13 The History of Animals

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Douglas J. Eernisse

Kevin J. Peterson

197

This is an exciting time for zoologists. A dramatic upsurge

in interest in the interrelationships among animals has occurred

across the biological subdisciplines; before the last

decade, the topic of high-level animal relationships was one

largely confined to zoological texts and older monographs.

Revolutionary advances in the fields of phylogenetic analysis,

paleontology, developmental biology, and microscopic

anatomy, combined with a new wealth of relevant data such

as DNA and protein sequences, have led to new insights into

animal genealogy. These insights are crucial in this era of

“omics”: a deeper understanding of any process, including

molecular processes, requires an understanding of the underlying

pattern, particularly the phylogenetic topology of

the systems under consideration.

One of the most significant changes to occur with our

understanding of animal evolution is the recognition that

animals should be arranged on a phylogenetic tree, and ancestors

inferred from character states, rather than the ladderlike

progression from protozoans to mammals with ancestors

inferred from “archetypes.” Despite this new appreciation for

the necessity of phylogenetic patterns, it is important to emphasize

that even if the topology were somehow precisely

known, there would still be uncertainties concerning the

appearance or life history attributes of many ancestral metazoan

taxa, to say nothing of gene regulatory networks and

molecular cascades.

What follows is our attempt to synthesize what is known

about high-level (i.e., interphylum) animal relationships,

including the controversies that surround some of the crucial

cladogenic events. We start from the base of the animal

tree and proceed to the individual subclades of bilaterian

metazoans, with the latter summarized only briefly because

these topics are considered in much greater detail elsewhere

in this book. Controversies still remain, but it is also true that

agreement among zoologists has never been greater; the basic

pattern of animal evolution has largely been resolved into

a few major lineages. This congruence is shown in figure 13.1.

Figure 13.1A summarizes where the field is with respect to

animal interrelationships. This by necessity is a very conservative

tree with many polytomies, yet compared with the state

of the field just 15 years ago, we have made remarkable

progress, and we expect that most of these polytomies will

be resolved with the wealth of data being generated. Figure

13.1B is our total-evidence tree, where we combined our

morphological data matrix (modified from Peterson and

Eernisse 2001) with 335 small subunit (SSU) or 18S ribosomal

DNA (rDNA) sequences, and 43 myosin heavy chain type

II inferred amino acid sequences (details are provided in the

appendix). The common names of many of these taxa are

given in table 13.1, as is the number of SSU rDNA and myosin

II sequences analyzed for each taxon, and the Bremer

support index for selected nodes of interest. Although our

data set is able to resolve all of the polytomies, many with

high Bremer support (table 13.1), these should be viewed as

tentative hypotheses rather than a consensus among workers

in the field. We now discuss the interrelationships of the

198 The Relationships of Animals: Overview

major animal groups; the reader should refer to figure 13.1

and table 13.1 throughout the remainder of the chapter to

see the branching patterns discussed in each section and to

compare the consensus nodes with those that are more

equivocal.

Are Metazoans Monophyletic?

Until just recently, it seemed possible that sponges arose

independently from unicellular ancestors different from those

giving rise to all other animals. However, it is now clear from

both morphological and molecular analyses that all multicellular

animals, including sponges, are monophyletic. The

morphological evidence for monophyly consists of many

derived attributes that co-occur with the origin of multicellularity

at the base of Metazoa (“Met” in fig. 13.1B), including

the presence not only of multicellularity but also of the

extracellular matrix (Morris 1993) and septate junctions

(Nielsen 2001), as well as reproductive features such as eggs

with polar bodies and spermatozoa. Furthermore, the molecular

support extends beyond SSU rDNA (e.g., Wainright

et al. 1993) to include combined SSU rDNA and large subunit

(LSU, or 28S) rDNA (Medina et al. 2001), heat-shock

protein HSP70 (Borchiellini et al. 1998, Snell et al. 2001),

the largest subunit of RNA polymerase II (Stiller et al. 2001,

Stiller and Hall 2002), and EF-2 and b-tubulin proteins (King

and Carroll 2001). Because the monophyly of Metazoa is

robust, multicellularity evolved just once within the animal

lineage.

Figure 13.1. The interrelationships among major animal groups. (A) The consensus view from

the literature. Although the general structure is apparent, there are several places where much

controversy (and work) exists, including the base of Eumetazoa, and especially among the

lophotrochozoan taxa. (B) Summary of our combined data set analysis of metazoans. This is the

strict consensus summary of first 2000 most parsimonious trees (1115 parsimony-informative

characters for 337 taxa, including two with only morphology data; branch length, L = 12,700).

To simplify results, the resolution of some terminal taxa scored and analyzed separately are not

depicted (see text for details). Bremer support indices and the number of taxa analyzed for SSU

rDNA and myosin II are given in table 13.1. Some selected nodes have been labeled with a threeletter

taxon abbreviation: Ani, Animalia; Bil, Bilateria; Eum, Eumetazoa; Lop, Lophophorata; Met,

Metazoa; Neo = Neotrochozoa; Nep = Nephrrozoa; Spi, Spiralia; Tro, Trochozoa. Nexus format

data matrices, search blocks, and full consensus tree descriptions as well as details of sequences

analyzed are available from D.J.E.

Fungus

Choanoflagellates +

Mesomycetozoans

Siliceans

Calcareans

Ctenophores

Cnidarians

Placozoans

Acoels

Nemertodermatids

Gastrotrichs

Rotifers

Gnathostomulids

Chaetognaths

Onychophorans

Tardigrades

Arthropods

Nematomorphs

Nematodes

Priapulids

Kinorhynch

Loricifera

Chordates

Echinoderms

Hemichordates

Phoronids

Brachiopods

Ectoprocts

Catenulid

Rhabditophorans

Cycliophoran

Entoprocts

Nemerteans

Molluscs

Sipunculans

Echiurans

Annelids

"Sponges"

Ecdysozoans

Deuterostomes

Lophotrochozoans

Acoelomorphs

B Neo

Spi

Lop

Bil

Nep

Eum

Met

Ani

Tro

Fungi

Choanoflagellates

Siliceans

Calcareans

Ctenophores

Placozoans

Cnidarians

Acoels

Nemertodermatids

Chaetognaths

Gastrotrichs

Rotifers

Gnathostomulids

Nematodes

Priapulids

Panarthropods

Chordates

Echinoderms

Hemichordates

Brachiopods + Phoronids

Ectoprocts (Bryozoans)

Platyhelminths

Nemerteans

Molluscs

Sipunculans

Annelids + Echiurans

A

"Sponges"

Ecdysozoans

Deuterostomes

Lophotrochozoans

Acoelomorphs

Nep

Bil

Met

Ani

The History of Animals 199

Although animal monophyly is firmly established, controversies

still remain. One crucial issue relates to whether

particular features shared by sponges and all other animals

are truly derived for animals or whether they could be more

primitive (i.e., found outside of Metazoa). A good example

is the presence of receptor tyrosine kinases, a group of molecules

involved in cell–cell signaling and thought to be apomorphic

for Metazoa (Suga et al. 1999). King and Carroll (2001)

recently found a receptor tyrosine kinase in the choanoflagellate

Monosiga, raising the possibility that many molecules

(including those involved in such traditional multicellular

activities as cell-to-cell communication and development)

currently thought to exist only in animals (and known to be

absent in fungi) might be present in choanoflagellates as well.

This problem is not restricted to choanoflagellates: the absence

of molecules that characterize higher level metazoan groups

in “poriferans” is often the result of negative PCR experiments,

and until we have a genome sequence from a sponge,

all absences fall into the category of “absence of evidence”

rather than the preferable “evidence of absence.” As a point

in fact, nerve cell genes such as Pax transcription factors have

recently been isolated in sponges (Grцger et al. 2000), suggesting

that they might be much more complex than usually

presupposed (e.g., Mьller 2001).

What Is the Sister Taxon of Metazoans?

Molecular data support the monophyly of a subclade of eukaryotes

called Opisthokonta (Baldauf and Palmer 1993,

Baldauf et al. 2000, Atkins et al. 2000, Zettler et al. 2001; see

Loytynoja and Milinkovitch 2001), which includes metazoans,

choanoflagellates, fungi, and several other poorly

known unicellular eukaryotic taxa. Within Opisthokonta,

metazoans and choanoflagellates appear quite closely related

compared with the more distantly related fungi. The morphology

of choanoflagellates has long suggested an affinity

with animals, specifically sponges. The similarity between the

feeding “collar” cells of sponges and those single-celled but

frequently colonial choanoflagellates, first noticed more than

a century ago (James-Clark 1866, 1868), is striking, and all

morphological and molecular analyses conclude that this

similarity is not due to convergence but instead was present

in the last common ancestor of animals (“Ani” in fig. 13.1B:

Animalia = Choanoflagellata + Metazoa; Nielsen 1995).

There is also another recently recognized group, the mesomycetozoans

(alternatively known as ichthyosporeans), which

are closely related to choanoflagellates and/or metazoans.

Mesomycetozoans are parasites of various fish, birds, mammals,

and snails (reviewed in Mendozoa et al. 2002; see also

Hertel et al. 2002). In some analyses, Mesomycetozoa is resolved

as the sister taxon of choanoflagellates, whereas in others

it is the sister taxon of metazoans (Medina et al. 2001, Peterson

and Eernisse 2001). King and Carroll (2001) argued that, even

if mesomycetozoans comprise the sister taxon of metazoans,

choanoflagellates are still the most appropriate metazoan outgroups

to study because, as parasites, mesomycetozoans are

more likely to have experienced general genomic simplification

events. Nonetheless, it is prudent to include both choanoflagellates

and mesomycetozoans as outgroups when estimating

metazoan basal branching patterns. The diversity of

Table 13.1

Bremer, Support Indices (BSI) for Terminal and Selected

Higher Metazoan Taxa for Combined Analysis of Morphology,

SSU rDNA, and Myosin II Data Sets.

Taxa Common name BSI

Terminal Taxa

(No. SSU/myosin II)

Silicea (10/0) Siliceous sponges 2

Calcarea (4/0) Calcareous sponges 4

Ctenophora (3) Comb jellies 23

Cnidaria (27/3) Cnidarians 8

Placozoa (2/0) Trichoplax 22

Acoela (11/3) Acoel flatworms 28

Nemertodermatida (2/1) Nemertodermatid flatworms 37

Gastrotricha (2/0) Gastrotrichs 12

Rotifera (6/1) Rotifers 19

Gnathostomulida (3/0) Gnathostomulids 13

Chaetognatha (3/0) Arrow worms 15

Onychophora (2/0) Velvet worms 27

Tardigrada (6/0) Water bears 18

Arthropoda (47/9) Arthropods 1

Nematomorpha (3/0) Horsehair worms 14

Nematoda (17/3) Round worms 20

Priapulida (6/1) Priapulids 4

Kinorhyncha (1/0) Kinorhynchs —

Loricifera (0/0) Loriciferans —

Chordata (24/6) Chordates 5

Echinodermata (6/0) Echinoderms 12

Hemichordata (6/0) Hemichordates 3

Phoronida (3/1) Phoronids 9

Brachiopoda (20/1) Brachiopods 10

Ectoprocta (2/0) Bryozoans 4

Catenulida (1/0) Catenulid flatworms —

Rhabditophora (38/5) Rhabditophoran flatworms 11

Cycliophora (1/0) Cycliophorans —

Entoprocta (2/0) Entoprocts 15

Nemertea (4/1) Ribbon worms 5

Mollusca (12/3) Mollusks 1

Sipuncula (7/1) Peanut worms 27

Echiura (3/1) Spoon worms 18

Annelida (39/3) Segmented worms 1

Selected higher taxa

Metazoa Multicellular animals 6

Eumetazoa Eumetazoans 6

Bilateria Bilaterians 36

Acoelomorpha Acoelomorphs 1

Nephrozoa Nephrozoans 6

Ecdysozoa Ecdysozoans 4

Deuterostomia Deuterostomes 6

Lophotrochozoa Lophotrochozoans 1

Lophophorata Brachiopods + phoronids 6

Spiralia Spiralians 1

Trochozoa Trochozoans 1

Neotrochozoa Neotrochozoans 3

200 The Relationships of Animals: Overview

choanoflagellates and mesomycetozoans is still poorly known,

and it is possible that additional opisthokont taxa will be discovered

(Moon-van der Staay et al. 2001).

Are Sponges Monophyletic?

Porifera is usually assumed to be monophyletic, and this notion

is supported by their possession of the water-canal system,

a unique arrangement of canals and pores not found in

other metazoans. Nonetheless, recent analyses of SSU rDNA

that have included an appropriate assortment of sponges, other

animals such as cnidiarians, and non-metazoan outgroups have

instead found sponges to be paraphyletic (e.g., Borchiellini et al.

2001, Peterson and Eernisse 2001, Medina et al. 2001). In

particular, those sponges whose skeleton is composed of calcareous

spicules (Calcarea) have been supported as comprising

the sister taxon of Eumetazoa (“Eum” in fig. 13.1B), the

clade composed of all “nonsponge” metazoans, whereas the

remaining sponges with a skeleton composed of siliceous spicules

(Silicea) comprise the monophyletic sister taxon of the

Calcarea + Eumetazoa clade. If the recent SSU rDNA analyses

are accurate, then the name “Porifera” should be abandoned

and replaced by Calcarea and Silicea. The controversy has important

implications. Sponge paraphyly would simplify the

optimization of ancestral conditions in ancient metazoans because

then the last common ancestor of eumetazoans and

calcareans would be more confidently spongelike, complete

with a water-canal system. This is because the most proximal

outgroup to the Calcarea + Eumetazoa clade, Silicea, also has a

water-canal system indistinguishable from the calcarean watercanal

system. Furthermore, sponge paraphyly would suggest

that the last common ancestor of all animals had a water-canal

system as well, and that the acquisition of a spongelike body

plan occurred during the early evolution of metazoans and was

lost early in the evolution of eumetazoans. Despite the prevailing

textbook view of sponge monophyly, as well as our morphology-

only analysis (Peterson and Eernisse 2001), sponge

paraphyly is consistent with the presence of cross-striated rootlets

in calcareous sponges and eumetazoans, but not in siliceous

sponges or choanoflagellates (Nielsen 2001). Even if sponges

are monophyletic, the near certain monophyly of metazoans

and the placement of spongelike choanoflagellates as a near

outgroup together imply that our ancient ancestors were

“sponges.” If living sponges represent a paraphyletic grade, not

a clade, of basal metazoans, then the similarities between Silicea

and Calcarea reflect only what they lack: the derived traits associated

with the eumetazoan body plan.

What Are the Basal Relationships

within Eumetazoa?

As for Metazoa, the monophyly of Eumetazoa is strongly

supported by morphological evidence. Eumetazoans have

clear body symmetry (either radial or bilateral), a mouth and

gut, a nervous system, and tissues with characteristic organization,

including a basement membrane layer as well as gap

junctions and belt desmosomes, all of which are lacking in

sponges (Nielsen 2001). Eumetazoa consists of four monophyletic

groups whose interrelationships are still unresolved:

Cnidaria (anemones and jellies), Ctenophora (comb jellies),

Placozoa (a taxon of simple two-layered animals represented

by the genus Trichoplax), and Bilateria (i.e., all remaining

eumetazoans, which primitively have bilateral symmetry; also

referred to as the triploblasts because of their three-layered

bodies).

Although cnidarians, like sponges, have been popularly

represented as models for our ancient ancestors, there is a

fundamental difference: unlike sponges, there is substantial

molecular evidence for cnidarian monophyly (Collins 2002).

This is consistent with various morphological synapomorphies

(Schuchert 1993), including their unique production

of nematocysts, extracellular encapsulated structures that

cnidarians produce in association with their predatory feeding

(Tardent 1995). Also unequivocal is the close relationship

between cnidarians and bilaterians to the exclusion of

the sponges.

What is equivocal is how ctenophores and placozoans

fit into the eumetazoan topology. SSU rDNA studies often

find that ctenophores group either with the calcareous

sponges (e.g., Wainright et al. 1993, Cavalier-Smith et al.

1996, Collins 1998, Kim et al. 1999, Medina et al. 2001,

Podar et al. 2001) or basal to calcareous sponges and the

remaining eumetazoan taxa (e.g., Peterson and Eernisse

2001), resulting in a paraphyletic Eumetazoa. In contrast,

morphological studies have strongly supported ctenophores

as comprising the sister taxon of bilaterians (Nielsen et al.

1996, Zrzavэ et al. 1998, Peterson and Eernisse 2001). The

almost insurmountable difficulty with clade Ctenophora +

Calcarea is that complex systems like the nervous system, in

addition to many other characters such as tissues, must have

evolved twice, once in ctenophores and once in the remaining

eumetazoans (or secondarily lost in calcareous sponges),

a conclusion advocated by Cavalier-Smith et al. (1996).

When a combined analysis of morphology and SSU rDNA

sequence data is attempted, the multiple morphological

synapomorphies for Eumetazoa, as well as the few supporting

Ctenophora + Bilateria, cancel out the SSU rDNA synapomorphies

such that neither cnidarians nor ctenophores are

robustly supported as comprising a sister taxon of bilaterians

(e.g., Peterson and Eernisse 2001). In fact, our new combined

analysis (fig. 13.1B) finds a topology distinct from, but influenced

by, both data sets: Eumetazoa is monophyletic, but

ctenophores are basal to the remaining eumetazoans. This

placement is also consistent with newly emerging data on Hox

and Parahox genes, which appear to support a basal eumetazoan

position because ctenophores seem to lack most, if not

all, of these genes (Martindale et al. 2002). As above, we

emphasize that this absence might not be primary because it

The History of Animals 201

is a possible secondary loss or merely absence due to methodological

problems.

Placozoans are equally problematic. As discussed above,

molecular results tend to suggest an affinity with either

bilaterians or (more rarely) cnidarians, whereas morphologists

and morphological cladistic analyses have favored a basal

position among eumetazoans (Bonik et al. 1976, Grell and

Ruthmann 1991, Nielsen et al. 1996, Collins 1998, Zrzavэ

et al. 1998, Peterson and Eernisse 2001). A position within

Cnidaria, specifically within the Medusazoa (sensu Collins

2002; e.g., Bridge et al. 1995) is convincingly rejected by

Ender and Schierwater (2003), who show that placozoans

have a normal circular mitochondrial genome, not the derived

linear version known exclusively from medusozoans.

Contrary to morphology, analysis of SSU rDNA suggests a

more apical position for placozoans, often as comprising the

sister taxon of Bilateria, and the addition of morphology does

not change this result (fig. 13.1B). Therefore, their simplicity

might be better explained by reduction from a more complex

body plan than by primitive simplicity relative to the

other more complex eumetazoan taxa.

Resolving the interrelationships among eumetazoans is

crucial because only by doing so will we elucidate which

eumetazoan subgroup is the sister group of bilaterians. It

appears that comparisons with cnidarians will remain most

productive (Martindale et al. 2002) even should placozoans

be found more proximal to bilaterians than are cnidarians.

This is because of the similarities between cnidarians and

bilaterians in developmental complexity and because the

placozoan body plan is likely highly reduced.

Bilaterian Relationships

Of all the nodes found on the metazoan tree, none are more

strongly supported than the monophyly of Bilateria (“Bil” in

fig. 13.1B). Characters supporting the monophyly of Bilateria

include (1) distinct anterior-posterior, dorsoventral, and left

right axes [but see Martindale et al. (2002) for possible antecedents

in cnidarians and ctenophores]; (2) mesoderm as a

distinct germ layer giving rise to, for example, circular and longitudinal

muscles; (3) nerves organized into distinct ganglia;

(4) an expansion of the Hox complex to include at least seven

genes; (5) the polar bodies positioned on the animal pole; and

(6) the specification of one body axis during oogenesis (Peterson

and Eernisse 2001). Two other characters, the presence of

nephridia and a through-gut with mouth and anus, depend on

the phylogenetic position of acoelomorph flatworms, as discussed

below. Hence, all morphological studies find strong

support for bilaterian monophyly (e.g., Nielsen et al. 1996,

Zrzavэ et al. 1998, Peterson and Eernisse 2001). SSU rDNA data

are equally unequivocal (reviewed in Adoutte et al. 1999, 2000),

as are myosin heavy-chain data (Ruiz-Trillo et al. 2002).

The traditional “textbook” approach to bilaterian phylogeny

is to view the evolution of the coelom as a proxy for the

evolution of bilaterians themselves. This view is traditionally

ascribed to Hyman (1940; see also Hyman 1951), who in turn

credits Schimkewitsch (1891). This is the familiar view that

acoelomate flatworms are the most basal group; then come

the “pseudocoelomates,” including nematodes, priapulids,

and most other “aschelminth” groups; and then finally the

coelomates, including arthropods, mollusks, annelids, and

chordates. Although Hyman (1940) clearly viewed this transition

as a grade of increasing complexity, not always corresponding

to phylogenetic pattern, she argued forcefully

against the notion of acoelomate and pseudocoelomate conditions

as secondarily derived. Nonetheless, the first morphological

cladistic analyses based on explicit data matrices did

not support the “Hyman” hypothesis of progressive acquisition

of a coelomic condition. Schram (1991) found the

“aschelminths” to be basal to both flatworms and coelomates,

and Eernisse et al. (1992; see also for a reanalysis of the Schram

data set) found nematodes grouping with the arthropods, and

flatworms grouping with the spirally cleaving protostomes

such as annelids and mollusks.

Nonetheless, it was not until SSU rDNA studies starting

with Field et al. (1988) that a different view of bilaterian evolution

began to emerge (Adoutte et al. 1999). Rather than viewing

bilaterian evolution as a ladder of coelomic complexity,

instead bilaterians can be divided into three major groups independent

of the presence/absence of the coelom: (1) the deuterostomes,

composed of echinoderms, hemichordates, and

chordates; (2) the lophotrochozoans (Halanych et al. 1995),

composed of lophophorates (brachiopods and phoronids),

those taxa possessing a trochophore larva (e.g., annelids, mollusks),

the catenulid and rhabidophoran flatworms, and many

other minor groups, including rotifers, cycliophorans, and

possibly gastrotrichs and gnathostomulids; and (3) the ecdysozoans

(Aguinaldo et al. 1997), composed of panarthropods,

nematodes, priapulids, and other minor aschelminth groups

such as kinorhynchs and nematomorphs. Hence, Lophotrochozoa

consists of conventional coelomate, pseudocoelomate,

and acoelomate groups, and Ecdysozoa consists of “coelomate”

groups such as arthropods and most of the pseudocoelomate

taxa. This tripartite division removes “intermediate” taxa such

that characters thought to apply only to coelomates now characterize

all bilaterians (Adoutte et al. 1999). Thus, the story

underlying bilaterian evolution seems to be one of an initial

complexity followed by numerous simplifications within Ecdysozoa

and Lophotrochozoa, as well as Deuterostomia (Takacs

et al. 2002).

Although the monophyly of each of these groups is fairly

well supported, the interrelationships among the three are

not clear. Usually, a monophyletic Protostomia is assumed,

and one character supporting this hypothesis is the presence

of the UbdA signature peptide, a stretch of about 11 amino

acids C-terminal of the homeodomains of the Ubx, Abd-A,

Lox-2, and Lox-4 Hox genes (de Rosa et al. 1999, Salу et al.

2001). However, not a single SSU rDNA study has demonstrated

any appreciable support for the monophyly of

202 The Relationships of Animals: Overview

Protostomia, nor has any other arrangement been strongly

supported.

The Deuterostomes

Traditionally, deuterostomes consisted of six taxa: echinoderms,

hemichordates, chordates, lophophorates, ectoprocts,

and chaetognaths. However, both molecular and morphological

analyses agree that lophophorates, ectoprocts, and

chaetognaths are not deuterostomes. Deuterostomia sensu

stricto consists of hemichordates and echinoderms (collectively

called ambulacrarians), and the chordates, the monophyletic

sister group of the ambulacrarians. For further

discussion of deuterostome evolution, see Smith et al. (ch. 22

in this vol.).

The Lophotrochozoa

By far the most phylogenetically challenging group is Lophotrochozoa.

Named by Halanych et al. (1995) to reflect its

primary taxonomic constituents, the lophophorates (brachiopods

and phoronids) and trochozoans (i.e., those protostome

phyla having trochophore larva, e.g., annelids and mollusks),

as well as groups such as ectoprocts that do not fit under

either category, this is by far the largest group of higher level

metazoan taxa, containing up to about 14 phyla. Furthermore,

it is the least studied group with respect to molecular

investigations, because none of its members are currently

genetic model systems. In general, we can say very little about

how lophotrochozoan phyla are related to one another. There

are few morphological characters for resolving deep-level

lophotrochozoan relationships, and there is virtually no resolution

with SSU rDNA (for discussion and references, see

Halanych 1998, Peterson and Eernisse 2001, Giribet 2002).

Analyses of LSU (Mallat and Winchell 2002) and the myosin

heavy chain (Ruiz-Trillo et al. 2002) have also failed to

provide robust and biologically reasonable interrelationships

among lophotrochozoans. Even the monophyly of some of

the more conspicuous phyla, such as Annelida and Mollusca,

is rarely recovered using molecular data.

Our best estimate of lophotrochozoan relationships divides

this group into three subgroups: lophophorates [restricted

in Peterson and Eernisse (2001) to brachiopods and

phoronids], platyzoans (rotifers, gnathostomulids, platyhelminths,

and possibly gastrotrichs; Cavalier-Smith 1998; but

see Zrzavэ et al. 2003 for gastotrichs), and the trochozoans

(entoprocts, nemerteans, annelids, mollusks, echiurans, and

sipunculans, modified from Ghiselin 1988; compare Beklemishev

1969). There is strong morphological support for the

monophyly of lophophorates (e.g., Peterson and Eernisse

2001), but the monophyly of Lophophorata, as well as the

monophyly of the remaining groups, is still under debate with

respect to molecular data. Giribet and colleagues (Giribet

et al. (2000, Giribet 2002) recovered a monophyletic Platyzoa,

as did Peterson and Eernisse (2001) in their morphological

analysis. With respect to trochozoans, all analyses

agree that these taxa are more closely related to one another

than to any platyzoan subgroup, but the interrelationships

among these taxa are obscure at the moment, as is the taxonomic

constituency of such taxa as Annelida (Halanych et al.

2002).

Morphology alone strongly suggests that lophophorates

are basal lophotrochozoans, because they lack several important

spiralian (Spiralia = Platyzoa + Trochozoa) and trochozoan

characters such as spiral cleavage and a trochophore

larval form, respectively (Peterson and Eernisse 2001). The

difficulty is that most SSU rDNA analyses place the lophophorates

within the trochozoans, often as the sister group

to a mollusk or annelid subgroup, but usually with very little

support. Nonetheless, this hypothesis is supported by the

possession of annelid-like setae in brachiopods (Ghiselin

1989). The reason the position of the lophophorates is critical

is that characters supporting the monophyly of Lophotrochozoa

depend heavily on the relative position of

lophophorates. If Lophophorata is nested within Trochozoa,

then all of the traditional developmental characters, such as

spiral cleavage and the possession of a prototroch, would

constitute basal lophotrochozoan characters (with the interesting

by-product of making Lophotrochozoa equivalent

to Spiralia). As Giribet (2002) pointed out, Halanych et al.

(1995) did not include any platyzoans in their original analysis

when first diagnosing Lophotrochozoa, so the potential

membership of platyzoans in Lophotrochozoa must depend

on their position relative to lophophorates. If lophophorates

are basal to Spiralia, then the only nonsequence characters

presently supporting the monophyly of Lophotrochozoa are

the possession of two Abd-B Hox genes, post-1 and post-2 (see

Callaerts et al. 2002; note that this is known for only brachiopods,

annelids, and mollusks), and the Lox-5 signature

peptide, a stretch of eight amino acids C-terminal of the

homeodomain of the Lox5 gene, known in platyhelminths,

nemerteans, annelids, brachiopods, and mollusks (de Rosa

et al. 1999, Salу et al. 2001, reviewed in Balavoine et al. 2002).

Although there are several other lophotrochozoan taxa,

such as the ectoprocts, virtually nothing can be said about how

they fit into the lophotrochozoan tree. One of the problems is

that sequences for these taxa have been few and taxonomic

sampling has been sparse. In some cases (e.g., ectoprocts), this

can be easily remedied. In other cases (e.g., cycliophorans),

there are relatively few extant species to sample, so multiple

gene sequence comparisons are more apt to help.

The Ecdysozoa

Perhaps the most surprising result of SSU rDNA analyses was

the formulation of Ecdysozoa by Aguinaldo et al. (1997).

Instead of using long-branch nematode taxa like Caenorhabditis

elegans, Aguinaldo et al. (1997) found shorter branched

taxa that, when analyzed phylogenetically, grouped robustly

with arthropods. This was unusual given that all previous

The History of Animals 203

analyses found nematodes to be basal bilaterians, supporting

the traditional notion of a basal Pseudocoelomata (e.g.,

Winnepenninckx et al. 1995). Since Aguinaldo et al.’s (1997)

analysis, numerous SSU rDNA studies (e.g., Giribet et al.

2000, Peterson and Eernisse 2001) have found strong support

for a clade consisting of panarthropods, nematodes,

nematomorphs, priapulids, kinorhynchs, and loriciferans

(assumed, based on morphology alone, to be closely related

to kinorhynchs and priapulids). Moreover, the monophyly

of Ecdysozoa is further supported by phylogenetic analyses

of LSU (Mallatt and Winchell 2002) and myosin heavy chain

(fig. 13.1B; Ruiz-Trillo et al. 2002). In addition, a monophyletic

Ecdysozoa is recovered using morphological data (Zrzavэ

et al. 1998, Peterson and Eernisse 2001); ecdysozoans share

similarities in their cuticle and ecdysis pathways (Schmidt-

Rhaesa et al. 1998), a terminal mouth, a distinct Abd-B gene

(Van Auken et al. 2000), an internal triplication within the

[-thymosin gene (Manuel et al. 2000), neural expression of

horseradish peroxidase (HRP) immunoreactivity (Haase et al.

2001), the absence of cannabinoid receptors (McPartland

et al. 2001), and the absence of the Parahox gene Xlox (Ferrier

and Holland 2001)]. They might also share similarities in

their circumpharyngeal brain (Eriksson and Budd 2000).

Thus, the monophyly of Ecdysozoa is recovered using a variety

of data sets (fig. 13.1).

Both morphological and molecular analyses agree on

the monophyly of the three main Ecdysozoan groups: (1)

Scalidophora (Lemburg 1995, Schmidt-Rhaesa et al. 1998,

also referred to as Cephalorhyncha by some authors), consisting

of priapulids, kinorhynchs and loriciferans; (2)

Nematoida (Schmidt-Rhaesa 1996), consisting of nematodes

and nematomorphs; and (3) Panarthropoda (Nielsen 1995),

consisting of arthropods, onychophorans, and tardigrades.

However, the interrelationships among these three groups

are unclear.

The Chaetognath Problem

One of the more difficult groups to place phylogenetically is

Chaetognatha. Chaetognaths show an odd mix of deuterostome

and aschelminth-type characters (Hyman 1959), but

because preference was usually given to embryological characters,

chaetognaths were traditionally one of the six major

deuterostome groups. Initial studies based on cladistic arguments

found grouping with either deuterostomes (e.g.,

Brusca and Brusca 1990) or aschelminths (Schram 1991).

Initial SSU rDNA analyses (Telford and Holland 1993, Turbeville

et al. 1994, Wada and Satoh 1994; see also Giribet et al.

2000) did not support a placement within Deuterostomia but

could not place them with any significant support elsewhere

within Bilateria. Halanych (1996) argued that they were the

sister group of the nematodes and argued that this was not

due to long-branch attraction. More recent analyses seemed

to confirm a placement within Ecdysozoa (e.g., Peterson and

Eernisse 2001). Morphological analyses alone also suggest

that chaetognaths are basal ecdysozoans (Peterson and

Eernisse 2001, Zrzavэ et al. 2001), sharing with Ecdysozoa

proper a terminal mouth, possibly a chitinous cuticle, absence

of a ciliated epidermis, absence of an apical organ, and

other larval structures, and they share with nematoidans the

absence of circular muscles. A basal position to Ecdysozoa

sensu stricto is also supported by the absence of HRP immunoreactivity

in the chaetognath nervous system (Haase et al.

2001).

It has recently been shown that two characters usually

given for a deuterostome affinity were misunderstood in

chaetognaths. First, the presence of a trimeric arrangement

of the coeloms is at best questionable in chaetognaths because

the septum that divides the trunk into anterior and

posterior compartments is not a primary septum but a secondary

division derived from coelomic cells (Kapp 2000).

Second, radial cleavage does not occur in chaetognaths. Instead,

they have a tetrahedral four-cell embryo whose cleavage

planes are similar to those of crustacean arthropods and

nematodes (Shimotori and Goto 2001), and also comparable

with the Precambrian embryos described by Xiao et al.

(1998). The remaining deuterostome characters, for example,

mouth not derived from blastopore, may represent bilaterian

plesiomorphies (Peterson and Eernisse 2001). Thus, all available

evidence points to an affinity with ecdysozoans, but

where they fall within this group remains speculative at best.

Because chaetognaths have the most strongly guanine +

cytosine–biased sequences among all animal SSU rDNA sequences

sampled to date (Peterson and Eernisse 2001), it

would be desirable to test this hypothesis with amino acid

comparisons instead of (or in addition to) the traditional SSU

rDNA or LSU analyses.

The Acoelomorph Problem

One of the more interesting results to emerge from SSU rDNA

analyses is the purported basal position of acoelomorph flatworms

(Ruiz-Trillo et al. 1999, Jondelius et al. 2002), a placement

that could shed much light on the plesiomorphic state

of the early bilaterians (e.g., Ruiz-Trillo et al. 1999, 2002,

Adoutte et al. 2000, Jondelius et al. 2002). Acoelomorphs

(collectively the acoel and nemertodermatid flatworms) were

conventionally considered basal platyhelminths because they

possess neoblasts, a unique stem cell found only in flatworms

(Ax 1996, Gschwentner et al. 2001, Ramachandra et al.

2002), and morphology-alone analyses confirm a flatworm

affinity (e.g., Peterson and Eernisse 2001). Because of their

possession of neoblasts, a basal position within Bilateria appeared

suspicious, a suspicion that seemed justified given

that acoels were also very long-branched taxa (Adoutte et al.

2000, Peterson and Eernisse 2001). Peterson and Eernisse

(2001) tested this hypothesis and found that acoels strongly

attract random DNA sequences and, to the extent that distant

outgroups such as cnidarians might be behaving effectively

as random sequences, their attraction to a basal position

204 The Relationships of Animals: Overview

was considered to be potentially artifactual. In contrast, the

internal branch between protostomes and deuterostomes was

never attracted to random outgroups, yet that is where the

root attached when acoelomorphs and selected other taxa

subject to long-branch attraction were removed.

Nevertheless, Ruiz-Trillo et al. (2002) analyzed myosin

heavy-chain type II sequences from a variety of bilaterians,

including acoelomorphs, and similar to their SSU rDNA result,

found acoelomorphs to be basal bilaterians. Consistent

with these results, our total-evidence tree also finds a basal

Acoelomorpha (fig. 13.1B). A basal position is only moderately

less consistent with the morphological data: placing

acoelomorphs basally adds only four steps to the analysis.

Furthermore, Salу et al. (2001) reported that they were unable

to find more than three Hox/ParaHox genes in the acoels

Paratomella and Convoluta, and these observations are consistent

with the basal bilaterian position supported for

acoelomorphs based on available sequence data sets. Therefore,

Jondelius et al. (2002) proposed the name Nephrozoa

(“Nep” in fig. 13.1B; reflecting the evolution of nephridia)

to include the last common ancestor of all bilaterians except

acoelomorphs and all descendants of that last common ancestor

living or extinct. Nephrozoa would also be characterized

by the possession of a through-gut, complete with

mouth and anus, which was most likely lost secondarily in

platyhelminths (now restricted to exclude acoelomorphs).

The Biology of the Earliest Bilaterians

The implications for a basal position of Acoelomorpha (or

“acoelomorph” grade) are striking. Baguса et al. (2001) proposed

that if their mode of development is primitive then it

is likely that the earliest bilaterians were small, benthic, directly

developing animals without a coelom, segments, a true

brain, or nephridia. Of their conclusions, the proposed lack

of a true brain in the earliest bilaterians might need reconsideration

in light of the recently demonstrated brain primordium

in the acoel Neochildia, as assessed by the expression

of POU genes (Ramachandra et al. 2002). Jondelius et al.

(2002) further proposed that acoelomorphs arose via

progenesis from a planula-like larva. This is a very different

scenario for early bilaterian evolution than that espoused, for

example, by Davidson and colleagues (e.g., Davidson et al.

1995, Peterson et al. 2000), which postulated indirect development

to be primitive and the earliest bilaterians to

be small planktonic larval forms. It also differs from the

morphology-biased prediction of Peterson and Eernisse

(2001), that the last common ancestor of bilaterians (including

acoelomorphs) was a large organism with deuterostome-

like development (including possibly the possession

of a “dipleurula-like” larva) and a tripartite arrangement

of coeloms similar to modern hemichordates. However,

trimery can no longer be considered primitive for Bilateria

because neither phoronids (Bartolomaeus 2001) nor chaetognaths

(Kapp 2000) are trimeric, which reduces trimery

to a novel synapomorphy for Ambulacraria (see Smith et al.,

ch. 22 in this vol.). Furthermore, this result suggests that

there is no reason to postulate that a coelom is primitive

for either Bilateria or Nephrozoa (contra Budd and Jensen

2000).

We find it intriguing that if acoelomorphs are basal to

other bilaterians, this strengthens the inference that the earliest

bilaterians were small, interstitial, or meiofaunal animals.

Within the remaining bilaterians, small body size is

widespread, so it is at least feasible that the last common

ancestor of the most familiar animals (e.g., vertebrates, insects,

mollusks) was likewise small and benthic. The results

(not shown) of SSU rDNA plus morphology alone still support

acoelomorphs as basal bilaterians but differ from the

total-evidence tree (fig. 13.1B) in that gastrotrichs, gnathostomulids,

and rotifers are basal lophotrochozoans. We

also found the more conventional split between protostomes

(ecdysozoans + lophotrochozoas) and deuterostomes exclusive

of Acoelomorpha. If this topology is further supported,

then the case for a small, creeping, and direct-developing

last common ancestor of not only Nephrozoa but also Protostomia

is strongly supported, because the outgroup(s) (acoelomorphs)

and basal lineages of at least Lophotrochozoa are small

bodied. This could explain why trace fossils are absent during

the earliest phase of bilaterian evolution dating from

about 600 million years ago (K. J. Peterson, J. B. Lyons,

K. S. Nowak, C. M. Takacs, M. J. Wargo, and M. A. McPeek,

unpubl. obs.) to 555 million years ago, when traces make

their first appearance in the rock record (Martin et al. 2000).

The story underlying bilaterian evolution may be one of

initial genetic complexity not manifested until the Cambrian

explosion.

Conclusions

What continually strikes us is that, aside from a few minor

controversies, disparate data sets lead to a remarkably similar

topology of the major animal groups. But equally as important

(and interesting) is that no single data set is entirely accurate.

For example, morphology alone might be “incorrect” (albeit

relatively weak) in supporting a monophyletic Porifera, a sister

grouping between ctenophores and bilaterians, and placing

acoelomorphs within Platyhelminthes. On the other hand,

morphology, but not SSU rDNA, can potentially resolve the

interrelationships among trochozoans. Along the same vein as

our earlier works (e.g., Eernisse 1997, Peterson and Eernisse

2001), we continue to advocate a total-evidence approach with

several different types of data derived from numerous taxa. The

ever continual advancement in phylogenetic software, molecular

tools, and scientific perspective can only lead to a better

understanding of the interrelationships among the major animal

lineages and, of course, to animal evolution itself.

The History of Animals 205

Appendix: Materials and Methods

The morphology matrix is a revised version of the “morphology”

analysis presented in Peterson and Eernisse (2001). Our

new matrix consists of 168 characters; it is not exclusively

morphological because it also includes coding of developmental

or biochemical variation, as well as coding of some

molecular aspects such as inferred Hox gene duplication

events and genetic code differences. The results of this analysis

are only slightly different from our previous study and

largely agree with those derived from sequence data despite

a general perception that molecular results differ fundamentally

from what might be inferred from morphology. The

modified matrix is available from either author.

We also analyzed two different molecular data sets: 43

myosin heavy-chain type II inferred amino acid sequences,

and a data set of 335 selected and manually aligned SSU

rDNA sequences (the full matrix is available upon request

from D. J. E.). The myosin heavy-chain data set, recently

assembled by Ruiz-Trillo et al. (2002), is the newest nonrDNA

data set available for a broad range of metazoan taxa

and is probably the most promising current alternative to

the widely studied SSU rDNA data set [see Giribet (2002)

for a review of the others]. In order to combine these data

sets, we matched myosin heavy-chain sequences with sequences

from the same or related species whose SSU rDNA

sequences we analyzed, and then treated each combined

sequence as a single taxon. This is similar to the method

employed by Ruiz-Trillo et al. (2002) except that, whereas

they limited their analysis to only those taxa represented

by myosin heavy-chain sequences, we kept the nearly 300

SSU rDNA sequences not matched by particular myosin

heavy-chain sequences in the combined analysis, coding the

myosin heavy-chain portion for those sequences as missing

data. Also unlike those authors, we also combined these

molecular data with our morphology matrix. As in Peterson

and Eernisse (2001), we did not attempt to code corresponding

morphology scores for each of the 335 taxa whose SSU

rDNA sequences we analyzed. Instead, for our morphology

analysis we gave equivalent morphology scores to each of the

sequenced species within each of our terminal taxa. This will

create bias in the combined data set favoring the monophyly

of these terminal taxa; usually this was not a problem because

most of these taxa were already found to be monophyletic

in the molecular analyses. The few exceptions, such as annelids

and mollusks, that were monophyletic in the combined

but not the SSU rDNA analysis could be monophyletic

merely because of the groupwide morphology scores they

were given.

Methods used for sequence alignment, exclusion of those

sites with ambiguous alignment, data set combination, and

two-step heuristic search strategy in PAUP* (ver. 4b10; Swofford

2002), are very similar to those employed in Peterson and

Eernisse (2001; see also Eernisse and Kluge 1992, Eernisse

1997). We did not include one of the redundant rodent myosin

heavy-chain sequences in the combined analysis. Our SSU

rDNA data set consisted of 278 of the 302 SSU rDNA sequences

analyzed in Peterson and Eernisse (2001), plus 57

additional SSU rDNA sequences beyond those analyzed previously,

added to bolster previously underrepresented taxa.

We also varied the taxon composition of the SSU rDNA and

myosin heavy-chain sequence data sets, and analyzed a number

of these different taxon combinations plus our reported

335 taxon SSU rDNA data set with different algorithms, specifically

using minimum evolution heuristic searches (HKY85

and LogDet distances as implemented in PAUP*) and Bayesian

inference searches using Mr. Bayes software (ver. 2.01;

Huelsenbeck and Ronquist 2001). All of these results were

consistent with the general pattern resulting from the reported

analyses, with the most substantial differences typically involving

where particular “long-branch” sequences (e.g., chaetognaths,

nemertodermatids, gnathostomulids, onychophorans)

happened to be resolved within Bilateria. For example, the

nemertodermatid and gnathostomulid sequences were observed

to group together or apart anywhere from basally within

Bilateria, to within chordates, to within the panarthropods as

sister group to onychophorans, and such movement was characteristic

of all algorithms employed in the case of the SSU

rDNA analyses.

Literature Cited

Adoutte, A., G. Balavoine, N. Lartillot, and R. de Rosa. 1999.

Animal evolution: the end of intermediate taxa? Trends

Genet. 15:104–108.

Adoutte, A., G. Balavoine, N. Lartillot, O. Lespinet,

B. Prud’homme, and B. de Rosa. 2000. The new animal

phylogeny: reliability and implications. Proc. Natl. Acad.

Sci. USA 97:4453–4456.

Aguinaldo, A. M. A., J. M. Turbeville, L. S. Linford, M. C.

Rivera, J. R. Garey, R. A. Raff, and J. A. Lake. 1997.

Evidence for a clade of nematodes, arthropods and other

molting animals. Nature 387:489–493.

Ahlrichs, W. 1995. Ultrastruktur und Phylogenie von Seison

nebaliae (Grube 1859) und Seison annulatus (Claus 1876).

Hypothesen zu phylogenetischen Verwandtschaftsverhдltnissen

innerhalb der Bilateria. Cuvillier Verlag,

Gцttingen.

Atkins, M. S., A. G. McArthur, and A. P. Teske. 2000. Ancyromonadida:

a new phylogenetic lineage among the Protozoa

closely related to the common ancestor of Metazoans,

Fungi, and Choanoflagellates (Opisthokonta). J. Mol. Evol.

51:278–285.

Ax, P. 1996. Multicellular animals: a new approach to the

phylogenetic order in nature, vol. 1. Springer, Berlin.

Baguса, J., I. Ruiz-Trillo, J. Paps, M. Loukota, C. Ribera,

U. Jondelius, and M. Riutort. 2001. The first bilaterian

organisms: simple or complex? New molecular evidence.

Int. J. Dev. Biol. 45:S133–S134.

Balavoine, G., R. de Rosa, and A. Adoutte. 2002. Hox clusters

206 The Relationships of Animals: Overview

and bilaterian phylogeny. Mol. Phylogenet. Evol. 24:366–

373.

Baldauf, S. L., and J. D. Palmer. 1993. Animals and fungi are

each other’s closest relatives: congruent evidence from

multiple proteins. Proc. Natl. Acad. Sci. USA 90:11558–

11562.

Baldauf, S. L., A. J. Roger, I. Wenk-Siefert, and W. F. Doolittle.

2000. A kingdom-level phylogeny of eukaryotes based on

combined protein data. Science 290:972–977.

Bartolomaeus, T. 2001. Ultrastructure and formation of

the body cavity lining in Phoronis muelleri (Phoronida,

Lophophoroata). Zoomorphology 120:135–148.

Beklemishev, V. N. 1969. Principles of comparative anatomy of

invertebrates (J. M., MacLennan, trans.; Z. Kabata, ed.).

University of Chicago Press, Chicago.

Bonik, K., M. Grasshoff, and W. F. Gutmann. 1976. Die

Evolution der Tierkonstruktionen I. Problemlage und

Prдmissen. Vielzeller und die Evolution der Gallertoide. Nat.

Mus. 106:129–143.

Borchiellini, C., N. Boury-Esnault, J. Vacelet, and Y. Le Parco.

1998. Phylogenetic analysis of the Hsp70 sequences reveals

the monophyly of Metazoa and specific phylogenetic

relationships between animals and fungi. Mol. Biol. Evol.

15:647–655.

Borchiellini, C., M. Manuel, E. Alivon, N. Boury-Esnault,

J. Vacelet, and Y. Le Parco. 2001. Sponge paraphyly and the

origin of Metazoa. J. Evol. Biol. 14:171–179.

Bridge, D., C. W. Cunningham, R. Desalle, and L. W. Buss.

1995. Class-level relationships in the phylum Cnidaria:

molecular and morphological evidence. Mol. Biol. Evol.

12:679–689.

Brusca, R. C., and G. J. Brusca. 1990. Invertebrates. Sinauer,

Sunderland, MA.

Budd, G. E., and S. Jensen. 2000. A critical reappraisal of the

fossil record of the bilaterian phyla. Biol. Rev. Camb. Philos.

Soc. 75:253–295.

Callaerts, P., P. N. Lee, B. Hartmann, C. Farfan, D. W. Y. Choy,

K. Ikeo, K.-F. Fischback, W. J. Gehring, and H. Gert de

Couet. 2002. HOX genes in the sepiolid squid Euprymna

scolopes: implications for the evolution of complex body

plans. Proc. Natl. Acad. Sci. USA 99:2088–2093.

Cavalier-Smith, T. 1998. A revised six-kingdom system of life.

Biol. Rev. 73:203–266.

Cavalier-Smith, T., M. T. E. P. Allsopp, E. E. Chao, N. Boury-

Esnault, and J. Vacelet. 1996. Sponge phylogeny, animal

monophyly, and the origin of the nervous system: 18S

rRNA evidence. Can. J. Zool. 74:2031–2045.

Collins, A. G. 1998. Evaluating multiple alternative hypotheses

for the origin of Bilateria: an analysis of 18S rRNA molecular

evidence. Proc. Natl. Acad. Sci. USA 95:15458–15463.

Collins, A. G. 2002. Phylogeny of Medusozoa and the evolution

of cnidarian life cycles. J. Evol. Biol. 15:418–432.

Davidson, E. H., K. J. Peterson, and R. A. Cameron. 1995.

Origin of adult bilaterian body plans: evolution of developmental

regulatory mechanisms. Science 270:1319–1325.

de Rosa, R., J. K. Grenier, T. Andreeva, C. E. Cook, A. Adoutte,

M. Akam, S. B. Carroll, and G. Balavoine. 1999. Hox genes

in brachiopods and priapulids and protostome evolution.

Nature 399:772–776.

Eernisse, D. J. 1997. Arthropod and annelid relationships reexamined.

Pp. 43–56 in Arthropod relationships (R. A.

Fortey, and R. H. Thomas, eds.). Systematics Association

Special Volume Series 55. Chapman and Hall, London.

Eernisse, D. J., J. S. Albert, and F. E. Anderson. 1992. Annelida

and Arthropoda are not sister taxa: a phylogenetic analysis

of spiralian metazoan morphology. Syst. Biol. 41:305–330.

Eernisse, D. J., and A. Kluge. 1993. Taxomonic congruence

versus total evidence, and amniote phylogeny inferred from

fossils, molecules, and morphology. Mol. Biol. Evol.

10:1170–1195.

Ender, A., and B. Schierwater. 2003. Placozoa are not derived

cnidarians: evidence from molecular morphology. Mol. Biol.

Evol. 20:130–134.

Eriksson, B. J., and G. E. Budd. 2000. Onychophoran cephalic

nerves and their bearing on our understanding of head

segmentation and stem-group evolution of Arthropoda.

Arthrop. Struct. Dev. 29:197–209.

Ferrier, D. E. K., and P. W. H. Holland. 2001. Sipunculan

ParaHox genes. Evol. Dev. 3:263–270.

Field, K. G., G. J. Olsen, D. J. Lane, S. J. Giovannoni, M. T.

Ghiselin, E. C. Raff, N. R. Pace, and R. A. Raff. 1988.

Molecular phylogeny of the animal kingdom. Science

239:748–753.

Ghiselin, M. T. 1988. The origin of molluscs in the light of

molecular evidence. Oxford Surv. Evol. Biol. 5:66–95.

Ghiselin, M. T. 1989. Summary of our present knowledge of

metazoan phylogeny. Pp. 262–272 in The hierarchy of life

(B. Fernholm, K. Bremer, and H. Jцrnvall, eds.). Elsevier

Science Publishers, Amsterdam.

Giribet, G. 2002. Current advances in the phylogenetic

reconstruction of metazoan evolution: a new paradigm for

the Cambrian explosion? Mol. Phylogenet. Evol. 24:345–

357.

Giribet, G., D. L. Distel, M. Polz, W. Sterrer, and W. C.

Wheeler. 2000. Triploblastic relationships with emphasis on

the acoelomates and the position of Gnathostomulida,

Cycliophora, Plathelminthes, and Chaetognatha: a combined

approach of 18S rNDA sequences and morphology.

Syst. Biol. 49:539–562.

Grell, K. G., and A. Ruthmann. 1991. Placozoa. Pp. 13–28 in

Microscopic anatomy of invertebrates (F. W. Harrison and

J. A. Westfall, eds.), vol. 2. Wiley-Liss, New York.

Grцger, H., P. Callaerts, W. J. Gehring, and V. Schmid. 2000.

Characterization and expression analysis of an ancestor-type

Pax gene in the hydrozoan jellyfish Podocoryne carnea.

Mech. Dev. 94:157–169.

Gschwentner, R., P. Ladurner, K. Nimeth, and R. Rieger. 2001.

Stem cells in a basal bilaterian: S-phase and mitotic cells in

Convolutriloba longifissura (Acoela, Platyhelminthes). Cell

Tissue Res. 304:401–408.

Haase, A., M. Stern, K. Wдchtler, and G. Bicker. 2001. A tissuespecific

marker of Ecdysozoa. Dev. Genes Evol. 211:428–

433.

Halanych, K. M. 1996. Testing hypotheses of chaetognath

origins: long branches revealed by 18S ribosomal DNA.

Syst. Biol. 45:223–246.

Halanych, K. M. 1998. Consideration for reconstructing

metazoan history: signal, resolution, and hypothesis testing.

Am. Zool. 38:929–941.

Halanych, K. M., J. D. Bacheller, A. M. A. Aguinaldo, S. M. Liva,

The History of Animals 207

D. M. Hillis, and J. A. Lake. 1995. Evidence from 18S

ribosomal DNA that the lophophorates are protostome

animals. Science 267:1641–1643.

Halanych, K. M., T. G. Dahlgren, and D. McHugh. 2002.

Unsegmented annelids? Possible origins of four lophotrochozoan

worm taxa. Integ. Comp. Biol. 42:678–684.

Hertel L. A., C. J. Bayne, and E. S. Loker. 2002. The symbiont

Capsaspora owczarzaki, nov. gen. nov. sp., isolated from

three strains of the pulmonate snail Biomphalaria glabrata is

related to members of the Mesomycetozoea. Int. J. Parasitol.

32:1183–1191.

Hoffman, P. F., A. J. Kaufman, G. P. Halverson, and D. P.

Schrag. 1998. A Neoproterozoic snowball Earth. Science

281:1342–1346.

Huelsenbeck, J. P., and F. Ronquist. 2001. MRBAYES: Bayesian

inference of phylogeny. Bioinformatics L. H. 17:754–755.

Hyman, L. H. 1940. The invertebrates, Vol. 1: Protozoa through

Ctenophora. McGraw-Hill, New York.

Hyman, L. H. 1951. The invertebrates, Vol. 2: Platyhelminthes

and Rhynchocoela. McGraw-Hill, New York.

Hyman, L. H. 1959. The invertebrates, Vol. 5: Smaller Coelomate

groups. McGraw Hill, New York.

James-Clark, H. 1866. Note on the infusoria flagellata and the

spongiae ciliatae. Am. J. Sci. 1:113–114.

James-Clark, H. 1868. On the spongiae ciliatae as infusoria

flagellata; or observations on the structure, animality and

relationship of Leucosolenia botryoides, Bowerbank. Ann.

Mag. Nat. Hist. 1:133–142.

Jondelius, U., I. Ruiz-Trillo, J Baguса, and M. Riutort. 2002.

The Nemertodermatida are basal bilaterians and not

members of the Platyhelminthes. Zool. Scr. 31:201–215.

Kapp, H. 2000. The unique embryology of Chaetognatha. Zool.

Anz. 239:263–266.

Kim, J., W. Kim, and C. W. Cunningham. 1999. A new

perspective on lower metazoan relationships from 18S

rDNA sequences. Mol. Biol. Evol. 16:423–427.

King, N., and S. B. Carroll. 2001. A receptor tyrosine kinase

from choanoflagellates: molecular insights into early animal

evolution. Proc. Natl. Acad. Sci. USA 98:15032–15037.

Lemburg, C. 1995. Ultrastructure of the introvert and associated

structures of the larvae of Halicryptus spinulosus (Priapulida).

Zoomorphology 115:11–29.

Loytynoja, A., and M. C. Milinkovitch. 2001. Molecular

phylogenetic analyses of the mitochondrial ADP-ATP

carriers: the Plantae/Fungi/Metazoa trichotomy revisited.

Proc. Natl. Acad. Sci. USA 98:10202–10207.

Mallatt, J., and C. J. Winchell. 2002. Testing the new animal

phylogeny: first use of combined large-subunit and smallsubunit

rRNA gene sequences to classify the protostomes.

Mol. Biol. Evol. 19:289–301.

Manuel, M., M. Kruse, W. E. G. Mьller, and Y. Le Parco. 2000.

The comparison of -thymosin homologues among Metazoa

supports and arthropod-nematode clade. J. Mol. Evol.

51:378–381.

Martin, M. W., D. V. Grazhdankin, S. A. Bowring, D. A. D.

Evans, M. A. Fedonkin, and J. L. Kirschvink. 2000. Age of

Neoproterozoic bilaterian body and trace fossils, White Sea,

Russia: implications for metazoan evolution. Science

288:841–845.

Martindale, M. Q., J. R. Finnerty, and J. Q. Henry. 2002. The

Radiata and the evolutionary origins of the bilaterian body

plan. Mol. Phylogenet. Evol. 24:358–365.

McPartland, J., V. Di Marzo, L. De Petrocellis, A. Mercer, and

M. Glass. 2001. Cannabinoid receptors are absent in insects.

J. Comp. Neurol. 436:423–429.

Medina, M., A. G. Collins, J. D. Silberman, and M. L. Sogin.

2001. Evaluating hypotheses of basal animal phylogeny

using complete sequences of large and small subunit rRNA.

Proc. Natl. Acad. Sci. USA 98:9707–9712.

Mendozoa, L., J. W. Taylor, and L. Ajello. 2002. The class

Mesomycetozoea: a heterogeneous group of microorganisms

at the animal-fungal boundary. Annu. Rev. Microsc.

56:315–344.

Moon-van der Staay, S. Y., R. De Wachter, and D. Vaulot. 2001.

Oceanic 18S rDNA sequences from picoplankton reveal

unsuspected eukaryotic diversity. Nature 409:607–610.

Morris, P. J. 1993. The developmental role of the extracellular

matrix suggests a monophyletic origin of the kingdom

Animalia. Evolution 47:152–165.

Mьller, W. E. G. 2001. Review: how was metazoan threshold

crossed? The hypothetical Urmetazoa. Comp. Biochem.

Physiol. A 129:433–460.

Nielsen, C. 1995. Animal evolution: interrelationships of the

living phyla. Oxford University Press, Oxford.

Nielsen, C. 2001. Animal evolution: interrelationships of the

living phyla. 2nd ed. Oxford University Press, Oxford.

Nielsen, C., N. Scharff, and D. Eibye-Jacobsen. 1996. Cladistic

analysis of the animal kingdom. Biol. J. Linn. Soc. 57:385–

410.

Peterson, K. J., R. A. Cameron, and E. H. Davidson. 2000.

Bilaterian origins: significance of new experimental

observations. Dev. Biol. 219:1–17.

Peterson, K. J., and D. J. Eernisse. 2001. Animal phylogeny and

the ancestry of bilaterians: inferences from morphology and

18S rDNA gene sequences. Evol. Dev. 3:170–205.

Podar, M., S. H. D. Haddock, M. L. Sogin, and G. R. Harbison.

2001. A molecular phylogenetic framework for the phylum

Ctenophora using 18S rRNA genes. Mol. Phylogenet. Evol.

21:218–230.

Ramachandra, N. B., R. D. Gates, P. Ladurner, D. K. Jacobs, and

V. Hartenstein. 2002. Embryonic development in the

primitive bilaterian Neochildia fusca: normal morphogenesis

and isolation of POU genes Brn-1 and Brn-3. Dev. Genes

Evol. 212:55–69.

Ruiz-Trillo, I., J. Paps, M. Loukota, C. Ribera, U. Jondelius,

J. Baguсa, and M. Riutort. 2002. A phylogenetic analysis of

myosin heavy chain type II sequences corrobrates that

Acoela and Nemertodermatida are basal bilaterians. Proc.

Natl. Acad. Sci. USA 99:11246–11251.

Ruiz-Trillo, I., M. Riutort, D. T. J. Littlewood, E. A. Herniou,

and J. Baguса. 1999. Acoel flatworms: earliest extant

bilaterian metazoans, not members of Platyhelminthes.

Science 283:1919–1923.

Salу, E., J. Tauler, E. Jimenez, J. R. Bayascas, J. Gonzalez-

Linares, J. Garcia-Ferdandez, and J. Baguса. 2001. Hox and

ParaHox genes in flatworms: characterization and expression.

Am. Zool. 41:652–663.

Schimkewitsch, W. 1891. Versuch einer Klassifikation des

Tierreichs. Biol. Zent. Bl. 11:291–295.

Schmidt-Rhaesa, A. 1996. The nervous system of Nectonema

208 The Relationships of Animals: Overview

munidae and Gordius aquaticus, with implications for the

ground pattern of the Nematomorpha. Zoomorphology

116:133–142.

Schmidt-Rhaesa, A., T. Bartolomaeus C. Lemburg, U. Ehlers,

and J. Garey. 1998. The position of the Arthropoda in the

phylogenetic system. J. Morphol. 238:263–285.

Schram, F. R. 1991. Cladistic analysis of metazoan phyla and

the placement of fossil problematica. Pp. 35–46 in The early

evolution of Metazoa and the significance of problematic

taxa (A. M. Simonetta and S. Conway Morris, eds.).

Cambridge University Press, Cambridge.

Schuchert, P. 1993. Phylogenetic analysis of the Cnidaria.

Z. Zool. Syst. Evol. 31:161–173.

Shimotori, T., and T. Goto. 2001. Developmental fates of the

first four blastomeres of the chaetognath Paraspadella gotoi:

relationship to protostomes. Dev. Growth Differ. 43:371–

382.

Snell, E. A., R. F. Furlong, and P. W. H. Holland. 2001. Hsp70

sequences indicate that choanoflagellates are closely related

to animals. Curr. Biol. 11:967–970.

Stiller, J. W., and B. D. Hall. 2002. Evolution of the RNA

polymerase II C-terminal domain. Proc. Natl. Acad. Sci.

USA 99:6091–6096.

Stiller, J. W., J. Riley, and B. D. Hall. 2001. Are red algae plants?

A critical evaluation of three key molecular data sets. J. Mol.

Evol. 52:527–539.

Suga, H., M. Koyanagi, D. Hoshiyama, K. Ono, N. Iwabe, K.-I

Kuma, and T. Miyata. 1999. Extensive gene duplication in

the early evolution of animals before the parazoaneumetazoan

split demonstrated by G proteins and protein

tyrosine kinases from sponge and hydra. J. Mol. Evol.

48:646–653.

Swofford, D. L. 2002. PAUP* phylogenetic analysis using

parsimony (* and other methods), ver. 4.0b10 for Macintosh.

Sinauer Associates, Sunderland, MA.

Takacs, C. M., V. N. Moy, and K. J. Peterson. 2002. Testing

putative hemichordate homologues of the chordates dorsal

nervous system and endostyle: expression of NK2.1 (TTF-1)

in the acorn worm Ptychodera flava (Hemichordata,

Ptychoderidae). Evol. Dev. 4:405–417.

Tardent, P. 1995. The cnidarian cnidocyte, a high-tech cellular

weaponry. Bioessays 17:351–362.

Telford, M. J., and P. W. H. Holland. 1993. The phylogenetic

affinities of the chaetognaths: a molecular analysis. Mol.

Biol. Evol. 10:660–676.

Turbeville, J. M., J. R. Schultz, and R. A. Raff. 1994. Deuterostome

phylogeny and the sister group of the chordates:

evidence from molecules and morphology. Mol. Biol. Evol.

11:648–655.

Van Auken, K., D. C. Weaver L. G. Edgar, and W. B. Wood.

2000. Caenorhabditis elegans embryonic axial patterning

requires two recently discovered posterior-group Hox

genes. Proc. Natl. Acad. Sci. USA 97:4499–4503.

Wada, H., and N. Satoh. 1994. Details of the evolutionary

history from invertebrates to vertebrates, as deduced from

the sequences of 18S rDNA. Proc. Natl. Acad. Sci. USA

91:1801–1804.

Wainright, P. O., G. Hinkle, M. L. Sogin, and S. K. Stickel.

1993. Monophyletic origins of the Metazoa: an evolutionary

link with Fungi. Science 260:340–342.

Winnepenninckx, B., T. Backeljau, L. Y. Mackey, J. M. Brooks,

R. De Wachter, S. Kumar, and J. R. Garey. 1995. 18S rRNA

data indicate that Aschelminthes are polyphyletic in origin

and consist of at least three distinct clades. Mol. Biol. Evol.

12:1132–1137.

Xiao, S., Y. Zhang, and A. H. Knoll. 1998. Three-dimensional

preservation of algae and animal embryos in a Neoproterozoic

phosphorite. Nature 391:553–558.

Zettler, L. A. A., C. J. O’Kelly, T. A. Nerad, and M. L. Sogin.

2001. The nucleariid amoebae: more protists at the animalfungal

boundary. J. Eukaryot. Microbiol. 48:293–297.

Zrzavэ, J. 2003. Gastrotricha and metazoan phylogeny. Zool.

Scripta 32:61–81.

Zrzavэ, J., V. Hypsa, and D. F. Tietz. 2001. Myzostomida are

not annelids: molecular and morphological support for a

clade of animals with anterior sperm flagella. Cladistics

17:170–198.

Zrzavэ, J., S. Mihulka, P. Kepka, A. Bezdek, and D. Tietz. 1998.

Phylogeny of the Metazoa based on morphological and 18S

ribosomal DNA evidence. Cladistics 14:249–285.

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