclic apical system (character 10), plesiechinid
compound plating (character 18), bilaterally symmetric and
radially ordered areoles (character 32) and solid primary
spines (character 34). As for Clade 1, characters related
to specialization of appendages (characters 18 and 32)
distinguish the Eognathostomata from other irregular taxa,
whereas other character changes (4, 10 and 34) are homo-
plastic within the Irregularia. The overall morphology of ‘P.’
hawkinsi is very close to ‘pygasteroid’ representatives of
the Eognathostomata, as already discussed above. Although
Plesiechinus can be considered a possible ancestor for
the clade, as a representative of basal irregular echinoids,
348 T. SAUC
`
EDE , R. M OO I & B. DAVI D
Figure 7. List of character state changes in the majority rule consensus tree. For example: 36-1 = change to state 1 of character
36. Non-homoplastic character changes are in bold; reversals are in italics. Clades discussed in the text are designated by encircled
numbers.
it cannot be included in the Eognathostomata because
of the plesiomorphic state of the apical system and of
the periproct. For the most par t, in publications before
the 1980s, ‘pygasteroid’ and ‘holectypoid’ echinoids were
considered completely independent lineages stemming from
unrelated ‘regular’ groups (Durham & Merville, 1957;
Melville, 1961; Philip, 1965; Durham, 1966; L. W. Mintz,
unpub. Ph.D. thesis, Univ. California Berkeley, 1966; M
¨
arkel,
1978; Jensen, 1981). In contrast, our analysis supports
Smith’s view (1981, 1984) and considers ‘pygasteroid’
and ‘holectypoid’ echinoids as sister groups in a distinct,
monophyletic assemblage. Moreover, our results do not
support the traditional dichotomy between ‘pygasteroids’
and ‘holectypoids’. Instead, the taxa Pileus (a traditional
‘pygasteroid’) and Holectypus (‘holectypoid’) form a well-
supported clade, excluding the paraphyletic ‘pygasteroids’
Plesiechinus and Pygaster (Fig. 6).
3.b.3. Clade 3
Clade 3 (Fig. 6) encompasses all irregular echinoids not
included in the Eognathostomata and that lack compounded
ambulacral plates (reversion to the most plesiomorphic state
of character 18), do not possess an Aristotle’s lantern as adults
(character 35), and do not have a complete and functional
perignathic girdle and buccal notches (characters 24 and
Phylogeny and origin of Jurassic irregular echinoids 349
25). This clade corresponds to the superorder Microstomata
as described by Smith (1984). Other character changes
that distinguish basal Microstomata are highly homoplastic.
These are: development of genital plate 2 (character 1),
supplementary plates between anterior oculars (character 8),
and the depression of ambulacra (character 17).
The basal taxon of the clade is L. ludovicii, which is
distinguished from other Microstomata by a mosaic of
plesiomorphic and apomorphic features (Smith & Anzalone,
2000). Plesiomorphic features that separate it from other
taxa in the clade concern the appendages and the periproct.
L. ludovicii is characterized by a single, large primary spine
on each interambulacral plate (characters 29 and 33), ordered
primary tubercles with radially symmetric areoles (characters
30 and 32), and a relatively large periproct that is not arranged
vertically in a deep anal groove (characters 14 and 16).
Clade 3 differs slightly from the superorder Microstomata
as defined by Smith (1984). First, relics of buccal notches
and of the perignathic girdle (characters 24 and 25) are
present in basal taxa and constitute the apomorphic state
for the clade, whereas these structures were considered
absent by Smith (1984). Moreover, the present clade includes
the ‘menopygids’ (the genus Menopygus and Clade 4) and
L. ludovicii, taxa not formally included by Smith (1984).
This extension of Microstomata agrees with Rose & Olver
(1988) and Solovjev & Markov (2004), whereas Smith &
Anzalone (2000) consider L. ludovicii as the sister taxon of
Microstomata.
3.b.4. Clade 4
Clade 4 includes all Microstomata that do not possess
specialized ambulacral plates and pores adorally (characters
19 and 21). This description corresponds to the family
Menopygidae Lambert & Thi
´
ery, 1911 as it was redescribed
by Mintz (L. W. Mintz, unpub. Ph.D. thesis, Univ. California
Berkeley, 1966), except for the exclusion of M. nodoti.
The absence of specialized ambulacral plates and pores
adorally distinguishes ‘menopygids’ from other Microsto-
mata but is not an attribute only of ‘menopygids’. For
example, Eognathostomata also lack specialized phyllodes,
a plesiomorphic character state within the Irregularia.
Characters at the base of Clade 4 (characters 2, 10, 11,
12 and 16) are apomorphic character states of the apical
system but display numerous homoplastic changes within the
Microstomata (Fig. 7). Within Clade 4, some species, such
as Desorella elata (Desor, 1847) in Agassiz & Desor, 1847
and Pachyclypus semiglobus (M
¨
unster, 1829) in Goldfuss,
1826–1844, could be more closely related (L. W. Mintz,
unpub. Ph.D. thesis, Univ. California Berkeley, 1966; Rose
& Olver, 1988), but previous analyses gave too much weight
to homoplastic characters of apical structures. Until new
material is described, we have no robust argument either
to separate Pyrinodia guerangeri (Cotteau, 1862) from the
other three species or to split the clade formed by these four
taxa.
The exclusion of M. nodoti from the clade is an essential
difference from previous works (Lambert & Thi
´
ery, 1911;
L. W. Mintz, unpub. Ph.D. thesis, Univ. California Berkeley,
1966; Rose & Olver, 1988), especially as the genus
Menopygus gave its name to the family Menopygidae. M.
nodoti differs from other ‘menopygids’ by lack of adoral
depression in the ambulacra (character 17), by relics of
the perignathic girdle (character 25), and by plesiomorphic
character states of the apical system (characters 2, 10, 11,
12 and 16). As discussed above, these characters display
important homoplastic changes among the Microstomata.
Rose & Olver (1988) excluded P. guerangeri from the
Menopygidae and put it in incertae sedis, because of the
lack of both an intercalary apical system and anal groove.
However, P. semiglobus exhibits these states as well (a
compact apical system and absence of anal groove), even
though it is included in the family by the same authors (Rose
& Olver, 1988).
3.b.5. Clade 5
Clade 5 comprises Microstomata with compound ambulacral
plates adorally and differentiated phyllodes (characters 19
and 21), as well as an anteriorly placed mouth (character
26). However, members of Clade 5 do not have intercalary
or disjunct apical systems (characters 12 and 13). In
addition, they have differentiated petals (character 20) and
no perignathic girdle (character 25), these characters being
homoplastic at the level of Irregularia. Clade 5 corresponds
to the series Neognathostomata of Smith (1981).
At the base of the Neognathostomata is a paraphyletic
assemblage formed by the so-called ‘galeropygoids’ that in-
cludes the genera Hyboclypus Agassiz, 1839, Eogaleropygus
Jesionek-Szymanska, 1978, and Galeropygus Cotteau, 1856
(Mortensen, 1948; Kier, 1962; Mintz, 1968; Smith, 1981;
Jesionek-Szymanska, 1978). This small paraphyletic group
of three taxa partly corresponds to the family Galeropygidae
Lambert in Lambert & Thiery, 1911 (elevated to the ordinal
rank by Mintz (1968)). ‘Galeropygoids’ constitute the stem
group of other Neognathostomata that correspond to the
orders Cassiduloida Claus, 1880 sensu Mintz (1968), and
Clypeasteroida Agassiz, 1872.
Mortensen (1948), Mintz (1968) and Smith (1981)
included Centropygus petitclerci Lambert, 1901 in the
Galeropygidae, whereas it is placed in incertae sedis by
Kier (1962). This taxon possesses differentiated petals and
bourrelets (characters 20 and 23) as well as an exocyclic
apical system (character 10). All three of these apomorphic
states bring C. petitclerci closer to the order Cassiduloida, of
which it constitutes the basal taxon, than to the paraphyletic
stem group formed by ‘galeropygoids’. The order Cassidu-
loida is supported by numerous synapomorphies, however,
it gave rise to the Clypeasteroida in the Palaeogene and
is paraphyletic de facto (Smith, 1981, 1984; Mooi, 1990;
Suter, 1994; Smith, 2001). Mintz (L. W. Mintz, unpub.
Ph.D. thesis, Univ. California Berkeley, 1966) also included
the poorly known species Jolyclypus jolyi (Gauthier, 1898)
of the Cenomanian within the ‘galeropygoids’. However,
observation of several newly collected specimens suggests
that this species (not included herein) displays close affinities
with the genus Nucleopygus Agassiz, 1840 from the Upper
Cretaceous.
Within the ‘cassiduloids’, the families Clypeidae Lam-
bert, 1898 (including C. plotii and P. depressus) and
Nucleolitidae Agassiz & Desor, 1847 (N. clunicularis
and P. orbignyana) are not differentiated (Fig. 6).
This result agrees with Suter’s (1994) phylogenetic analysis
of cassiduloids that showed the importance of homoplasies
between both families. On the contrary, Kier (1962)
differentiated the two families according to petal shape and
number of pores in the phyllodes.
3.b.6. Clade 6
Clade 6 includes Microstomata with both a disjunct apical
system (character 13) and intercalary apical structure
(character 12) and corresponds to the series Atelostomata.
350 T. SAUC
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EDE , R. M OO I & B. DAVI D
Although they are considered diagnostic characters of the
order Disasteroida Mintz, 1968, characters 12 and 13 undergo
reversion in more derived Disasteroida. That is, the apical
disjunction is resorbed before the appearance of Cretaceous
forms, and compact apical structures appear as early as
the Middle Jurassic in Disaster moeschi Desor, 1858.
What most distinguishes derived Disasteroida from more
basal ones (O. ebrayi, P. ringens, and C. kiliani) is the
differentiation in size and shape of adoral interambulacral
plates (character 22). This differentiation became even
more pronounced during the Cretaceous, corresponding
to a new phase of diversification that gave rise to the
orders Holasteroida Durham & Melville, 1957 (sensu Smith,
1981) and Spatangoida Claus, 1876. The differentiation of
interambulacral plates is a synapomorphy shared by the three
orders Disasteroida, Holasteroida and Spatangoida which
constitute the Atelostomata (Devri
`
es, 1960; Fischer, 1966;
Mintz, 1968; Kier, 1974; Smith, 1981).
Disasteroida have been subdivided into different families
or subfamilies, depending on configuration of apical struc-
tures and degree to which the peristome and ambulacra can
be depressed (Beurlen, 1934; Jesionek-Szymanska, 1963;
Mintz, 1968; Solovjev, 1971; Smith, 1984). However, most of
these different taxonomic subdivisions have not been suppor-
ted by cladistic analyses and seem to constitute paraphyletic
grades (however, see Barras (in press) concerning the family
Tithoniidae). In the present analysis, three different families
can be identified, namely the Tithoniidae Mintz, 1968
(Tithonia Pomel, 1883 and Metaporinus Agassiz, 1844),
Collyritidae d’Orbigny, 1853 (Collyrites and Pygomalus
Pomel, 1883) and Pygorhytidae Lambert, 1909 (Orbigniana
Ebray, 1860, Pygorhytis Pomel, 1883 and Cyclolampas
Pomel, 1883), all of which constitute paraphyletic groupings.
3.c. Homoplasy levels for key features
Parsimony indices for each character show that values
differ considerably according to the character set
analysed. Accordingly, characters coding for plate
structures of apical systems show high homoplasy
values. In particular, the appearance of supplementary
plates (characters 6, 7, 8 and 9) and the relationships
between the periproct and the posterior plates of the
apical system (characters 2 and 11) have the highest
levels of homoplasy. Only two characters show low
levels of homoplasy and depart significantly from
patterns shown by other characters of the apical disc:
the loss of perforation in genital 5 (character 5), an
apomorphy of all irregulars except ‘P.’ hawkinsi, and
the disjunction between bivium and trivium (character
13), an apomorphy of the Atelostomata. Most char-
acters describing the density and the organization of
tubercles (characters 28, 29, 30 and 32) as well as
spine size (character 33) also show low homoplasy
values. Highest values are obtained in characters coding
for the Aristotle’s lantern (characters 35, 36 and 37).
Remaining characters show high values of homoplasy;
they describe the shape and the position of periproct,
the peristome, plate and pore structure of ambulacra
and interambulacra, and the overall shape of the
test.
3.d. Completeness of the fossil record and stratigraphic
congruence
The congruence with stratigraphic range data is some-
times regarded as an additional test of phylogenetic
inferences (Wagner, 2000; Benton, Wills & Hitchin,
2000; Pol, Norell & Sidall, 2004). We do not consider
stratigraphy as a test of topology in the same way that
character distributions are, because the nature of the
evidence is totally different. However, we believe that
detection of stratigraphic incongruence might point
to the need for additional investigations (examination
of new fossils and reanalysis of characters). Among
the three indices calculated, Relative Completeness
Index (RCI) = 13.73, Stratigraphic Consistency Index
(SCI) = 0.61, Gap Excess Ratio (GER) = 0.80 (the
tested values were significantly different from a random
distribution with 0.1 % uncertainty), only the Gap
Excess Ratio (GER) value falls within the range of
values calculated for echinoids in previous analyses
(Benton, Hitchin & Wills, 1999; Villier et al. 2004).
Comparisons between raw values of analyses on
different taxonomic groups are to be considered
cautiously (Pol, Norell & Sidall, 2004), however, it is
noticeable that only the Gap Excess Ratio (GER) values
obtained in our analysis correspond to values obtained
in other works (Benton, Hitchin & Wills, 1999; Villier
et al. 2004). An explanation may come from the fact
that we have selected some taxa of the Lower Jurassic,
where the fossil record of echinoids is particularly
uneven (Thierry et al. 1997; Smith & Anzalone, 2000)
and ghost ranges are potentially significant for primitive
irregular echinoids. Consequently, low values obtained
for the Relative Completeness Index (RCI) are not
surprising. On the contrary, the Gap Excess Ratio
(GER), that is, the proportion of the total ghost range
imposed by the contraints of the cladogram, is not
necessarily affected by significant ghost ranges (Wills,
1998). Moreover, the Stratigraphic Consistency Index
(SCI) values have been shown to be more sensitive
to tree topology than Gap Excess Ratio (GER) values
(Benton, Hitchin & Wills, 1999; Wagner, 1995; Pol,
Norell & Sidall, 2004), and the majority-rule consensus
tree (Fig. 6) shows a pectinate topology with basal taxa
characterized by stratigraphic ranges not drastically
older than the ranges of terminal taxa.
Our choice of representative species implies the
existence of numerous gaps and conflicts between
the tree topology and the stratigraphy, as the strati-
graphic range of the species selected as representative
of a certain combination of characters does not
always correspond to the origination date of the
clades (most of the irregular clades are supposed
to have originated during the Early Jurassic but are
poorly known before the Bajocian). For example, M.
nodoti (Bathonian) is a basal taxon of Microstomata,
although more derived species like E. microstoma
(Middle Toarcian) have an earlier known stratigraphic
Phylogeny and origin of Jurassic irregular echinoids 351
Figure 8. Synthetic representation of the majority rule consensus tree, showing the five main clades of Irregularia. Picture captions
from left to right: Eodiadema minutum, from Wright, 1855–1860; ‘Plesiechinus’ hawkinsi, from Jesionek-Szymanska, 1970; Pygaster
gresslyi, Votat private collection; Loriolella ludovicii, from Smith & Anzalone, 2000; Menopygus nodoti, from Rose & Olver, 1988;
Infraclypeus thalebensis, Clavel private collection; Centropygus petitclerci, Claude Bernard University; Pygomalus analis, from B.
Martin-Garin, unpub. M.Sc. thesis, Univ. Dijon, 2000.
origination. Another example is the basal taxon of
Neognathostomata, Hyboclypus caudatus Wright, 1851
(Bajocian–Bathonian), which is younger than more
derived Neognathostomata such as G. agariciformis
(Upper Toarcian–Bathonian) or C. petitclerci (Upper
Aalenian).
4. Taxonomic implications
The present phylogenetic analysis corroborates the
monophyly of the Irregularia as well as the other
higher taxonomic groupings established by Smith
(1984), namely the superorders Eognathostomata and
Microstomata, and the series Neognathostomata and
Atelostomata (Fig. 8). The analysis also supports
the paraphyly of the family ‘Galeropygidae’ already
suspected by previous authors (Kier, 1962; Mintz,
1968). Unlike those of previous workers (Durham &
Melville, 1957; Melville, 1961; Fell, 1966), our results
suggest the paraphyly of the order ‘Pygasteroida’. We
also consider the family Menopygidae as a paraphyletic
grouping (as opposed to the classifications of Lambert
& Thi
´
ery (1911), Mintz (L. W. Mintz, unpub. Ph.D.
thesis, Univ. California Berkeley, 1966) and Rose &
Olver (1988)). All these changes have implications
for the way in which we classify sea urchins. We
have chosen herein to make reference to PhyloCode
principles in the designation of taxa (De Queiroz &
Gauthier, 1990, 1992, 1994, among many others), and
to rely on stem-based diagnoses of the form, ‘the most
inclusive clade containing one or more component
taxa but excluding others’. PhyloCode designations
are restricted to the six main clades discussed above,
all being retained in the strict consensus of the 156
352 T. SAUC
`
EDE , R. M OO I & B. DAVI D
trees. The PhyloCode is designed so that it can be used
concurrently with the rank-based codes (Cantino & De
Queiroz, 2004), and PhyloCode designations do not
invalidate publication criteria as presently established
for traditional systematics. As the PhyloCode has
not gained universal acceptance for the time being,
we have decided herein to give traditional taxonomic
designations as well.
PhyloCode designation:
Irregularia [P] Latreille, 1825 (converted clade name)
Diagnosis. The largest monophyletic group containing
‘P.’ hawkinsi Jesionek-Szymanska, 1970 but excluding
E. minutum (Buckman, 1845) in Strickland & Buck-
man, 1845.
Traditional taxonomic designation:
Cohort Irregularia Latreille, 1825 sensu Smith, 1981
Remarks. Smith (1984) included E. minutum in a new
family, the Eodiadematidae, which he considered the
first representative of the Irregularia. Members of the
Eodiadematidae possess the diamond-shaped teeth of
Irregularia, but do not share the other synapomorphies
of the clade (that is, the relatively large size of the
periproct and the specialization in size and number of
spines). We restrict herein the usage of Irregularia to
preserve traditional usage, and to hone the description
of the group to include those forms that have numerous
miniaturized spines and a relatively large periproct.
However, we recognize the close affinity between
Eodiadematidae and Irregularia. Eodiadematidae cer-
tainly constitute the stem group of Irregularia, but are
not considered as their first representatives (Fig. 8).
Therefore, we do not include E. minutum and the family
Eodiadematidae within the Ir regularia. A consequence
of the origin of the Irregularia from a common
ancestor with the Eodiadematidae is that ‘regular’
echinoids do not form a natural grouping, but a
paraphyletic stem group for Irregularia. The common
term ‘regular’ remains convenient to designate non-
irregular echinoids, but as a taxonomic concept, it is
bankrupt.
The basal and oldest known representative of the
Irregularia is ‘P.’ hawkinsi. This species already has
the specialized spines and an overall morphology close
to the Eognathostomata and to the species arranged
under the generic names Plesiechinus and Pygaster. ‘P.’
hawkinsi is plesiomorphic for characters that concern
phyllodes and the structure of the apical system. In
contrast, the second oldest known irregular species,
L. ludovicii, displays large interambulacral spines
but specialized phyllodes and a more derived apical
structure than ‘P.’ hawkinsi. This suggests that the
very first irregulars, which radiated during the Early
Jurassic, should display a mosaic of plesiomorphic
and apomorphic features. As demonstrated by Smith
(1978b) and Smith & Anzalone (2000), this mosaic
depends on the relative degree of specialization of first
irregulars for both deposit feeding (L. ludovicii) and an
infaunal life-style (‘P.’ hawkinsi).
Contrary to Lambert’s description (1931, 1937),
A. jeanneti possesses no synapomorphies with the
Irregularia and nothing to justify maintaining it within
that clade.
PhyloCode designation:
Eognathostomata [P] Smith, 1981 (converted clade
name)
Diagnosis. The largest monophyletic group containing
P. ornatus (Buckman, 1845) in Strickland & Buckman,
1845, but excluding L. ludovicii (Meneghini, 1867).
Traditional taxonomic designation:
Superorder Eognathostomata Smith, 1981
Remarks. Because ‘P.’ hawkinsi is the basal taxon
of the Irregularia, the genus
Plesiechinus is de facto
paraphyletic. Consequently, the order Pygasteroida
justified by Durham & Melville (1957) and Melville
(1961), and including the genera Plesiechinus, Py-
gaster, and Pileus, is also paraphyletic. Moreover,
the clade formed by P. gresslyi, Pileus hemisphaeri-
cus and Holectypus depressus (Leske, 1778) makes
Pygasteroida paraphyletic as well. However, a more
detailed analysis at a lower taxonomic level is needed to
determine the precise position of the species within the
genera Plesiechinus, Pygaster and Pileus. Concerning
‘pygasteroid-like’ species, this could lead to the
partial abandonment of the generic name Plesiechinus
in favor of the name Pygaster. In this case, the
name Plesiechinus would be maintained only for the
species ‘P.’ hawkinsi, as already suggested by Smith
(http://www.nhm.ac.uk/palaeontology/echinoids/).
PhyloCode designation:
Microstomata [P] Smith, 1984 (converted clade name)
Diagnosis. The largest monophyletic group containing
L. ludovicii (Meneghini, 1867) but excluding P. ornatus
(Buckman in Strickland & Buckman, 1845).
Traditional taxonomic designation:
Superorder Microstomata Smith, 1984
Remarks. We include L. ludovicii in the Microstomata,
of which it represents the earliest form. M. nodoti and
the clade formed by other menopygids are included
in the Microstomata as well, and form a paraphyletic
basal grouping. The crowngroup of the Microstomata
is subdivided into two sister groups formed by the
Neognathostomata and the Atelostomata (Fig. 8).
PhyloCode designation:
Infraclypeidae [P] (new clade name)
Diagnosis. The largest monophyletic group containing
both Infraclypeus thalebensis Gauthier, 1875 in Cot-
teau, P
´
eron & Gauthier, 1873–1891 and P. guerangeri
Phylogeny and origin of Jurassic irregular echinoids 353
(Cotteau, 1862) but excluding H. caudatus Wright,
1851.
Traditional taxonomic designation:
Family Infraclypeidae, new family
Type genus: Infraclypeus Gauthier, 1875 in Cotteau,
P
´
eron & Gauthier, 1873–1891
Other genera included: Pyrinodia Pomel, 1883,
Desorella Cotteau, 1855 and Pachyclypus Desor,
1858
Diagnosis. Microstomata with an exocyclic apical
system and that do not possess specialized ambulacral
plates and pores adorally, that is to say, without
differentiated phyllodes.
Remarks. The former Menopygidae here constitutes
a paraphyletic grouping, and its diagnosis must be
changed. Menopygus displays a more derived tuber-
culation and apical structure than Loriolella, but does
not have synapomorphies with other ‘menopygids’. In
the present analysis, four menopygids form a clade
supported by homoplastic characters, but excluding M.
nodoti (Fig. 8). As Menopygus was the type genus of the
former family Menopygidae, we are forced to provide a
new name for the ‘menopygids’ of Clade 4. We propose
the most derived genus of the clade, and its type species
I. thalebensis, as the source for that name, and call the
new clade the Infraclypeidae [P].
PhyloCode designation:
Neognathostomata [P] Smith, 1981 (converted clade
name)
Diagnosis. The largest monophyletic group containing
H. caudatus Wright, 1851 but excluding O. ebrayi
(Cotteau, 1874) in Gotteau, P
´
eron & Gauthier, 1873–
1891.
Traditional taxonomic designation:
Series Neognathostomata Smith, 1981
Remarks. The Galeropygidae is a paraphyletic grouping
and constitutes the stem group of Cassiduloida.
‘Galeropygoids’ share the plesiomorphic character
states of Neognathostomata, such as the absence
of bourrelets, and differ fundamentally from basal
Atelostomata only by a non-disjunct apical system.
In particular, the species H. caudatus and O. ebrayi
(a basal atelostomate) are very similar except for the
disjunction of the apical system. This close affinity
between certain basal Neognathostomata and basal
Atelostomata explains why both clades are more
weakly supported (Bremer support = 1, Fig. 6) than
the other clades defined herein (Fig. 8). However,
basal Neognathostomata and basal Atelostomata are
distinguished by a non-homoplastic, unequivocal char-
acter dealing with apical structure (disjunction of the
apical system) and no confusion is possible. Therefore,
phylocode designations are proposed herein for the
monophyletic groups Atelostomata and Neognathosto-
mata.
PhyloCode designation:
Atelostomata [P] Zittel, 1879 (converted clade name)
Diagnosis. The largest monophyletic group containing
O. ebrayi (Cotteau, 1874) in Gotteau, P
´
eron & Gauthier,
1873–1891, but excluding H. caudatus Wright, 1851.
Traditional taxonomic designation:
Series Atelostomata Zittel, 1879 sensu Smith, 1981
Remarks. The Disasteroida is the only representative
of the Atelostomata in the Jurassic. It constitutes the
stem group of Holasteroida and Spatangoida, which
necessarily makes the Disasteroida in the original
sense paraphyletic. Within the ‘disasteroids’, our
results do not support the monophyly of Pygorhytidae,
Collyritidae and Tithoniidae.
5. Discussion
5.a. Exocyclism and irregularity
Results of our analysis reinforce Smith’s conclusions
(1981, 1984) concerning the monophyly of Irregu-
laria and the phylogenetic interrelationships existing
between the main groups of irregular echinoids
(Fig. 8). Moreover, our results permit better assessment
and placement of the evolutionary events at the origins
of the principal subsets of irregular echinoids, partic-
ularly concerning the evolution of apical structures.
Therefore, it can be established from the eccentric
position of the periproct within the apical circle that
the migration of the periproct out of the apical system
started at the outset of the origins of the group
(in ‘P.’ hawkinsi). However, the complete separation
between the periproct and the rest of the apical system
(= tr ue exocyclism) occurred several times independ-
ently, at different times, following different morpho-
logical patterns within the different irregular clades
as early as the Early Jurassic (in Eognathostomata)
and as late as the Late Jurassic (in Microstomata).
Therefore, irregularity and exocyclism are not perfectly
synonymous terms (Jesionek-Szymanska, 1959; L. W.
Mintz, unpub. Ph.D. thesis, Univ. California Berkeley,
1966), and true exocyclism cannot be considered
an apomorphy of Irregularia to the exclusion of all
‘regular’ endocyclic echinoids. Irregularity must be
defined by characters of the corona as well, namely the
high density and small size of tubercles and spines,
and not only by characters of the apical system.
The appearance of irregularity is a unique event,
accompanied by changes in both the corona and the
apical system, whereas exocyclism has occurred inde-
pendently along several lineages, and does not serve
to characterize any single clade. This interpretation
relies explicitly on the distribution of evolutionary
events in a phylogeny, using several features to
support each node instead of relying on the more
354 T. SAUC
`
EDE , R. M OO I & B. DAVI D
classical idea of using a single, sometimes superficial
feature to describe a large and complex taxonomic
assemblage.
5.b. Adaptation and homoplasy
The evolution of the first irregular echinoids was
achieved through important morphological changes
concerning both external and inter nal features and
plate architecture. The external features concerned
were spines, tubercles, amb ulacral pores (phyllodes
and petals) and the periproct, and internal features
include the Aristotle’s lantern. These features are
related to the biological functions of locomotion,
nutrition and breathing, and their evolution is controlled
by phylogenetic constraints. Adaptive characters are
sometimes associated with high levels of homoplasy
in irregular echinoids (Suter, 1994; Villier et al.
2004). However, our results would show that most
of these ‘adaptive’ characters provide an excellent
phylogenetic signal when they are not coded as
superficial similarities, but as features that are analysed
with phylogenetic definitions of homology firmly in
mind. Specialization of the Aristotle’s lantern, spines,
tubercles and phyllodes constitute apomorphies for
the different taxa, and even for the entire Irregularia.
The phylogenetic signal yielded by these characters
stresses the importance of the environmental context
of the origin and diversification of irregular echinoids.
The palaeoenvironmental context of the appearance of
irregular echinoids is the colonization of new habitats
that forced a rapid diversification of the group during
the Early Jurassic (Kier, 1974, 1982; Smith, 1978b,
1984). Smith (1981) interpreted the reduction in size
and the increase in number of spines and tubercles
as an adaptation of the first irregular echinoids to
locomotion in soft bottom environments and to an
infaunal life-style (Smith, 1984). According to Rose
& Olver (1984), this is a first step in the specialization
of irregular echinoids, and it allows determination of
a morphological and stratigraphic boundar y between
regularity and irregularity.
Smith & Anzalone (2000) showed that the first
known Microstomata, L. ludovicii, retained large
primary interambulacral tubercles and spines. This
constitutes evidence of an epifaunal life-style. How-
ever, L. ludovicii had already adopted a deposit-feeding
habit (small peristome, atrophy of the Aristotle’s lantern
and specialization of ambulacral pores adorally). In
contrast, the Eognathostomata retained the lantern to
collect the organic component of particles at the surf ace
of the sediment in spite of the fact that they could have
lived buried in the sediment (Smith, 1978b, 1984).
Therefore, in Microstomata, it seems that there has
been a rapid and early specialization to deposit-feeding
before the appearance of an infaunal or semi-infaunal
behaviour. As early as the end of the Liassic, the
Microstomata (e.g. Galeropygus) possessed special-
ized tubercles (with asymmetric areoles), a bilateral
symmetry of the test, and prominent phyllodes. These
characters are adaptations for burrowing (Kier, 1974;
Smith, 1978b, 1984) and show that at that time,
unlike the Eognathostomata, the Microstomata no
longer lived semi-epifaunally. Therefore, the two main
clades of the Irregularia, the Eognathostomata and the
Microstomata, adopted two different strategies in the
adaptation to new ecological niches. This explains why
adaptative characters are phylogenetically informative
in separating the clades.
Periproct migration has an adaptative significance
as well. It has been constrained, initiated or fostered
by environmental factors (Smith, 1984). However,
it accompanies disruptions of apical structures that
are developmentally (David, 1990) or epigenetically
controlled. This is true only for (1) the whole clade
of the Irregularia, characterized by a stretching of
posterior oculars and genital 5 in basal taxa, and for (2)
basal Atelostomata, distinguished by the disjunction of
the apical system into a bivium and a trivium. However,
all other characters showed numerous homoplastic
changes and illustrate an iterative evolutionary scheme
within main irregular clades. For example, vertical
orientation of the periproct occurred five times, and the
appearance of supplementary plates, the disappearance
(atrophy) of genital 5 and exocyclism was realized
independently in almost all of the main clades. Unlike
Suter’s work (1994) on Cassiduloida, this high level of
homoplasy cannot be directly interpreted as a result of
adaptation to the external environment. This instead
suggests invocation of a ‘structuralist’ explanation,
namely internal constraints that limit the disparity
of apical structures, as advocated by Rieppel (1989).
These constraints may derive from the conservative
morphogenetic processes and hierarchical structure of
ontogenetic processes (Rieppel, 1989), that is, epigen-
esis. To sum up, the evolution of the first irregular
echinoids (evolution of plate, lantern and appendage
features) illustrates the interplay between functionalist
(external) and structuralist (internal) factors (Wake,
1989).
5.c. The Extraxial–Axial Theory
The reduction of extraxial body wall and the correlated
increase in axial body wall is a general pattern in
echinoderm evolution, and par ticularly in echinoids
in which the extraxial region is extremely reduced
(David & Mooi, 1996, 1998). In irregular echinoids,
the restructuring of the extraxial region (periproct and
genital plates), delimited by the axial corona, is realized
through a secondary and temporary development
of the extraxial part of the body wall within the
apical system. It is realized either by the significant
increase in periproct size in the Eognathostomata and
early Microstomata such as L. ludovicii (Smith &
Anzalone, 2000), or by the pronounced development
Phylogeny and origin of Jurassic irregular echinoids 355
of supplementary plates in the Microstomata. However,
once the periproct has moved down interambulacrum
5 and becomes separated from the apical system, the
extraxial component is again reduced. Therefore, the
evolution of the apical system of the first irregular
echinoids is realized through a temporary (Early and
Middle Jurassic) change in the ratio between the
extraxial and the axial components of the body wall.
This is yet another example of the fact that the
interaction of the two major components of the body
wall of echinoderms plays an integral role even in those
forms in which the extraxial component is the most
reduced: the echinoids.
Acknowledgements. This paper is a contribution to the team
‘Macro
´
evolution et dynamique de la biodiversit
´
e’ of the
UMR CNRS 5561 Biog
´
eosciences. We are indebted to D.
Cassel, B. Clavel, P. Courville, J.-C. Dudicourt, D. Fournier,
J. Thierry and P. Votat for the loan of specimens. A. Rage
(MNHN, Paris) and A. Prieur (Universit
´
e Claude Bernard,
Lyon) are thanked for their assistance. The constructive
comments of C. Barras and of an anonymous reviewer greatly
improved an early draft of this paper.
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