22 From Bilateral Symmetry to Pentaradiality

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The Phylogeny of Hemichordates and Echinoderms

Andrew B. Smith

Kevin J. Peterson

Gregory Wray

D. T. J. Littlewood

365

Nested within the clade of bilaterally symmetrical animals,

variously called the triploblasts or the bilaterians, lies a most

unusual group. Although most bilaterians have a bilaterally

symmetric body plan, with a clear anterior–posterior axis and

in most cases a differentiated head region, the echinoderm

adult is constructed on a pentaradiate plan and lacks an

obvious anterior–posterior axis (e.g., figs. 22.1, 22.6, and

22.8). Yet echinoderms clearly start out life as bilateral organisms,

and their peculiar body plan is a secondary modification

that arises during the metamorphosis that transforms

them from larva to adult. It is because echinoderms are so

very different in appearance from their closest relatives, the

hemichordates, that they provide a fascinating and important

group for evolutionary and developmental studies.

Based on their pattern of development, both echinoderms

and their bilateral relatives the hemichordates clearly fall

among the deuterostomes. Until comparatively recently, five

major groups (Echinodermata, Hemichordata, Chordata,

Lophophorata, and Chaetognatha) were considered to be

deuterostomes. However, molecular evidence now overwhelmingly

suggests that only the echinoderms, hemichordates,

and chordates belong together (Adoutte et al. 2000,

Cameron et al. 2000, Giribet et al. 2000, Peterson and

Eernisse 2001, Winchell et al. 2002). TheLophophorata are

now recognized to be members of the protostome clade,

specifically part of “Lophotrochozoa,” which includes the

lophophorates and the classically spirally cleaving taxa such

as annelids and mollusks (Halanych et al. 1995). The phylogenetic

affinity of chaetognaths (arrow worms) has been

more difficult to resolve, but the first studies to address their

affinity based on 18S ribosomal DNA (rDNA) data showed

that they were not deuterostomes (Telford and Holland

1993, Wada and Satoh 1994). The bulk of evidence that

has since accumulated suggests that chaetognaths are ecdysozoans

(Halanych 1996, Peterson and Eernisse 2001), although

their precise position within that group remains

uncertain (e.g., Giribet et al. 2000, Zrzavэ et al. 1998, Littlewood

et al. 1998).

Deuterostome Relationships

There are sound reasons for hypothesizing that echinoderms,

hemichordates, and chordates are all closely related: unequivocal

synapomorphies for the clade Deuterostomia include

the shared presence of endogenous sialic acids (Warren

1963, Segler et al. 1978) and gill slits (although these are

present in stem-group echinoderms only). Furthermore, De

Rosa et al. (1999) suggested that deuterostomes also share

two (presumably) independent Hox gene duplications, one

involving the generation of Hox6, Hox7, and Hox8, and the

other involving the generation of the apomorphic Abd-B or

9–13 complex. However, we find the evidence for the central

class duplication being a synapomorphy for Deuterostomia

far from convincing (K. J. Peterson et al., unpubl.

obs.), as did Telford (2000).

366 The Relationships of Animals: Deuterostomes

Resolving the relationships of these three deuterostome

groups has proved controversial. One reason for this is that

hemichordates have an echinodermlike larva but a chordatelike

adult. As a consequence, depending upon whether adult

or larval characters have been emphasized, either an echinoderm

or chordate affinity has been proposed. Thus, Metschnikoff

in 1881 emphasized larval similarity when arguing

that hemichordates and echinoderms are more closely related,

and it was he who proposed uniting them in the taxon

Ambulacraria. Others, starting with Bateson in 1885, have

emphasized the adult similarities and thus come to regard

hemichordates as more closely related to chordates than to

echinoderms [see Hyman (1959) for all historical references].

The first cladistic analyses of morphological characters seemed

to confirm Bateson’s hypothesis. Schaeffer (1987), Gans

(1989), Brusca and Brusca (1990), Cripps (1991), Schram

(1991, 1997), Nielsen (1995, 2001, Nielsen et al. 1996), and

Peterson (1995) all found hemichordates to be the sister group

of the chordates, not of the echinoderms. In some of these

analyses hemichordates were either paraphyletic (Cripps 1991,

Peterson 1995) or polyphyletic (Schram 1991, Nielsen 1995,

2001), with enteropneusts the sister group of Chordata. Characters

shared between echinoderms and hemichordates (e.g.,

dipleurula larva, trimery) were seen as either deuterostome

plesiomorphies or were not considered.

However, starting with the analyses of Turbeville et al.

(1994) and Wada and Satoh (1994), virtually all 18S rDNA

analyses have found significant support for the monophyly

of Ambulacraria (reviewed in Adoutte et al. 2000; see also

Bromham and Degnan 1999, Cameron et al. 2000, Giribet

et al. 2000, Peterson and Eernisse 2001, Winchell et al. 2002,

Furlong and Holland 2002). There are now also several molecular

markers supporting the monophyly of Ambulacraria.

For example, the mitochondrial genetic code for the transfer

RNA lys-1 protein gene in both echinoderms and hemichordates

carries the anticodon CTT rather than TTT as

Figure 22.1. Representative ambulacrarian taxa. (1–9) Echinoderms: (1) brittlestar (Ophiuroidea,

Ophiactis); (2 and 3) sea cucumbers (Holothuroidea, Holothuria and Thelenota); (4) sea lily

(Crinoidea, Anachalypsicrinus); (5) feather star (Crinoidea, Oligometra); (6 and 7) starfishes

(Linckia, Oreaster); (8) regular sea urchin (Echinoidea, Eucidaris); (9) sand dollar (Echinoidea,

Leodia). (10 and 11) Hemichordates: (10) acorn worm (Enteropneusta, Saccoglossus); (11)

colonial hemichordate (Pterobranchia, Cephalodiscus). From Rigby (1993).

From Bilateral Symmetry to Pentaradiality 367

found in most other metazoans, whereas ATA encodes for

isoleucine rather than methionine, a reversal to the primitive

condition (Castresana et al. 1998a, 1998b). Finally, the

Hox11/13a and Hox11/13b genes of echinoderms (Long and

Byrne 2001) have orthologues in hemichordates (specifically

the ptychoderid Ptychodera flava) but are unknown from

other taxa (K. J. Peterson et al., unpubl. obs.).

Morphological characters also lend support to the

monophyly of Ambulacraria (Peterson and Eernisse 2001).

The close similarity between the larva of enteropneust hemichordates

and asteroid echinoderms is striking, and indeed

the former was long thought to be the larva of an unknown

asteroid. Both have a preoral feeding band that creates an

upstream feeding current using monociliated cells and a perioral

ciliated band that manipulates food into the esophagus.

Their basic tricoelomate body organization is also very

similar, both possessing a protocoel and paired mesocoels

and metacoels (called axocoels, hydrocoels, and somatocoels,

respectively, in echinoderms). Peterson and Eernisse

(2001) considered trimery a possible bilaterian plesiomorphy

because they believed both phoronids and potentially

chaetognaths also had a trimeric body plan. However,

Bartolomaeus (2001) has recently shown that phoronids are

not trimeric—the “protocoel” is actually an enlarged subepidermal

extracellular matrix. Hence, neither phoronids

nor brachiopods possess a distinct protocoel. The situation

in chaetognaths is equally dubious because Kapp (2000)

noted that the transverse septum dividing the female part

of the trunk from the male part of the trunk is associated

only with the development of the gonads and forms from

coelomic cells. Therefore, it appears that true trimery is a

synapomorphy uniting the ambulacrarians.

In terms of adult morphology, the most conspicuous derived

character uniting hemichordates and echinoderms is the

axial complex (Ruppert and Balser 1986, Balser and Ruppert

1990). This is the metanephridium (“kidney”) of the adult in

which fluid from the blood vascular system is pressure filtered

by contractions of the madreporic vesicle (echinoderms) or the

heart vesicle (hemichordates) across a layer of podocytes in

the axial gland (echinoderms) or glomerulus (hemichordates)

into the axocoel (echinoderms) or protocoel (hemichordates).

This coelom contains a pore (hydropore) through which the

filtrate is expelled into the external environment. The extensive

development of the mesocoel/hydrocoel to form a tubular

network of tentacles used in feeding is a second obvious

similarity between pterobranchs and echinoderms but, as

shown below, is probably not homologous.

Traditionally, hemichordates have usually been considered

closer to chordates than echinoderms because both

have pharyngeal openings (gills). There is striking morphological

similarity between the gill anatomy of enteropneusts

and chordates and the similarities extend to the molecular

level, because both taxa express the same transcription factor

in the gills (Ogasawara et al. 1999). There is therefore

little doubt that the structures are indeed homologous. As

pharyngeal slits are absent from crown-group echinoderms,

this has been taken as evidence that echinoderms are primitive

and sister group to the clade chordates plus hemichordates.

However, because echinoderms and hemichordates

are sister taxa, the evidence only implies that the possession

of pharyngeal slits is plesiomorphic for deuterostomes

as a whole, and so their loss is an apomorphy of

crown-group echinoderms (fig. 22.2). When precisely echinoderms

lost these structures is something that paleontological

data can shed light on. Evidence that stem group

echinoderms may have had gill slits comes from the careful

work of Jefferies and students (e.g., Dominguez et al.

2002). They have shown that structures comparable with

pharyngeal slits are widely developed amongst a subgroup

of the pre-pentameral stem-group Echinodermata loosely

termed carpoids. Not all, however, agree that these structures

represent gill slits, and some recent analyses place

carpoids within crown group Echinodermata (Sumrall

1997, David et al. 2000).

Most of the other traditional deuterostome characters can

be shown to be either bilaterian plesiomorphies (e.g., radial

cleavage, enterocoely, posterior fate of the blastopore) or restricted

to just the ambulacrarians (e.g., trimery, “dipleurula”

larva). In fact, Peterson and Eernisse (2001) suggested that,

because lophophorates (phoronids and brachiopods, sensu

Peterson and Eernisse 2001) were basal lophotrochozoans, and

chaetognaths were basal ecdysozoans, many of the traditional

characters ascribed to deuterostomes are in fact bilaterian

plesiomorphies. Thus the latest common ancestor of bilaterians

may have been very deuterostome-like.

In summary, a substantial body of corroborative evidence

now exists, from comparative anatomy of both larval and

adult form, from molecular data and from the fossil record,

that echinoderms and hemichordates are sister group to the

exclusion of chordates (fig. 22.2).

Figure 22.2. Deuterostome relationships showing principal

morphological characters of Ambulacraria.

368 The Relationships of Animals: Deuterostomes

Hemichordates

The phylum Hemichordata has traditionally been partitioned

into two groups, the enteropneusts, or acorn worms, and the

pterobranchs. There are approximately 75 species of acorn

worm grouped into 11 genera, and about 20 species of pterobranchs

grouped in only two valid genera Cephalodiscus and

Rhabdopleura [see Benito (1982) for classification]. A third

group, Planctosphaeroidea, are known only as fairly large and

distinctive larvae and are assumed to be the larval form of an

unknown enteropneust (Benito and Pardos 1997). All hemichordates

are benthic marine animals as adults, and those

with indirect development pass through a planktonic larval

stage called a tornaria. Their body is constructed around five

coeloms bilaterally arranged, a single anterior protocoel,

and paired mesocoels and metacoels. The anterior part of

the body associated with the protocoel is the shield (pterobranchs)

or proboscis (enteropneusts). The mesocoel region

forms the collar, and a long trunk contains the metacoels.

There is either one or a pair of protocoel pores, a pair of

mesocoelic ducts and one or more pairs of gill pores in the

anterior part of the metacoel together with genital openings

[see Benito and Pardos (1997) for a detailed description].

Enteropneusts

Enteropneusts are wormlike creatures (fig. 22.1.10), with an

anterior proboscis (protosome), a short collar (mesosome)

and a long cylindrical trunk (metasome). The mouth opens

between the proboscis and collar, and the anus is terminal

at the end of the trunk. There is a series of gill pores on left

and right of the anterior part of the trunk, and unlike pterobranchs,

the paired mesocoelomic ducts open into the first

pair of gill slits. Enteropneusts also differ from pterobranchs

in having no feeding tentacles developed from the collar.

Enteropneusts are solitary and are common in the intertidal

zones where they usually live buried in soft sediment, although

a few are known from depths of up to 400 m, with

one (Saxipendium coronatum) associated with the Galapagos

geothermal vent community. They vary in size from a few

centimeters long (Saccoglossus pygmaeus of the North Sea) to

2 m or more in length (Balanoglossus gigas of Brazil).

Three families of enteropneusts have traditionally been

recognized, Ptychoderidae, Spengelidae, and Harrimaniidae

(Benito 1982). Ptychoderidae is usually considered the most

complicated and “advanced” family united by several synapomorphies,

including the possession of well-developed genital

ridges with lateral septa in the trunk, a pygocord, and

externally visible hepatic sacculations. They also possess

synapticules, but as argued below, this may be a plesiomorphy.

Spengelidae are considered intermediate between

the ptychoderids and the harrimaniids. Spengelids are characterized

by having an appendix on the anterior end of the

stomochord or buccal diverticulum. All known ptychoderids

and spengelids pass through a tornaria larval stage and hence

are indirect developers. The most basic or “primitive” family

is Harrimaniidae. Harrimaniids have proboscis skeleton crura,

which create dorsolateral grooves in the stomochord, and

well-developed proboscis musculature. Development is of the

direct type and is best known in the genus Saccoglossus. A

fourth monotypic family, Protoglossidae, has been proposed,

but most hemichordate workers consider Protoglossus a member

of Harrimaniidae (e.g., Giray and King 1996). Woodwick

and Sensenbaugh (1985) erected a new family, Saxipendiidae,

for the vent worm Saxipendium because it does not

clearly belong to any of the three traditional enteropneust

families.

As nonskeletonized animals, enteropneusts have a scanty

fossil record. The earliest definitive occurrence is from the

Pennsylvanian Mazon Creek fauna (Bardack 1997), with a

second occurrence from the Lower Jurassic or northern Italy

(Arduini et al. 1981). A distinctive trace fossil from the Lower

Triassic of northern Italy has been assigned to Enteropneusta

(Twitchett 1996), but surely many fossilized burrows and

traces reflect the activities of enteropneusts. In fact, Jensen

et al. (2000) suggest that an enteropneust may have been the

maker of the trace fossil Treptichnus pedum, the fossil that

defines the base of the Cambrian system in the stratotype

section in Newfoundland. Yunnanozoon, an enigmatic form

from the famous Early Cambrian Chengjiang Lagerstдtte of

China, has been described as a chordate (Chen et al. 1995),

an enteropneust hemichordate (Shu et al. 1996), or a stemgroup

deuterostome (Budd and Jensen 2000). In our view,

Yunnanozoon shows two chordate apomorphies, a notochord

and segmented muscles, and resembles hemichordates only

in shared primitive characters such as pharyngeal slits. Hence,

we agree with Chen and Li (1997) that Yunnanozoon is best

considered a member of the phylum Chordata.

Pterobranchs

Pterobranchs have the same tripartite body plan as enteropneusts

(fig. 22.1.11). There is a platelike anterior shield

(protosome), a narrow U-shaped collar (mesosome) from

which a paired series of feeding tentacles arise, and a bipartite

trunk (metasome) from which an extensible stalk with a

terminal sucker arises. There are paired mesocoelic ducts and

pores and, in Cephalodiscus, a pair of gill pores that penetrate

the pharynx (Rhabdopleura lacks gill pores, although traces

marking their position remain). Pterobranchs are much less

common than are enteropneusts and are small (generally >

1 cm). All are colonial and attached to the seafloor, either

aggregating (Cephalodiscus) or colonial (Rhabdopleura), and

both inhabit a horny tube (coenecium). Although they can

move out of their tube, they generally remain attached by

their sucker. Reproduction is direct and asexual budding

occurs, with new individuals arising from the stalk. They are

ubiquitous and range in depth from 5 to 5000 m.

Pterobranchs are fairly common fossils with both rhabdopleurid

and cephalodiscid-like fossils known from as early

From Bilateral Symmetry to Pentaradiality 369

as the Middle Cambrian (Chapman et al. 1995). Of course,

what is found is just the collagenous tube built by the animal

(the coenecium). The most important hemichordate

fossil group are the graptolites, which thrived from the

Middle Cambrian until the Late Carboniferous and are especially

important for biostratigraphy from the Early Ordovician

through the Early Devonian. The graptolite coenecium

is very similar to modern, and fossil pterobranchs both in

terms of structure (Crowther 1981) and composition

(Armstrong et al. 1984). However, many graptolites possessed

a structure on the coenecium called a nema that was

not known to be part of any pterobranch coenecium, and to

some this absence precluded a pterobranch affinity for graptolites

(Rigby 1993). Fortunately, Dilly (1993) described a

new species of Cephalodiscus, C. graptolitoides, collected in

deep water off the coast of New Caledonia that possesses a

spine virtually indistinguishable from the graptolite nema.

The demonstration of a nema on a recent pterobranch effectively

removed the last barrier to ascribing a pterobranch

affinity for graptolites (Rigby 1993).

Hemichordate Phylogeny and Classification

A clear account of the history of hemichordate classification

is provided by Hyman (1959). In early cladistic analyses of

deuterostomes the monophyly of Hemichordata was assumed,

with hemichordates treated as a terminal taxon. However,

Cripps (1991), Schram (1991, 1997), Nielsen (1995, 2001,

Nielsen et al. 1996) and Peterson (1995) coded for Pterobranchia,

and Enteropneusta separately and all found Hemichordata

to be either paraphyletic (Cripps, Peterson) or

polyphyletic (Schram, Nielsen). Cripps (1991) even found

Pterobranchia to be paraphyletic, with Cephalodiscus more

closely related to enteropneusts, echinoderms, and chordates

than to Rhabdopleura.

In their recent analysis of metazoan taxa, Peterson and

Eernisse (2001) found support for a monophyletic Hemichordata.

They identified two hemichordate synapomorphies:

(1) the stomochord, a unique extension of the dorsal wall of

the pharynx into the protosome, and (2) the mesocoelomic

ducts, which connect the mesocoel directly to the exterior (see

also Ruppert 1997).

The monophyly of Pterobranchia, although not tested by

Peterson and Eernisse (2001), seems clear. Pterobranch synapomorphies

include the presence of tentacular arms, the

U-shaped gut, the coenecium secreted by the protosome or

cephalic shield, and mesocoelomic ducts that communicate

through pores not connected with the gill slits (as they are

in “enteropneusts”). On the other hand, Enteropneusta were

shown to be paraphyletic, with Harrimaniidae identified as

sister taxon to Pterobranchia, both possessing a ventral postanal

stalk. Some harrimaniids also possess two hydropores

like pterobranchs, raising the possibility that harmaniids

themselves are paraphyletic. However, molecular data (see

below) suggest that this is unlikely, at least for the genera

Harrimania and Saccoglossus. Finally, Peterson and Eernisse

(2001) also found support for the monophyly of Ptychoderidae

+ Spengelidae, both, for example, having metacoelomic

peribuccal spaces in the collar (Benito 1982).

Molecular data are consistent with the morphological

data reviewed above. Studies involving 18S rDNA by

Halanych (1996), Cameron et al. (2000), and Peterson and

Eernisse (2001) support the two major conclusions derived

solely from the morphological analysis, namely, the monophyly

of Hemichordata, and that harrimaniids are the sister

group of the pterobranchs. Furthermore, Cameron et al.

(2000) show with 18S rDNA data that Ptychoderidae, Harrimaniidae,

and Pterobranchia are each monophyletic. 28S

rDNA data, on the other hand, suggest that pterobranchs are

the sister taxon of enteropneusts, and hence Enteropneusta

is monophyletic, although this is not supported in the combined

18S + 28S analysis (Winchell et al. 2002).

Combining available molecular and morphological data

(fig. 22.3; for data, see Smith 2003b) leads to the following

conclusions: (1) Hemichordata is a monophyletic taxon, and

(2) Enteropneusts are a paraphyletic grade, with Harrimaniidae

as more closely related to pterobranchs than to the other

enteropneust families.

If this is a correct phylogeny, then it implies that pterobranchs

may have undergone some secondary simplification

associated with miniaturization. Cephalodiscus, rather

than having a complicated gill skeleton, has just two relatively

simple gill pores, and gill slits are entirely wanting in

Rhabdopleura. Furthermore, pterobranchs have a simple

neuronal ganglion in the collar region, whereas enteropneusts

have a dorsal nerve cord whose development in at

least saccoglossids is reminiscent of chordates (Bateson

1885). Finally, it also implies that the water vascular system

of echinoderms and the tentacles of pterobranchs must have

been independently acquired.

Echinoderms

Echinodermata are a well-characterized group of exclusively

marine invertebrates that includes the familiar starfishes and

Figure 22.3. Phylogenetic relationships of hemichordates based

on 18S rRNA data (from Cameron et al. 2000).

370 The Relationships of Animals: Deuterostomes

sea urchins. They are solitary and almost exclusively benthic

as adults. The group first appears near the base of the Cambrian

and has expanded to colonize a wide range of marine

habitats from intertidal to abyssal trench depths. There are

about 6000 species alive today, and several groups have left

an extensive fossil record.

Echinoderm Autapomorphies

Echinoderms are unique within Bilateria in having an adult

body plan that is pentaradiate in construction, although their

larvae are clearly bilaterally symmetrical. In addition to their

obvious pentaradiate body plan, echinoderms share four

other important morphological traits that identify them as a

monophyletic clade: (1) In the transition from larval rudiment

to adult, there is a striking asymmetry in the fate of

coelomic compartments. Although there is variation in detail

within echinoderm classes (e.g., Janies and McEdward

1993), in all the right hydrocoel is reduced in size and plays

no part in adult structures, whereas the remaining coeloms

ultimately become vertically stacked, with the right somatocoel

aboral to the left somatocoel and the left somatocoel

aboral to the left hydrocoel (see Hyman 1955, Peterson et al.

2000). (2) The left hydrocoel gives rise to a system of tentacles,

as in hemichordates, but in living forms these are not

free extensions, because they remain embedded within the

body-wall and associated with somatocoel components even

when prolonged into a filtration fan. (3) There are no gill

pores, at least among extant representatives. (4) There is a

mesodermal skeleton of calcite that takes the form of a distinctive

meshwork termed stereom. This is present in all

groups, although in holothurians it is typically reduced to

microscopic spicules, and may occasionally be wanting

altogether.

Molecular data are equally unambiguous as to the monophyly

of echinoderms. Phylogenetic analysis of ribosomal

RNA sequence data (Field et al. 1988, Littlewood et al. 1997,

Janies 2001, Peterson and Eernisse 2001) all identify echinoderm

exemplars as forming a monophyletic clade with

strong bootstrap and Bremer support.

Echinoderm Body Plan Organization

One question has long puzzled echinodermologists: What is

the relationship of the adult pentaradiate body plan of an

echinoderm to the bilateral symmetrical plan of a chordate

or hemichordate? In contrast to other deuterostomes, an adult

echinoderm has no obvious anteroposterior, dorsoventral

or left–right axes (fig. 22.4A). Echinoderm researchers have

tended to avoid the whole question of body axis homologies

by referring echinoderm orientation not to an anterior–posterior

axis but an oral–aboral axis. But recent work on the developmental

molecular genetics has finally provided an answer.

One possibility is that each of the five ambulacra in an

echinoderm represents a serially duplicated anterior–posterior

axis in echinoderms. So a starfish would have five anterior–

posterior axes, with each arm tip being the equivalent

of a bilaterian anterior (fig. 22.4C). This idea found initial

support from developmental genetics, when it was shown

that the regulatory gene orthodenticle, which in arthropods

and vertebrates is a “specifier” of anterior structures, is expressed

distally in the arms of developing ophiuroids and

starfish. Another developmental regulatory gene, engrailed,

is active along the anterior–posterior axis of the central nervous

system of several bilaterally symmetrical metazoan phyla

and is also expressed along the developing arms of echinoderms

(Lowe and Wray 1997). However, because developmental

regulatory genes can readily be co-opted into different

roles, such evidence is weak (Wray and Lowe 2000).

More convincing evidence has come from following the

fate of the bilaterally symmetrical coeloms from larva to adult

Peterson et al. (2000) pointed out that because “posterior”

Hox genes are expressed colinearly in the posterior coeloms

(the somatocoels; see also Arenas-Mena et al. 2000), this must

be the primitive locus of expression. If true, then this means

that the primitive adult anterior–posterior axis can be seen

in the larval mesoderm, specifically the paired coelomic sacs.

The development of the adult body plan involves a rotation

of the coeloms such that the right somatocoel comes to lie

underneath the left somatocoel, with both coeloms giving rise

to extraxial skeletal structures at the aboral end of the animal.

Because the primitive axis is mesodermal, this means

that the modified anterior–posterior axis runs from the oral

surface through the left hydrocoel, then the left somatocoel,

and finally the right somatocoel at the aboral end of the animal

(fig. 22.4B). Furthermore, their pentamery is an expres-

Figure 22.4. Schematic representation of body axes in

echinoderms and other deuterostomes. (A) The body outlines

show the arrangement of the nervous system (N), hemal system

(H), digestive system (G), and hydrocoel system (W) in

chordates, enteropneusts, pterobranchs, and echinoderms. A,

anterior; P, posterior. (B and C) Two alternative interpretations

of anterior–posterior body axis in a brittlestar.

Chordate

Enteropneust

Pterobranch

Echinoderm

N H G

H N

G N

W H

N G

G

W

N

H

P

A

A

A

A

A

P

A

A

A

A

P

P

P

A B

C

From Bilateral Symmetry to Pentaradiality 371

sion of secondary lateral outgrowth, not a duplication of

primary body axes as suggested by Raff (1996).

The Five Classes and Their Relationships

There are five extant classes of echinoderms: the crinoids (sea

lilies and feather stars), asteroids (starfishes), ophiuroids

(brittlestars), echinoids (sea urchins), and holothurians (sea

cucumbers). These five classes are well characterized from

both morphological and molecular perspectives. A sixth class,

Concentricycloidea (sea daisies), composed of one genus with

two deep-sea species, has been proposed (Baker et al. 1986),

but recent molecular work (Janies and Mooi 1999) has shown

that this taxon nests well inside Asteroidea.

The crinoids stand clearly apart from the other four

classes. They are primitively stalked and sessile (fig. 22.1.4),

although in one important but derived subclade, the comatulids

(fig. 22.1.5), the stalk is lacking and they are able to swim.

In crinoids, the mouth faces away from the seafloor and the

anus opens in close proximity on the same anatomical surface.

A system of branched arms, which carry extensions of

the somatocoel and water vascular system, form a filtration

fan for food capture. The plates that make up the arms and

that bear the radial water vessels have traditionally been

thought of as ambulacral in origin and thus homologous to

the ambulacral plates in other echinoderms. However, the

presence of somatocoel and somatocoel-related structures

(e.g., gonads) in the arms is evidence for there being part of

the aboral plating system (extraxial plating of David and Mooi

1999, Mooi and David 1997) rather than ambulacral (axial)

plates. Extraxial plating thus is much more extensively developed

than axial plating. In addition the nervous system

of crinoids is very different from that in other echinoderms,

being dominated by the subepithelial component rather than

the epithelial component that dominates in other echinoderms

and hemichordates (Heinzeller and Welsch 2001).

Crinoids have a long fossil record going back to the start of

the Ordovician, although extant crinoids all belong to a clade

whose origins are much more recent, at about 250 Mya (million

years ago; Simms 1999).

The four other echinoderm classes are free-living and

have been grouped together under the name Eleutherozoa.

They live mouth downward and have a nervous system dominated

by the ectoneural component. The starfish (Asteroidea)

are stellate forms whose body projects as five or more arms

from a central region (fig. 22.1.6–7). Major body organs such

as the gonads and stomach extend into the arms. Aboral

(extraxial) and ambulacral (axial) surfaces are approximately

equally developed in almost all taxa, and the ossicles around

the mouth are relatively unspecialized and do not form a jaw

apparatus. Finally, the radial nerve lies externally within the

epithelial layer (fig. 22.5).

Brittlestars (Ophiuroidea) resemble starfish in shape but

have a much more clearly demarked boundary between the

central disk and the narrow, whiplike arms (fig. 22.1.1). The

arms differ fundamentally from those of starfishes in having

a cylindrical core of ossicles (vertebrae) that are modified

ambulacral plates. Aboral (extraxial) and oral (axial) plating

systems are again equally developed. In a few taxa the gonads

extend into the arms, and this was probably much more

common in primitive, extinct representatives. During development,

the radial nerve and radial water vessel become

Figure 22.5. Schematic cross

sections through the body wall

to show radial nerve arrangement

in echinoderms. en =

ectoneural plexus; ep, epithelial

tissue; hn, hyponeural plexus;

m, mesoderm; rn, ectoneural

plexus. Phylogenetic relationships

are indicated by lines.

From Heinzeller and Welsch

(2001).

372 The Relationships of Animals: Deuterostomes

enveloped by epithelial flaps and a secondary cavity, the

epineural sinus, is created (fig. 22.5). All brittlestars and most

starfishes have a blind gut and lack an anus.

Sea urchins (Echinoidea) are primitively globular forms

but have over geological time evolved into a wide range of

shapes (figs. 22.1.8–9). Irrespective of shape, most of their

body skeleton is formed of axial components and thus homologous

to the oral surface of starfish and brittlestars. Aboral

(extraxial) components in sea urchins are confined to the

10 plates of the apical disk and the periproctal system they

enclose. Sea urchins also primitively have a complex internal

jaw apparatus, known as the Aristotle’s Lantern, composed

at least in part of modified ambulacral plates. The

lantern is secondarily lost in some irregular echinoids.

Sea cucumbers (Holothuroidea) are mostly sausage or

worm-shaped animals (figs. 22.1.2–3) whose skeleton is reduced

to microscopic spicules embedded in their thick collagenous

skin. Their mouth and anus are situated at opposite

poles, as in echinoids, with the mouth encircled by a ring of

large feeding tentacles. The only substantial skeletal structure

is an internal ring of 10 ossicles that surrounds the buccal

cavity. Interestingly, holothurians are the only group of

echinoderms that pass through metamorphosis with little

torsion (Smiley 1988).

The relationships among these four eleutherozoan groups

has been much disputed and remain far from settled. Traditionally,

they have been subdivided into two groups, Asterozoa

for the stellate starfishes and brittlestars, and Echinozoa for

the globular to cylindrical sea urchins and sea cucumbers (e.g.,

Fell 1967). However, one or other body form is presumably

the primitive condition for Eleutherozoa as a whole. The transformation

between the two body plans requires only a modest

change in the relative production of aboral and oral

(extraxial and axial) plating systems. Simply by retarding the

production of aboral plating, starfishes such as Podosphaeraster

take on an echinoid-like form (see Blake 1984).

Smith (1984) has argued that Asterozoa are a paraphyletic

grouping, with brittlestars more closely related to Echinozoa

(i.e., Echinoida + Holothuroida) than to starfishes. This was

based on the similarity of larval form, jaw apparatus construction,

internal coelom arrangement, and the enclosure of the

radial nerve and water vessel in ophiuroids and echinoids.

A cladistic analysis of a large morphological data matrix

supported this view (Littlewood et al. 1997), as did a more

detailed analysis of the nervous system of echinoderms

(Heinzeller and Welsch 2001). A revised and emended morphological

character matrix compiled by Janies (2001) also

supported the same topology.

An alternative view (Sumrall 1997, Mooi and David 1997,

2000, David and Mooi 1996, 1999) is that Asterozoa are

monophyletic. Strongest support for this grouping initially

came from mitochondrial genome order (but see below). Just

two morphological synapomorphies support this group; the

presence of a saccate gut and the presence of a system of

adambulacral ossicles.

The relationship between sea urchins and sea cucumbers

is more difficult to establish on morphological grounds. This

is in part because of the extreme skeletal reduction in holothurians,

making detailed comparisons difficult. In addition,

there are also major uncertainties over the homologies

of certain structures, such as the calcareous ring and radial

water vessel. Holothurians, other than apodids, have five

radial water vessels that run along the length of the body and

give rise to tube-feet. These lie within the mesoderm and

have an overlying epineural sinus exactly as in echinoids

(Heinzeller and Welsch 2001; see fig. 22.5), suggesting secondary

enclosure. However, Mooi and David (1997) point

out that the tube-feet are added irregularly along the length

rather than terminally, and that they arise secondarily after

the oral tentacles have formed. Under their model only the

buccal tentacles are homologous to the radial water vessels

in echinoids. They homologize only the oral region of holothurians

with the body of echinoids and believe the trunk

is a novel structure that has been derived from the extraxial

portion of larval tissue.

The fossil record provides crucial evidence linking the

echinoids and holothurians, because of the unusual character

combination found in the extinct and probably paraphyletic

Ophiocistioida. Ophiocistioids have a complex

lantern that is homologous in almost every detail to the lantern

of echinoids. Furthermore, they have an arrangement

of plates similar to that seen in the most primitive of echinoids,

in which there is a central uniserial series of plates in

each ambulacral zone (Smith and Savill 2002). Yet advanced

members reduce their skeleton to wheel-shaped spicules and

platelets that are almost indistinguishable from those of holothurians

(Gilliland 1993). This combination of holothurian

and echinoid traits implies sister-group relationship

between the two living groups.

Molecular Evidence for Echinoderm

Class Relationships

Molecular evidence, derived principally from nuclear and

mitochondrial ribosomal RNA (rRNA) genes, provides clear

support for the monophyly of each of the five classes. Exemplars

of each class always group together, confirming the

long-standing picture from the fossil record that crowngroup

diversification within each class is relatively recent

compared with the time at which the classes diverged from

one another. However, the relationships of the five classes

are much more controversial.

Ribosomal Sequence Data

The pioneering analysis of Raff et al. (1988), based on partial

18S rRNA sequences, identified Asterozoa as paraphyletic,

with asteroids as sister group to Echinozoa. Littlewood

et al. (1997) undertook a more comprehensive analysis for

both complete 18S and partial 28S sequences. They found

that, although both Eleutherozoa and Echinozoa were well

From Bilateral Symmetry to Pentaradiality 373

supported, other groups were only poorly supported. The

most parsimonious solution had ophiuroids as sister group

to Echinozoa, but the two other possible solutions (asteroids

as sister group to Echinozoa, and asteroids and ophiuroids as

sister group) were only one step longer. In the analysis of

Littlewood et al. (1997) regions of ambiguous alignment were

removed before analysis, and consensus sequences were constructed

for each class based on the sequences then available.

Janies (2001) added a considerable number of asterozoan 18S

rRNA sequences to the database and carried out both separate

and combined analyses of molecular and morphological

data. Unlike Littlewood et al. (1997), Janies used the full sequence

data aligned using CLUSTAL (Thompson and Jeanmougin

2001) with various weightings. This identified asteroids

as sister group to Echinozoa when indels, transversions, and

transitions were all equally weighted, and ophiuroids as sister

group when indels and transversions were given a weight of 2.

Janies (2001) then applied a dynamic analysis of the combined

morphological and molecular data (POY; Wheeler and

Gladstein 2000) whereby alignment and tree building occur

together so as to co-optimize all available data. Once again,

there was strong support for Eleutherozoa, Echinozoa, and

each of the five classes. His best total evidence tree identified

Asterozoa as a clade, but with very weak Bremer support.

Just suboptimal is a tree that has asteroids as sister group

to Echinozoa. Significantly, although Echinozoa, Eleutherozoa,

and all five classes can be recovered under a wide range

of parameters (indicating that there is strong support for

these groups), the grouping Asterozoa was only recovered

under a small subset of conditions, and the ophiuroidechinoid-

holothurian clade was hardly ever recovered.

We have reanalyzed the now quite extensive rRNA sequences

in various ways (aligned sequences are provided at

in Smith 2003b) both under parsimony (Paup 4*; Swofford

2001) and Bayesian inference (MrBayes 2.01; Huelsenbeck

and Ronquist 2001). Individually, both 18S and 28S rRNA

sequences rooted on hemichordates identify the same

topology, namely (crinoids(asteroids(ophiuroids(echinoids,

holothurians)))), but with weakest support for the

ophiuroid-echinoid-holothurian pairing. The same topology

resulted from a combined sequence analysis irrespective

of whether only exemplars common to both data sets are used

or whether taxa whose 28S rRNA sequences are currently

unknown were included (fig. 22.6A).

For the combined morphological and molecular analysis,

instead of using gene sequences from exemplars, we have

constructed consensus gene sequences for each class. For

each variable position, the consensus sequence replaces two

or more alternate bases with the international nucleotide code

encompassing the uncertainty. The logic behind this approach

is that it removes the variation within each class that

has arisen since the crown group started to diverge. The sequences

for each order were then aligned, and fast-evolving

regions where alignment was ambiguous (usually because of

the presence of long strings of N values) were removed. The

results are shown in figure 22.6B. High Bremer support was

found for most branches, with the most parsimonious solution

placed ophiuroids as sister group to Echinozoa.

Mitochondrial Gene Order

When the first complete mitochondrial genomes of echinoderms

became available, it was quickly realized that the order

in which genes were arranged around the circle differed

significantly between asteroids and echinoids (Smith et al.

1989). A 4.6-kilobase section of the genome, incorporating

four protein coding genes, was inverted. Subsequently, when

holothurian and ophiuroid mitochodrial genome order became

known, it was shown that echinoids and holothurians

had one arrangement and asteroids and ophiuroids another

(Smith et al. 1993). Comparison with vertebrates as outgroup

showed that it was the asteroid-ophiuroid arrangement that

was inverted, suggesting that the inversion was a synapomorphy

for Asterozoa. However, it is becoming clear that the

order of genes may not be so reliable a marker (e.g., Mindell

et al. 1998) even though there has been reasonable stability

of the mitochondrial gene order among echinoid groups that

last shared a common ancestor some 170 Mya (Giorgi et al.

1996).

The recent publication of the complete crinoid mitochondrial

gene sequence (Scouras and Smith 2001) has confirmed

this view. Crinoids, as the immediate outgroup to Eleutherozoa,

should provide the most appropriate sequence for

determining which mitochondrial genome arrangement is

primitive. However, the crinoid arrangement is significantly

different from both the asterozoan and echinozoan arrangements.

Specifically the crucial 4.6–kilobase section is partly

inverted as in Asterozoa and partly normal as in echinozoans

(fig. 22.7). Thus, the initially strong evidence for an asterozoan

clade is now much more problematic to interpret. Considerable

gene rearrangement is required to transform the

outgroup vertebrate mitochondrial gene sequence to any of

the three echinoderm arrangements, although the echinozoan

sequence requires slightly fewer steps. Both crinoids and

asterozoans have an inverted portion of the genome compared

with either vertebrates or echinoids. It appears, therefore, that

there has been a complicated pattern of rearrangement of the

mitochondrial genomes in the lines leading up to the recent

echinoderm classes. Again, there is no clear solution: either

an inversion has occurred before crown group separation and

then been reversed in Echinozoa, or crinoids and Asterozoa

have independently inverted part of their genome sequence.

Other Molecular Data

Scouras and Smith (2001) used amino acid and sequence

data of the cytochrome oxidase gene complex to explore

echinoderm relationships. The ophiuroid sequence was unfortunately

very strongly divergent, and although they were

able to demonstrate the monophyly of Eleutherozoa, they

were unable to resolve interclass relationships with any statistical

confidence.

374 The Relationships of Animals: Deuterostomes

Figure 22.6. Phylogenetic relationships of the major clades of Ambulacraria. (A) Tree derived

from Bayesian inference of complete large subunit (LSU) ribosomal rRNA and partial small

subunit (SSU) ribosomal rRNA sequences of the 59 taxa whose complete large subunit (LSU)

ribosomal rRNA sequences are known (the matrices can be found at http://puffin.nhm.ac.uk:81/

iw-mount/default/main/Internet/WORKAREA/palaeontology/Web-Site/palaeontology/I&p/abs/

abs.html). Bayesian inference analysis used the following parameters: nst = 6, rates = invgamma,

ncat = 4, shape = estimate, inferrates = yes, basefreq = empirical, which corresponds to the GTR +

I + G model. Posterior probabilities were approximated using more than 200,000 generations via

four simultaneous Markov chain Monte Carlo chains with every 100th tree saved. Nodal support

is shown, estimated as posterior probabilities (Huelsenbeck et al. 2001). (B) Tree derived from

parsimony analysis of the combined complete LSU ribosomal rRNA and partial SSU ribosomal

rRNA sequences and morphological data (all data can be found at the web site noted above noted

above). Consensus sequences were constructed for each echinoderm class with positions that vary

in base composition within each class scored with the international nucleotide code to reflect this

uncertainty. Bremer support values are given for each node.

Branchiostoma

Styela

Herdmania

Cephalodiscus

Harrimania

Saccoglossus

Balanoglossus

Ptychodera

Glossobalanus

100

100

100

100

100

100

100

100

100

100

93

100

100

100

100

10 changes

Hemichordates

Echinoderms

Crinoids

Asteroids

Ophiuroids

Holothurians

Echinoids

Branchiostoma

Herdmania

Cephalodiscus

Harrimania

Saccoglossus

Ptychodera

CRINOID

ASTEROID

OPHIUROID

HOLOTHURIAN

ECHINOID

50 changes

29

36

17

4

14

20

16

29

A B

From Bilateral Symmetry to Pentaradiality 375

In conclusion, there is strong support from both morphological

and molecular data for the monophyly of Echinodermata

and for a basal crinoid-eleutherozoan split. Within

Eleutherozoa, all molecular data support a pairing of Echinoida

and Holothuroida, and there is also some morphological data

to support the monophyly of Echinozoa, as well, depending

upon how one interprets certain structures. The ophiuroidasteroid-

echinozoan trichotomy remains the most difficult to

resolve, but both morphology and molecular data point to an

ophiuroid-echinozoan sister group (Cryptosyringida), albeit

with a reduced level of statistical support.

Relationships within Echinoderm Classes

There are marked differences as to how well we currently

understand relationships of the families and higher taxa

within each of the five classes. This only partially reflects the

amount of work that has been carried out, because there is

also variation in how well morphological and molecular estimates

agree. Both morphological and molecular phylogenies

are well advanced and show a high degree of congruence in

echinoids, for example, whereas relationships of the major

clades of asteroids remain highly problematic, with different

data sets giving highly conflicting results.

Crinoids

The basic taxonomy of crinoids that we have today is founded

on the monographic efforts of A. H. Clark and A. M. Clark

(Clark 1915–1950, Clark and Clark 1967). The group is

relatively small with approximately 560 extant species. Of

these, more than 500 belong to the free-living Comatulida,

the remainder being stalked crinoids that are rarely encountered

and because they are entirely deep-water creatures today.

Although workers continue to add to our understanding

of the species-level taxonomy, surprisingly little progress

has been made in unraveling the relationships of the major

crinoid lineages. The principal cladistic analysis for the group

remains that of Simms (1988, 1999; fig. 22.8). According

to Simms, crown-group diversification started in the Early

Mesozoic (~250 Mya). He recognized two major groups,

Millericrinida and Isocrinida. These two groups differ from

their Paleozoic antecedents in having the axial nerves buried

within the skeleton of the cup and in having pinnulate

arms. Of the two groups, the obligate deep-sea millericrinids

are less common today. Isocrinida include both the stemmed

deep-sea isocrinids and the very much more diverse shallowwater

commatulids. Commatulids are stemless as adults and

are primarily reef dwellers, having undergone a major radiation

since the Mesozoic. Isocrinidans are characterized by

having synarthrial columnal articulations and, except for the

deep-water bourguetticrinids, all also possess fingerlike cirri

for gripping the seafloor.

Crinoids were a major constituent of benthic faunas in the

Paleozoic, appearing first in the earliest Ordovician and remaining

diverse through to the Permian. Four major groups existed

throughout this period, one of which (the Cladida) gave rise

to modern crinoids. An excellent summary of crinoid biology

and palaeontology is given in Hess et al. (1999).

There are no detailed molecular studies of crinoid relationships

available as yet, although one is currently being

undertaken (M. Ruse, pers. comm.).

Asteroids

This is the second largest of the echinoderm classes, composed

of some 1400 species. There is little consensus at

present about the phylogenetic framework for asteroid orders.

The morphological analyses of Gale (1987) and Blake

(1987) used data from both extant and extinct asteroids but

disagreed about key character polarities and character definitions

(fig. 22.9). A more extensive reappraisal of the morphological

data that takes into account the rival views of

character scoring is urgently needed.

The molecular analyses all suffer to a greater or lesser

extent from limited taxonomic sampling and long-branch

Figure 22.7. Mitochondrial gene order in echinoderms. The

gray zones in the mitochondrial gene represent the variable

region. Arrows indicate transcription polarity (after Scouras and

Smith 2001).

376 The Relationships of Animals: Deuterostomes

usually creep along the ground on a well-developed sole.

Dendrochirotids include the most heavily plated of holothurians

and have branched, dendritic feeding tentacles without

ampullae that can be retracted into an oral introvert. This

group is split into two orders, Dactylochirotida and Dendrochirotida,

differing in how branched the tentacles are and in

the structure of the calcareous ring. Finally, Molpadiida have

10 or 15 simple tentacles and the posterior end of the body

is narrowed into a “tail.” A useful introduction to the group

can be found in Kerr (2003).

The accepted view was that the heavily plated dendrochirotids

represented the most primitive holothurians (e.g.,

Pawson 1966). However, this view has recently been overturned,

and the recent cladistic analysis of the 25 extant

families based on 47 morphological characters by Kerr and

Kim (2001) has now placed holothurian relationships on

a much firmer footing (fig. 22.10). They found strong

support for the monophyly of four of the six orders (Apodida,

Elasipoda, Aspidochirotida, and Dactylochirotida) but

found Dendrochirotida to be paraphyletic, with Dactylochirotida

nested inside. The class is rooted on Apodida. A

second, more detailed analysis of the genera within the three

families of Apodida has also been carried out (Kerr 2001).

This again found that the current taxonomic classification

consisted of a mixture of paraphyletic and monophyletic

groups.

Few molecular sequence data are currently available to

test this phylogeny (Smith 1997, Kerr and Kim 1999). Complete

18S rRNA sequences are available for six holothurians

(representing four of the six orders), and these generate a

phylogeny fully congruent with the morphology-based tree

(fig. 22.10). The basal position of Apodida in phylogenies is

particularly robust based on molecular data.

Although the fossil record of holothurians is poor compared

with that of other echinoderm groups, isolated body

wall spicules recovered from sedimentary samples are frequently

encountered and can be used to deduce much about

the timing of appearance of holothurian groups in the fossil

record Gilliland (1993). Kerr and Kim (2001) found a good

match between their phylogeny and the stratigraphic record

based on spicules.

One of the most interesting outcomes of this work is that

the holothurian crown group appears to be considerably

older than the crown group of any other echinoderm class.

Holothurians are the only class in which undisputed crowngroup

clades appear well before the end of the Paleozoic, and

the dichotomy between Apodida and other holothurians has

a Bremer support more than twice the value at which the

clades within other classes collapse to a polytomy.

Ophiuroids

Ophiuroids are the most diverse of extant classes, with around

2000 extant species. Despite this diversity, many workers

follow Mortensen (1927) in recognizing just two orders,

Euryalina for forms with arm ossicle articulations that are hour-

Figure 22.8. Cladogram for crinoids based on morphological

analysis (after Simms 1999).

problems. Lafay et al. (1995) used partial 28S rRNA gene

sequence data for nine asteroids and found almost no information

about ordinal relationships. Wada et al. (1996) used

12S and 16S rDNA in combination to investigate phylogenetic

relationships. Collapsing branches with less than 50%

bootstrap support in the Wada et al. topology produces a

topology congruent with that of Lafay et al. (1995) except

for the placement of Crossaster. Smith (1997) reanalyzed the

data for the two genes separately and combined with 28S

rRNA data. Knott and Wray (2000) sequenced a large number

of species for two mitochondrial genes (tRNA and COI)

and analyzed these both separately and combined with previous

data. Finally, Janies (2001) has provided a number of

new asteroid 18S rDNA sequences carried out new methods

of analysis. It is difficult to see any common thread emerging

from this work. Forcipulatids appear to be monophyletic,

but most other major traditional groupings were not

recovered in the analyses of Janies or Knott and Wray

(fig. 22.9). Furthermore, different methods of analysis give

very different groupings. It would appear, therefore, that

there is very little signal in the molecular data currently available

with which to resolve asteroid relationships. Even the

question of whether Paxillosida is basal or not remains ambiguous

based on molecular data. Asteroids have a rather

poor and patchy fossil record. The earliest asteroids come

from the basal Ordovician (Smith 1988). However, it is clear

that the modern crown group asteroids arose in the early part

of the Mesozoic and that, like other groups, the major orders

had become established by the Middle Jurassic.

Holothurians

Until very recently holothurians remained the most poorly

known of the echinoderm classes. Twenty-five families in six

orders are currently distinguished based on body form

spiculation. Apodidans are slender wormlike forms that lack

tube-feet and respiratory trees. The body wall is thin, and

its spicules are wheel-shaped ossicles that are present

throughout life (Chirodotidae and Myriotrochidae) or in

larvae only (Synaptidae). Similar ossicles are found in the

extinct ophiocistioids. Elasipodans are entirely deep-water

forms and include the only holopelagic (swimming) echinoderm.

They often have highly modified dorsal tube-feet

that are fused to form curtainlike structures. Aspidochirotidans

have shieldlike tentacles with internal ampullae and

From Bilateral Symmetry to Pentaradiality 377

Figure 22.9. Alternative phylogenetic hypotheses for asteroids.

glass-shaped (streptospondyline), and Ophiurina for forms

with a peg-and-socket-type articulation between arm ossicles

(zygospondyline). The former group includes both simplearmed

forms and the basket stars with branched arms and has

long been considered primitive with respect to Ophiurina.

Smith et al. (1995b) undertook a cladistic analysis of the

27 extant families that confirmed the paraphyletic nature of

Euryalina. This suggested that, although the multiarmed basket

stars (Gorgonocephalidae and Euryalidae) from a clade

together with certain simple-armed forms, Ophiomyxidae

were a more derived clade and sister group to Ophiurina,

whereas Ophiocanops might be sister group to all other extant

ophiuroids.

Smith et al. (1995b) also used partial 28S rRNA sequence

data from 10 representative taxa to test the morphological

hypothesis. Unfortunately, no simple-armed euryalinans were

included, and the resultant trees had most internal nodes rather

poorly supported. Subsequently, both Ophiomyxa and Ophio-

Pseudarchasterinae

Archasteracea

Odontasteracea

Ganeriacea

Goniasteracea

Ophidiasteracea

Oreasteracea

Benthopectinidae

Radiasteridae

Astropectinidae

Luidiidae

Ctenodiscinidae

Goniopectinidae

Porecellanasteridae

Solasteridae

Korethrasteridae

Pterasteridae

Echinasteridae

Brisingida

Zorocallina

Asteriidae

Heliasteridae

Spinulosida

Paxillosida

Forcipulatida

Notomyotida

Valvatida

Velatida

Blake (1987) Gale (1987)

Archasteridae

Goniasteridae

Poraniidae

Solasteridae

Luidiidae

Pterasteridae

Echinasteridae

Zoroasteridae

Asteriidae

Heliasteridae

Spinulosida

Paxillosida

Forcipulatida

Valvatida

Velatida

Knott & Wray (2000)

Labidiasteridae

Asteriidae

Forcipulatida

Brisingidae Brisingida

Acanthasteridae

Velatida

Oreasteridae

Asterinidae

Oreasteridae

Goniasteridae Valvatida

Astropectinidae

Brissingidae

Janies (2001)

Asterinidae

Solasteridae

Labidiasteridae

Asteriidae

Pterasteridae

Echinasteridae

Heliasteridae

Luidiidae

Goniasteridae

Poraniidae

Asterinidae

Forcipulatida

Valvatida

Velatida

Brisingida

Velatida

Spinulosida

Paxillosida

Forcipulatida

Valvatida

378 The Relationships of Animals: Deuterostomes

canops have had their 18S gene sequenced, and a partial 28S

gene sequence is available for Ophiocanops. Analysis of total

molecular data confirms that Ophiocanops is the sister taxon

to the Ophiurina, but 18S rRNA data alone place Ophiocanops

and Ophiomyxa as sister taxa nested within Ophiurina (but with

low bootstrap support). Better sampling of both taxa and genes

is required to generate a more robust phylogeny for the class.

Ophiuroids first appear in the fossil record near the start

of the Ordovician, about 490 Mya, but the modern orders

all appear to stem back to a major crown-group radiation of

the class that occurred in the Late Triassic or Early Jurassic.

Echinoids

Of all echinoderm classes, the echinoids have the most detailed

and well-established phylogeny. There are about 900 extant

species equally divided between regular forms whose anus

opens in the aboral plated surface and that live epifaunally,

and irregular forms whose anus is displaced out from the aboral

plates into the posterior interambulacral zone and that live

predominantly infaunally. The most basal group is Cidaroida,

which differs from all other echinoids in having lantern muscle

attachments that are interradial in position (apophyses) and

simple ambulacral plating. Other major regular echinoid

groups have lantern muscle supports that are radial in position

(auricles), and all but Echinothurioida have soft-tissue

extensions of the internal coelom called buccal expansion sacs.

Echinothurioids, which are deep sea forms, differ further in

having an entirely flexible skeleton. The remaining regular

echinoids are divided on their tooth and lantern structure, and

on whether tubercules are perforate or imperforate. Diadematoida

and Pedinoida have simple U-shaped teeth in cross

section, like cidaroids and echinothurioids, whereas Camarodonta

and Stirodonta have teeth that are T-shaped in cross

section. Camarodonta are the more derived of the two because

they also have a fused brace in their lantern.

There are two major extant groups of irregular echinoid

alive today. One group are the heart urchins, which have

secondary bilateral symmetry and have completely lost their

lantern. Heart urchins (orders Spatangoida and Holasteroida)

are exclusively deposit feeders. The other group consists also

of deposit feeders but ones that have retained a much more

obvious pentameral symmetry. Traditionally, two orders have

been distinguished, Clypeasteroida and Cassiduloida, but the

latter is paraphyletic and requires reclassifying (Smith 2001).

Clypeasteroida includes the well-known sand dollars and

have the distinct synapomorphy of having large numbers of

tube-feet to each ambulacral plate (all other echinoids have

just a single tube-foot to each plate). Irregular echinoids first

appeared in the Early Jurassic and diversified rapidly as deposit

feeders. Clypeasteroids are the most recent group to

have arisen, first appearing about 50 Mya. A general introduction

to sea urchin morphology, biology and systematics

can be found in Smith (2003a).

In recent years, many groups of echinoid have begun to

be analyzed cladistically, and in some cases with both morphological

and molecular data (Smith, 1988, 2001, Smith

et al. 1995a, Harold and Telford 1990, Mooi and David 1996,

Jeffery et al. 2003). The primary framework for ordinal relationships

is well established through the work of Littlewood

and Smith (1995). They used a combined morphological and

molecular approach (18S and 28S rRNA gene sequences)

from a wide range of taxa to construct a phylogenetic hypothesis.

Both approaches proved closely comparable topologies,

although with some differences among the camarodont taxa

(fig. 22.11). Echinoids first appeared in the Middle Ordovician

but were never particularly diverse during the Paleozoic.

Just two lineages passed through into the Mesozoic, one of

which gave rise to modern cidaroids, and the other, to all

other extant echinoids. Most of the higher taxa were established

during the Late Triassic to Middle Jurassic.

The Importance of Ambulacraria

in Metazoan Phylogeny

The Ambulacraria hold an important position within the

Metazoa for several reasons.

(1) As the immediate sister group to chordates, Ambulacraria

provides the closest outgroup from which to establish

basal character polarities in early chordate evolution.

Significant difficulties in reconstructing the evolutionary

history of deuterostome body plans remain, yet the fact that

phylogenetic relationships among the deuterostome phyla are

now clear means that inferences about body plan changes

are on a more secure footing. For instance, it is no longer

necessary to derive the chordate body plan from precursors

with trimerous coeloms and a hydropore (see above). Likewise,

anatomical similarities in the larva shared between living

enteropneust hemichordates and eleutherozoan echinoderms

(Strathmann 1988) can no longer be taken as ancestral

features that were modified or lost during the origin of

chordates (Garstang 1928). This is not to say that we can

Figure 22.10. Morphological and molecular phylogenies for

holothurians (after Kerr and Kim 1999, 2001).

From Bilateral Symmetry to Pentaradiality 379

confidently rule out trimery or any of the other features

uniquely shared by hemichordates and echinoderms as also

being a plesiomorphic condition within the stem lineage leading

to the urochordate + chordate clade. It simply requires

positive evidence for the possession of the trait, either from

fossils or living taxa.

(2) Ambulacrarians are turning out to be crucial in developing

our understanding of the genetic basis of the evolution

of body-plans. Despite the tremendous progress of

developmental genetics during the past two decades, most

of what we know about body plan patterning still comes from

two phyla: arthropods and chordates. Echinoderms (and, increasingly,

hemichordates) have emerged as a crucial group

for studying the evolution of the developmental mechanisms

that establish animal body plans (Wray and Lowe 2000,

Davidson 2001, Tagawa et al. 2001).

It is clear that the basic genetic mechanisms that govern

body patterning among bilaterians were already established

in the latest common ancestor of Bilateria (Gerhart and

Kirschner 1997, Peterson and Davidson 2000, Carroll et al.

2001). Furthermore, we now have a good working understanding

of the way in which the regulatory molecules that

carry out these functions operate. The transcription factors

that regulate gene expression and the signaling systems that

define the morphogenetic fields that establish the bilaterally

symmetrical body plan are reasonably well understood in

forms as distant as insects, nematodes, and mouse (Gellon

and McGinnis 1998, Carroll et al. 2001).

These genetic controls and mechanisms are also present

in the echinoderms (Davidson 2001), but the body plan that

results is drastically different. Echinoderms, with their radial

body organization, are thus likely to provide crucial evidence

as to what sort of modifications in ancient regulatory genes

are required to generate such a large shift in basic body organization

(Wray and Lowe 2000). Long and Byrne (2001)

reviewed the Hox gene clusters in the five classes of echinoderm

and identified orthologues for most of the chordate

Hox genes, and orthologues of many other crucial regulatory

genes have been identified as well. Thus, the evolutionary

modifications in developmental mechanisms that resulted

in the echinoderm body plan must have included co-option

and modification of roles and expression domains of preexisting

bilaterian regulatory genes (Wray and Lowe 2000).

Nonetheless, echinoderms do show some autapomorphic

uses of regulatory genes (Lowe and Wray 1997, Wray and

Lowe 2000), including the absence of Hox gene function in

the sea urchin embryo (Arenas-Mena et al. 2000). Therefore,

echinoderms provide a unique opportunity to investigate the

genetic basis of pattern formation and morphogenesis in the

generation of novel evolutionary structures.

(3) Echinoderms, like many animal phyla, are composed

largely of species that develop indirectly, by means of a larva

that is ecologically and anatomically distinct from the adult.

Because evolutionary changes in larval ecology occur commonly

in the echinoderm crown group, including multiple

transitions from planktotrophy to lecithotrophy and from

lecithotrophy to brooding, the group has become one of

the best studied in terms of understanding diverse aspects

of larval ecology (Hart et al. 1997, McEdward and Miner

2001). Comparisons of larval and life-history diversity have

taken advantage of the growing understanding of phylogenetic

relationships within echinoderms to formulate spe-

Figure 22.11. Morphological

and molecular phylogenies for

orders of echinoids (after

Littlewood and Smith 1995).

380 The Relationships of Animals: Deuterostomes

cific hypotheses about evolutionary history (Wray 1992,

1996).

(4) Echinoderms are the dominant component of the

macrobenthos in the deep sea, forming more than 90% of

the biomass in abyssal settings, the largest single ecosystem in

the world (Kerr and Kim 2001). Many echinoderms have a

complex endoskeleton and an excellent fossil record, making

them ideal subjects for investigating patterns and processes of

evolution within a rigorous phylogenetic framework.

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