14 Protostomes and Platyhelminthes The Worm’s Turn

Back

D. Timothy J. Littlewood

Maximilian J. Telford

Rodney A. Bray

209

The simplest partitioning of the bilaterally symmetrical animals

(Bilateria) is the split between the Deuterostomia and

Protostomia, divisions founded primarily on very different

modes of embryonic development. The protostomes (Gr.

“mouth first”) include those animals in which, after gastrulation,

the mouth is formed at or near the blastopore opening

rather than being a secondary opening (deuterostomy).

Here we introduce some of the major protostome groups not

treated elsewhere in this volume, with a particular emphasis

on the flatworms (phylum Platyhelminthes) and their allies.

We cover 15 phyla, including a number of important but

enigmatic groups that have either flirted with shared ancestry

with the flatworms or that are difficult to place among

the protostomes. Early phylogenetic scenarios often placed

the flatworms as basal bilaterian groups (even as ancestral

archetypes) from which a range of more complex protostomes

arose. As with any phylogenetic tree, the placement

of the most basal group has important consequences for our

understanding of an evolutionary radiation. Consequently,

identifying the basal bilaterian is pivotal for understanding

the evolutionary radiation of the major animal phyla.

The Protostomia are currently split into Lophotrochozoa,

with members characterized by spiral embryonic cleavage

patterns, and Ecdysozoa, characterized by animals that molt

an exoskeleton as they grow and develop (see Eernisse and

Peterson, ch. 13 in this vol.; see also Gilbert 2000). The taxa

we cover (shown in boldface in fig. 14.1) are to be found in

both groups, or have yet to be placed convincingly in the tree.

Untangling the inter- and intraphyletic relationships of the

various taxa covered here has been driven variously by purely

systematic goals and evolutionary questions but also, importantly,

within some phyla, by a need to understand parasites

and parasitism. Some of the most medically and economically

important parasites are found among the Platyhelminthes,

Nematoda and Acanthocephala. Additionally, some

protostome species have been model organisms for the latest

developments in genome research; the nematode Caenorhabditis

elegans, for example, was the first multicellular animal

to have its entire genome sequenced and remains a favored

organism for understanding gene function. These applied

aspects of biology have often provided both the need to resolve

wider patterns of evolutionary radiation and the sources

of characters with which phylogenies can be estimated.

Our starting point is the tree shown in figure 14.1. The

lack of resolution indicated by the collapsed nodes, and the

tentative placement of taxa with dashed lines, indicates conflict

and uncertainty over the interrelationships of the protostomes.

The tree is an updated version of what Adoutte et al.

(2000) termed “the new animal phylogeny.” Based largely on

ribosomal RNA (rRNA) gene sequences, and other molecular

data, it is overall poorly resolved but represents major

groupings that are well supported.

Almost without exception, the groups we consider here

have little or no fossil record. As soft-bodied animals, their

fossil record is, at best, restricted to traces, which provide

few reliable characters for phylogenetic analysis. This is in

210 The Relationships of Animals: Overview

contrast to other protostome groups such as Arthropoda and

Mollusca, which are addressed elsewhere in this volume.

Wherever possible, we provide detailed interrelationships

within each phylum considered.

Basal Bilaterians

Which was the first bilaterally symmetrical animal to evolve,

and what did it look like? As members of Bilateria ourselves,

this question generates more than an intrinsic academic interest.

The fossil record has not been able to help us because

it seems most likely that the first bilaterian was a soft-bodied

and possibly microscopic organism that has left few, if any,

clues as to its identity. Identifying the earliest branching taxon

within Bilateria has been difficult, and different lines of evidence

have not converged on a single satisfactory solution.

Because we can work only with extant organisms, the best

we can do is to reveal the earliest divergent living group while

necessarily ignoring the extinct groups that have left little or

no trace. Notwithstanding the usual conflict in opinion over

character homology when comparing deeply branching taxa,

an additional problem has been that confusion reigns when

we inadvertently use para- or polyphyletic taxa as monophyletic

groups for coding purposes or when subsequently interpreting

a tree. A case in point concerns the acoelomorph

flatworms, which, combined with the perceived “primitiveness”

of all the flatworms, are responsible for pulling the

Platyhelminthes to the base of Bilateria or Protostomia in

works dating before the 1990s.

Acoelomorpha

Acoelomorph flatworms include two groups, Acoela (19 families,

120 genera) and the far less species-rich Nemertodermatida

(two families, six genera; fig. 14.2). Long established

as the most basal members of the phylum Platyhelminthes,

along with Catenulida (Ehlers 1985a), the apparent simplicity

of members of Acoelomorpha may have contributed to the

view that the whole phylum is an early offshoot of the bilateral

Metazoa, in combination of course with the phylum’s

lack of anus or coelom. Their simplicity in form makes the

acoelomorphs attractive candidates from which more complex

forms may be postulated to have evolved, and although

there are no derived characters that unite acoelomorphs with

other flatworm groups (Tyler 2001), they have long since

been considered members of Platyhelminthes. Insidiously,

this simple body plan shared by acoelomorphs and all other

flatworms has led to a deal of conflict and a range of scenarios,

with flatworms being variously placed as sister group to all

protostomes or nestled within Lophotrochozoa. Smith and

Tyler (1985) and Smith et al. (1986) were the first to question

the monophyly of Platyhelminthes, and Haszprunar

(1996b), suggested that acoels alone should be considered

basal, with the catenulid and rhabditophoran flatworms as

more closely related offshoots of a para- if not polyphyletic

Platyhelminthes. Molecular data from small subunit (SSU)

ribosomal DNA (rDNA) began a renewed debate that carries

on to this day. Ruiz-Trillo et al. (1999) presented evidence

that acoels are the most basal bilaterian group and are not

monophyletic with the other flatworms, which were indeed

Lophotrochozoa. Efforts to avoid long-branch attraction,

where divergent taxa spuriously appear at the base of a rooted

tree, failed to convince some authors that the basal placement

of Acoela was anything but artifact (e.g., Adoutte et al. 1999),

and appears to have plagued others (Peterson and Eernisse

2001). The polyphyly of Acoelomorpha in Ruiz-Trillo et al.’s

(1999) study has also not helped the case, because strong

morphological characters unite the two constituent groups

(see below; see also Ehlers 1992, Littlewood et al. 1999b).

Figure 14.1. Interrelationships of the major protostome

groups. Groups covered in this chapter are shown in boldface.

Broken lines indicate possible affinities of various groups.

Acoelomorpha, once considered members of Platyhelminthes,

are now convincingly placed at the base of Bilateria (Deuterostomia

+ Protostomia).

Protostomes and Platyhelminthes 211

Jondelius et al. (2002) have since shown that the sequence

attributed to the nemertodermatid Nemertinoides elongatus

was probably that of a rhabditophoran flatworm and have

subsequently provided a denser sampling of SSU rDNA, and

a recent study of complete large subunit (LSU) rDNA by

Telford et al.(2003) shows that both Acoela and Nemertodermatida

appear as basal bilaterians. Although in these studies

Acoelomorpha remains weakly paraphyletic, its basal

position is robust, setting this group apart from both catenulid

and rhabditophoran platyhelminths, which appear

convincingly among the Lophotrochozoa. Evidence from a

further gene, coding for myosin II, strongly corroborates the

basal position of Acoelomorpha (Ruiz-Trillo et al. 2002).

Although not giving evidence of a basal position for Acoela,

developmental studies demonstrated unique duet spiral

cleavage (Henry et al. 2000). Members of Acoela apparently

lack ectomesoderm and all musculature, and peripheral parenchyma

is of entomesodermal origin, suggesting a possible

link with Ctenophora (see Henry et al. 2000, Martindale and

Henry 1999a, 1999b). Evidence from neuronal cytochemistry

continues to support the uniqueness of Acoelomorpha

when contrasted with other flatworm groups (Reuter et al.

2001a, 2001b). The interrelationships of Acoela have been

explored phylogenetically most recently with SSU by Hooge

et al. (2002), and the relatively species-poor Nemertodermatida

has been tackled thoroughly by a morphological analysis

(Lundin 2000).

Apomorphies of Acoelomorpha (Ehlers 1985a)

Epidermal cilia with shelflike termination

Rostral rootlet of epidermal cilia with kneelike bend

Posterior rootlet of epidermal cilia with two fiber

bundles

Reduction of protonephridia

Additional molecular data from the gene that encodes

EF-1a protein (Littlewood et al. 2001b) and surveys of mitochondrial

genetic code assignment throughout the flatworms

(Telford et al. 2000) have conclusively demonstrated

the separation of acoelomorphs and rhabditophoran flatworms,

and strong evidence from three genes places acoelomorphs

as the most basal Bilateria (fig. 14.1).

Gnathostomulida: The Jaw Worms

Gnathostomulida (fig. 14.3), a group consisting of about 100

species of nonsegmented microscopic marine worms, is considered

by some to be the sister group to Platyhelminthes;

synapomorphies include hermaphroditism, direct transfer of

sperm and internal fertilization of egg cells, threadlike sperm,

and no mitosis in somatic cells (Ax 1996). In turn, this clade,

Plathelminthomorpha, was postulated to be the sister group

to all other members of Bilateria (Ax 1985). Recent studies

including both molecular and combined analyses have

prompted a bewildering array of possibilities: based on SSU

rDNA, they have been placed among the Ecdysozoa (Littlewood

et al. 1998); based on SSU rDNA and morphology,

with Platyhelminthes in a clade, Platyzoa, that includes

Cycliophora, Syndermata (Acanthocephala + Rotifera), and

Gastrotricha (Giribet et al. 2000); based on a combined analysis

of SSU rDNA and morphology, in a clade that unites

Gnathostomulida and Gastrotricha affiliated with Ecdysozoa

(Zrzavэ et al. 1998); and based on morphology, in a clade

with Rotifera and Acanthocephala related to Lophotrochozoa

(Sшrensen et al. 2000).

Although gnathostomulids are not strong contenders for

the title of most basal bilaterian, their position among the

Metazoa is unstable, based on both molecular and morphological

studies, and so additional evidence is needed to secure

their true position. Recent morphological studies on jaw

ultrastructure suggest an affiliation with Rotifera and Micrognathozoa

(Sшrensen and Sterrer 2002).

Apomorphy of Gnathostomulida (Ax 1985)

Pharynx with jaws and basal plate

Gastrotricha

Gastrotrichs are microscopic, cryptic animals that usually live

between grains of sand and silt in both freshwater and saltwater.

Figure 14.2. Representatives of each of the constituent

acoelomorph groups; courtesy of Queensland Museum, from

Cannon (1986), with permission. Scale bars, 200 mm.

Convoluta norwegica

Convolutidae

ACOELA

Nemertoderma bathycola

Nemertodermatidae

NEMERTODERMATIDA

212 The Relationships of Animals: Overview

They are nonsegmented, have a through-gut with a pharynx,

and are generally microscopic (50–1000 mm; fig. 14.4). The two

constituent orders are very different from one another, but the

group has long been considered monophyletic from a morphological

perspective. As with other members of the meiofauna,

gastrotrichs are relatively poorly studied but constitute an important

and ubiquitous component of limnetic and marine

sediments and detritus. Ciliated, hermaphroditic, and often

bottle-shaped, gastrotrichs are usually flattened ventrally with

the posterior end sometimes split into a fork.

Apomorphies of Gastrotricha

Unique, cuticle-covered duo-gland adhesive organ

Multilayered epicuticle

Cuticle-covered locomotory and sensory cilia

Possibly unique left and right helicoidal muscle

The order Macrodasyida, with six recognized families,

includes exclusively marine or brackish, interstitial creatures,

whereas the more species-rich Chaetonotida, with seven

families, includes freshwater and epibenthic animals. Each

order is defined primarily on the fine structure of the pharynx.

Gastrotricha is another phylum that has vied for the position

of most basal bilaterian, with apparent affinities to

Gnathostomulida, according to some (e.g., Boaden 1985), or

to the ecdysozoan phyla, most notably Nematoda, by others

(Ruppert 1991, Wallace et al. 1996). Many of the early cladistic

analyses appear to have suffered from choosing characters

unique to chaetonotids, rather than ones apomorphic for the

phylum (e.g., see discussion in Hochberg and Litvaitis 2000).

The position is even more confused from molecular estimates,

largely because of poor sampling of both genes and taxa.

Early molecular studies have variously placed the gastrotrichs

as a sister group to Acanthocephala or Nematomorpha

(Carranza et al. 1997), Gnathostomulida (Littlewood et al.

1998), or Platyhelminthes (Winnepenninckx et al. 1995). In

each case, rarely more than a single gastrotrich sequence was

used. Subsequent denser sampling of taxa produced unsatisfactory

results because only a limited sampling and range

of other metazoan taxa were employed (Wirz et al. 1999),

with the result that the group’s affinities are not well supported

by molecular or by morphological data. Combined

molecular and morphological analyses have placed the group

as sister group to Gnathostomulida (Zrzavэ et al. 1998) or

Platyhelminthes (Giribet et al. 2000) and within Ecdysozoa

(Peterson and Eernisse 2001).

The gastrotrichs are at least resolved as a monophyletic

phylum, although this has yet to be confirmed with molecular

data, and recent morphological analyses lend some resolution

to the interrelationships of constituent families (see

fig. 14.4; see also Hochberg and Litvaitis 2000), although the

authors urge caution and suggest the main use of such a

phylogeny is for hypothesis testing and appropriate future

sampling for molecular studies. Clearly, much has to be done

with this neglected but fascinating phylum.

Figure 14.3. Member of the enigmatic Gnathostomulida;

redrawn from Ax (1996).

Figure 14.4. Interrelationships of Gastrotricha based on a

morphological analysis (Hochberg and Litvaitis 2000), with line

drawings of representatives.

Thaumastodermatidae

'Chaetonotidae'

Xenotrichulidae

'Chaetonotidae'

'Chaetonotidae'

'Chaetonotidae'

'Chaetonotidae'

'Chaetonotidae'

Dichaeturidae

Proichthydidae

Neogosseidae

Dasydidytidae

'Lepidodasyidae'

Turbanellidae

'Planodasyidae'

Macrodasyidae

'Lepidodasyidae'

'Planodasyidae'

'Lepidodasyidae'

Dactylopodolidae

Dasydetes goniathrix

Dasydidytidae

Chaetonotus bogdanovii

Chaetonotidae

Gnathostomula lutheri

Bursovaginoidea

GNATHOSTOMULIDA

Protostomes and Platyhelminthes 213

Xenoturbellida

One species alone, Xenoturbella bockii, forms the taxon Xenoturbellida

(fig. 14.5). As with the Acoelomorpha, Xenoturbella

is very simple, and perhaps as a consequence it has been placed

as a sister group to both Acoelomorpha (Franzйn and Afzelius

1987, Hyman 1951) and Bilateria (Ehlers and Sopott-Ehlers

1997a, 1997b, Franzйn and Afzelius 1987). The worm shares

with members of Acoelomorpha the ability to resorb worn or

damaged ciliated epidermal cells (Lundin 2001) and a shelflike

termination of the epidermal cilia (Ax 1996). Affinities with

Mollusca, based on molecular data (Norйn and Jondelius 1997),

appear to results from contamination in the study, because

sequences are almost identical to those from the species of

protobranch mollusks that Xenoturbella feeds on, and affinities

based on morphology are likely misinterpretations (Israelsson

1999). Ultrastructural evidence argues strongly against molluscan

affinities (Lundin 1998, Lundin and Schander 1999,

Raikova et al. 2000), and in the absence of crucial corroborative

molecular data, we are left with no concrete idea of the position

of Xenoturbella. However, new sequence data in the form

of SSU rDNA and two mitochondrial genes have recently demonstrated

that Xenoturbella falls among Deuterostomia perhaps

as sister group to Ambulacraria (Bourlat et al. 2003).

Platyhelminthes: The Flatworms

Platyhelminthes includes Acoelomorpha, Catenulida, and

Rhabditophora, but as described above, there is no synapomorphy

uniting these taxa, and the acoelomorphs appear to

be sufficiently different to consider them apart from the other

two. Recent analyses of full LSU and SSU rDNA place Catenulida

and Rhabditophora as sister groups, and it is these

two groups we believe constitute Platyhelminthes to the

exclusion of acoelomorphs, although again, there are no

morphological synapomorphies for this grouping. The

monophyly of the two constituent groups is not in doubt,

and the resolution of rhabditophoran relationships has

progressed considerably, although some groupings remain

contentious (see fig. 14.6). An excellent online taxonomic

database for the free-living flatworms is Tyler (2003). Although

a total evidence estimate of the interrelationships of

members of Platyhelminthes has been attempted, combining

morphological and molecular data (Littlewood et al.

1999a), there are still many problems in resolving a stable

phylogeny because we are limited by numbers of morphological

characters and by problems in their coding and, in

many cases, establishing homology.

Catenulida

Although little systematic effort has been expended in resolving

the interrelationships of members of Catenulida, it is clear

that as sister group to all other (rhabditophoran) flatworms,

it deserves greater attention from both morphological and

molecular perspectives. With five families, 11 genera, and

more than 100 species, it is surprising that only two species

have been sequenced for various molecular estimates of

phylogeny. All catenulids are free-living, primarily in freshwater

but some in marine environments (see fig. 14.7).

When scored for various platyhelminth features, they are

notably lacking in many systems that define the majority of

other groups, such as a duo-gland adhesive system, or show

a great deal of variability in the presence or absence of other

features between the families.

Apomorphies of Catenulida (Ehlers 1985a)

Unpaired protonephridium

Unique organization of the cyrtocyte

Dorsally located male genital porus

Aciliary spermatozoa

Rhabditophora

The majority of Platyhelminthes are members of Rhabditophora,

and the group is very readily recognized as monophyletic.

With the exception of members of Catenulida, the

rhabditophorans encapsulate the full diversity of the phylum.

The clade is split into a number of distinct groups that have

variously been ascribed class, ordinal, and family level status.

Apomorphies of Rhabditophora (Ehlers 1985a,

Telford et al. 2000)

Lamellated rhabdites

Duo-gland adhesive system

Duo-cell weir of the protonephridia

Multiciliary terminal cells of the protonephridia

Unusual codon usage in mitochondrial genes: AAA =

Asn not Lys, AUA = Ile not Met

Figure 14.5. Xenoturbella bocki, Xenoturbellida; redrawn from

Ax (1996).

Xenoturbella bocki

XENOTURBELLIDA

214 The Relationships of Animals: Overview

We take each of the major groups in turn. Figure 14.6

illustrates the best estimate of their interrelationships based

on both morphological and molecular evidence.

Macrostomorpha

Macrostomorphs encompass Haplopharyngida and Macrostomida,

and in almost all phylogenetic analyses they appear

as the sister group to the remaining Rhabditophora groups.

Haplopharyngida are represented by just three species, all

marine, whereas the macrostomids, with three families, 23

genera, and many hundreds of species, is much more diverse

with representatives found in marine, brackish, and freshwater.

Early competing hypotheses as to the interrelationships

of the constituent groups are founded on phylogenies

prepared on assessments of the adhesive system (Tyler 1976,

Tyler and Rieger 1977) or the construction of the pharynx

(Doe 1981). Most recently, Rieger (2001) using these features

plus the rhammites and the female canal system, offered two

alternative phylogenies, the consensus of which suggests that

complementary molecular sequencing will serve well in resolving

the interrelationships of this, perhaps most basal

rhabditophoran group. If Rhabditophora do indeed represent

the majority of flatworms (or at least the monophyletic

Platyhelminthes), this group is pivotal within the phylum

(fig. 14.7).

Apomorphies of Macrostomorpha (Doe 1986, Rieger 2001)

Duo-gland adhesive organs emerge in one collar of

modified microvilli

Pharynx simplex coronatus

Aciliary spermatozoa

Polycladida

Although some representatives of the 37 families of polyclads

live in fresh or brackish water, these generally large worms

are predominantly marine, free-living flatworms. Many are

associated with other organisms as symbionts, and tropical

representatives found on reefs include some of the most spectacularly

colorful invertebrates. Split into Cotylea, whose

members have a pseudosucker posterior to the female genital

pore, and Acotylea, whose members do not, polyclads are

often resolved as relatively deep-branching platyhelminths.

A combined morphological and molecular assessment places

the group as sister taxon to Macrostomorpha at the base of

Rhabditophora (Littlewood et al. 1999b), although molecular

data alone fail to adequately resolve monophyly of a

Polycladida + Macrostomorpha clade (Littlewood and Olson

2001). The internal relationships have yet to be tackled, but

such a phylogeny will be invaluable because the group includes

many unique larval forms, and the evolution of their

development will prove fascinating (fig. 14.7).

Apomorphies of Polycladida (Ehlers 1985a, Littlewood

et al. 1996b)

Extensive intestinal branching

Resorption of certain blastomeres during development

Characteristic plicatus-type pharynx

Figure 14.6. Interrelationships of Platyhelminthes based on

various sources.

Figure 14.7. Basal flatworm groups; images

courtesy of Queensland Museum, from

Cannon (1986), with permission. Scale bars,

200 mm.

*F+U+G = Fecampiida+Urastomidae+Genostomatidae

Rhabditophora

Catenulida

Tricladida

Prolecithophora

Rhabdocoela

Proseriata

Polycladida

Lecithoepitheliata

Macrostomida

Gyrocotylidea

Monopisthocotylea

Polyopisthocotylea

Digenea

Aspidogastrea

Eucestoda

Amphilinidea

Haplopharyngida

Macrostomorpha

Trematoda

Monogenea

Cestoda

Neodermata

F+U+G*

Catenula lemnae Macrostomum curvituba Discocelis australis Gnosonesima borealis

Protostomes and Platyhelminthes 215

Lecithoepitheliata

Of the major flatworm groups this is probably the least studied

as regarding internal phylogeny, at least in terms of modern

phylogenetic systematic methods. The worms are free-living

and are found in freshwater, marine, and terrestrial environments.

The only morphological assessment places them as the

sister group to Prolecithophora + Rhabdocoela (Littlewood

et al. 1999b), but there are no explicit autapomorphies for the

group. Composed of two families, Prorhynchidae and Gnosonesimidae,

according to Timoshkin (1991), the group has

no well-defined homology to unite it and may not even be

monophyletic. SSU rDNA data have been collected only for

one genus of Prorhynchidae, but the analyses including the

most densely sampled flatworms places the lecithoepitheliates

as a basal group united with macrostomorphs (fig. 14.7).

Proseriata

Proseriates are marine worms, predominantly interstitial but

occupying a variety of trophic levels. Seven families are recognized

and include more than 250 species. Although a recent

combined molecular assessment of Proseriata cast doubt as to

whether the group is truly monophyletic (Littlewood et al.

2000), additional evidence based on complete SSU and LSU

rDNA has since demonstrated monophyly (Lockyer et al.

2003). Three synapomorphies were erected to describe the

group, but each of these has been found to be present in nonproseriates,

and Curini-Galletti (2001) considers this sufficient

reason to focus on the constituent clades, which each have

strong autapomorphies. The two proseriate groups are Unguiphora

and Lithophora, and molecular estimates using both

complete SSU and LSU rDNA show each to be monophyletic.

Apomorphies for Unguiphora (Curini-Galletti 2001)

“Multiple” ovaries

Claw-shaped stylet

Cocoons with up to nine openings

Apomorphies for Lithophora (Curini-Galletti 2001)

One pair of compact ovaries

Sclerotized copulatory structures never claw shaped

Cocoons with one opening

Figure 14.8 depicts the interrelationships of four of the

six lithophoran families according to recent analysis (Curini-

Galletti 2001, and see discussion therein). Of the remaining

families, it seems likely that Monotoplanidae are not monophyletic

and probably fall within the Monocelididae.

Tricladida

There are more than 100 genera of triclads and many hundreds

of species. Originally considered to be sister group to

Proseriata in a clade called Seriata, Tricladida is not placed

anywhere near the proseriates by SSU rDNA. Instead, these

ubiquitous, free-living worms inhabit freshwater, brackish,

marine, and terrestrial environments and appear quite robustly

in a clade that includes Prolecithophora and a small

but remarkable group of non-neodermatan parasitic flatworms,

Fecampiida + Urastomidae + Genostomatidae (see

below and fig. 14.6). In the most densely sampled SSU rDNA

analysis, Tricladida is sister group to Prolecithophora (Littlewood

and Olson 2001), but there are no obvious morphological

synapomorphies for this grouping. The internal

relationships of Tricladida have been estimated using a variety

of gene fragments and, although requiring additional

evidence, are shown in figure 14.9 (Baguса et al. 2001, Carranza

et al. 1998). Triclads, or more commonly planarians,

include some of the best-known free-living flatworms. Many

have the ability to regenerate after being cut in two or more

pieces and are therefore excellent candidates for studies on

developmental genetics (Baguса 1998). Additionally, some,

such as Dugesiidae, appear to be potential indicators of terrestrial

biodiversity (Sluys 1999), so their phylogeny has been

investigated in some detail (Sluys 2001).

Apomorphies of Tricladida (Baguса et al. 2001,

Carranza et al. 1998, Ehlers 1985a, Littlewood

et al. 1999b)

Three-branched intestine

Two germaria located at anterior end of

germo-vitelloducts

Formation of transitory embryonic pharynx

Crossing over of pharynx muscles

Cerebral position of female gonads

Figure 14.8. Interrelationships

of Proseriata; images courtesy of

Queensland Museum, from

Cannon (1986), with permission.

Scale bars, 200 mm.

Proseriata

Coelogynoporidae

Unguiphora

Monocelididae

Otoplanidae

Archimonocelididae

Lithophora

Nematoplana ciliovesiculae

Nematoplanidae

Unguiphora

Promonotus orthocirrus

Monocelididae

Lithophora

216 The Relationships of Animals: Overview

Serial arrangement of many nephridiopores

Marginal adhesive zone

Prolecithophora

There are approximately 150 species of this group classified

into 11 or so families. The most recent assessment of prolecithophoran

interrelationships combines a predominantly

molecular approach with an assessment of sperm characters

(Jondelius et al. 2001). Not all the families have been sampled

for molecular analysis, but SSU rDNA resolves most of the

interfamilial phylogeny quite well. A combination of results

from two separate molecular studies is shown in figure 14.10

(see Jondelius et al. 2001, Littlewood and Olson 2001, and

D. T. J. Littlewood, unpubl. obs.).

Apomorphy of Prolecithophora (Ehlers 1988)

Abundantly folded membrane derivatives in the

aflagellar sperm cells

Rhabdocoela

This group originally included all remaining flatworms, a

clade composed of Dalyelliida, Temnocephalida, Kalyptorhynchia,

Typhloplanida, and Neodermata. With a single

putative morphological autapomorphy, “unspecialized pharynx

bulbosus,” molecular data consistently fail to resolve the

group as a whole, and Rhabdocoela is now restricted to the

original constituent taxa, excluding Neodermata. Consequently,

there is no apomorphy for the group, although

it seems well supported at least from SSU rDNA analyses

(Littlewood and Olson 2001, Littlewood et al. 1999b). Temnocephalida,

whose members are characterized by an epidermis

made of multiple syncytial plates (Joffe and Cannon

1998), and Dalyelliida and Typhloplanida likely form a clade

according to SSU rDNA, but their interrelationships need

further investigation; kalyptorhynchs appear consistently as

the sister group to these three taxa (Littlewood and Olson

2001, Littlewood et al. 1999b; fig. 14.11).

Little effort has been made to elucidate the interrelationships

of the constituent groups of Rhabdocoela except among

polcystid Kalyptorhynchia (Artois and Schockaert 1998) and

the Temnocephalida (Cannon and Joffe 2001). The temnocephalids

are all ectosymbiotic and have developed a distinct

posterior sucker. A recent analysis of interrelationships by

Cannon and Joffe (2001), which also includes a list of apomorphies

for the group, is shown in figure 14.11. Watson (2001)

has provided additional apomorphies from studies on sperm

and spermiogenesis for Temnocephalida and Kalyptorhynchia.

Fecampiida, Urastomidae, Genostomatidae,

and a Note on the Revertospermata

Three enigmatic groups of flatworms that have been allied

historically with the free-living taxa, but are all found in close

association with vertebrate or invertebrate hosts, were

recently thought to be members of a clade including the obligate

parasites, the Neodermata. The clade, termed Revertospermata

[so named because of a peculiar migration of the

sperm nucleus relative to sperm tail seen in neodermatans

and these taxa (Kornakova and Joffe 1999)], is not supported

by molecular data. However, Fecampiida, Urastomidae, and

Genostomatida do form a convincing clade, and molecular

data place the clade as sister to Tricladida + Prolecithophora.

A revertospermatan clade is compelling from a parasitological

perspective, uniting most of the flatworms with a close

Figure 14.9. Interrelationships of Tricladida; image courtesy of

Queensland Museum, from Cannon (1986), with permission.

Scale bar, 200 mm.

Figure 14.10. Interrelationships of

Prolecithophora; images courtesy

of Queensland Museum, from

Cannon (1986), with permission.

Scale bars, 200 mm.

Terricola

Cavernicola

Dendrocoelidae

Dugesiidae

Planariidae

Maricola

Tricladida

Dugesia gonocephala

Dugesiidae

Prolecithophora

Scleralophoridae

Plagiostomidae

Protomonotresidae

Ulianinidae

Cylindrostomidae

Pseudostomidae

Baicalarctiidae

Baicalarctia gulo

Baicalarctiidae

Allostoma pallidum

Cylindrostomidae

Protostomes and Platyhelminthes 217

association with invertebrate and/or vertebrate hosts, but

remains controversial.

Neodermata

The major obligate parasite groups of the Platyhelminthes

(i.e., the Cestoda, Trematoda, and Monogenea) have often

been thought distinct enough not to be closely related.

Bychowsky (1937), for example, postulated that Trematoda

and Cestoda/Monogenea or Cercomeromorphae were each

derived independently from Rhabdocoela. Other authors

have been in favor of even more disparate origins, with Digenea

not even being flatworms (Sinitsin 1911) or having a

common ancestor with the Mesozoa (Wright 1971) and

Cestoda being derived from poriferan-like forms (Ubelaker

1983)!

The first detailed cladistic treatments of the phylum Platyhelminthes

by Ehlers (1984, 1985a, 1985b) and Brooks et al.

(1985b) produced strong evidence for the monophyly of

these parasites, for which Ehlers (1984) coined the name

Neodermata, referring to the replacement of the epidermis

during ontogeny. Later work, particularly molecular phylogenies

(e.g., Baverstock et al. 1991, Blair 1993, Littlewood

et al. 1999b, Rohde et al. 1993) have provided further evidence

of this monophyly, although some studies (Joffe and

Kornakova 2001, Rohde 2001) have thrown doubt on some

of the original apomorphies. Littlewood et al. (1999b) considered

the monophyly of the Neodermata “beyond doubt,”

and Joffe and Kornakova (2001) considered this problem

“finally solved,” citing as evidence three unique insertions in

the SSU rDNA sequence.

Apomorphies of Neodermata (Brooks et al. 1985b, Ehlers

1984, 1985a, 1985b, Littlewood et al. 1999b)

Multiciliated ectoderm is limited to “larval” stages and

is shed later and replaced by syncytial neodermis

with subepidermal perikarya each separately

connected to surface layer

Protonephridia with a two-cell weir

Epidermal locomotory cilia with single, cranial rootlet

Epithelial sensory receptors with electron-dense collars

Complete incorporation of both axonemes is sperm

body

Two long and one short insertions in SSU rDNA

sequence ( Joffe and Kornakova 2001)

The relationships of the major groups within the Neodermata

are becoming well accepted, although new molecular

data may add some confusion. Neodermata consist of two

sister groups, Cercomeromorphae (i.e., Cestoda + Monogenea)

and Trematoda (fig. 14.12a). The separateness and

main constituents of these taxa were recognized as early as

Baer (1931) and Bychowsky (1937), although recognition of

their joint monophyly awaited cladistic study (see above).

Although almost all recent morphological (Brooks et al.

1985b, Ehlers 1985b, Zamparo et al. 2001) and molecular

(Baverstock et al. 1991, Littlewood and Olson 2001, Littlewood

et al. 1999b) analyses agree with this dichotomy, a

recent study using LSU rDNA sequences indicated the relationship

(Trematoda, Cestoda) Monogenea (Lockyer at al.

2003; fig. 14.12b,c)]. This unusual result relies solely on data

from one gene, and until corroborated, Cercomeromorphae

continue to be recognized. The monophyly of the Monogenea

is discussed below.

Cercomeromorphae

Janicki (1930), on the basis that the digenean cercarial tail, the

monogenean opisthaptor, and the cestode cercomer are homologues,

erected the taxon Cercomeromorphae. The name

is now used for the taxon including Monogenea and Cestoda,

with the posterior hooklets as the major innovation.

Apomorphy of Cercomeromorphae (Littlewood et al. 1999b)

Posterior hook of larva and adults (ancestrally probably

16 hooks)

Figure 14.11. Interrelationships of Rhabdocoela; images courtesy of Queensland Museum, from

Cannon (1986), with permission. Scale bars, 200 mm.

Temnocephala semperi

Temnocephalidae

Temnocephalida

Rhabdocoela

Proxonetes ampullatus

Trigonostomidae

Typhloplanida

Gyratricella attemsi

Polycystidae

Kalyptorhynchia

Provortex balticus

Provorticidae

Dalyellida

Temnocephalida

Typhloplanida

Dalyelliida

Kalyptorhynchia

Temnocephalidae

Scutarielloidea

Diceratocephalidae

Actinodactylellidae

Didymorchiidae

Temnocephalida

218 The Relationships of Animals: Overview

Monogenea = Monogenoidea

Members of Monogenea, occasionally referred to as Monogenoidea,

are as diverse as any of the obligate flatworm parasites

despite using only single hosts in their life cycle.

Predominantly ectoparasites of marine and freshwater teleost

fishes, usually clinging to species-specific regions of the outer

surfaces of gills and body, some groups have successfully

exploited a wide range of aquatic vertebrates, including elasmobranchs,

dipnoi, teleosts, amphibians, and even the

hippopotamus. The monophyly of the group has been challenged

by molecular data (Justine 1998, Littlewood et al.

1999a, Mollaret et al. 1997) and some sperm morphology

(Justine 1993), but neither challenge has been conclusive.

Indeed, the rates of evolution of both SSU and LSU rDNA,

both of which suggest paraphyly, are so different between

the major constituent groups of Monogenea that additional

molecular evidence is required to solve the problem (Olson

and Littlewood 2002). It seems likely that, whether monophyletic

or paraphyletic, members of Monogenea radiated

very rapidly from their ancestral stock. Morphology alone

suggests monophyly (Littlewood et al. 2001a; fig. 14.12a),

complete SSU suggests paraphyly but monophyly of the

Cercomeromorphae (Littlewood et al. 2001a; fig. 14.12b),

partial LSU suggests paraphyly and non-monophyly of the

Cercomeromorphae (Mollaret et al. 1997), and complete LSU

suggests monophyly of Monogenea and non-monophyly of

Cercomeromorphae (Lockyer et al. 2003; fig. 14.12c).

Apomorphies of Monogenea (Boeger and Kritsky 2001)

Larva with three ciliated zones

Larva and adult with two pairs of pigmented eyes

One pair of ventral anchors

One egg filament

As with other parasitic flatworms, members of Monogenea

possess attachment organs, and as appropriate for

ectoparasites, these can be quite elaborate with various arrangements

of suckers, hooks, and anchors. Monogenea

have anterior and posterior structures, and it is predominantly

the structure of the posterior organ that delineates

the two major constituent groups: Polyonchoinea and

Heteronchoinea. The naming of these two groups is as hotly

debated as their interrelationship, but at least each group

is recognized as being monophyletic. Polyonchoinea, most

commonly referred to as Monopisthocotylea, are supported

by eight synapomorphies, and Heteronchoinea, composed

of the Polystomatidae, Sphyranuridae, and Polyopisthocotylea,

are supported by six (Boeger and Kritsky 2001; see

fig. 14.13). The interrelationships of families are based on

a multitude of adult features and, to a lesser extent, the

unique larval form called the oncomiracidium. Boeger and

Kritsky are responsible for much of the modern morphologically

based phylogenetic systematic (i.e., cladistic) work

on Monogenea, and their publications provide a review of

characters, hypotheses on interrelationships, and interpretations

based on host associations (Boeger and Kritsky

1993, 1997, 2001); their most recent estimate of interrelationships

is shown in figure 14.13. A recent analysis of interrelationships

based on molecular evidence is given by

Olson and Littlewood (2002).

Cestoda

This taxon includes all gutless tapewormlike groups, including

those in which no serial repetition of the genitalia occurs.

Xylander (2001) enumerated eight autapomorphies as evidence

of the monophyly of Cestoda. Some workers have

doubted the monophyly of the group, including Ubelaker

(1983), who found it “tempting” to propose an early

poriferan-like ancestor and went as far as considering “Cestoidea”

a phylum, which did not include Gyrocotylidea or

Amphilinidea. More recent morphological and molecular

evidence, however, supports the monophyly of these groups

(Brooks et al. 1985b, Ehlers 1985a, Littlewood et al. 1999b,

Zamparo et al. 2001).

Apomorphies of Cestoda (Xylander 2001)

All stages without intestine

Neodermis with distinct type of microvilli (microtriches,

microthrix)

Figure 14.12. Interrelationships of the Neodermata: competing hypotheses (a–c) based on

morphology and molecular data.

Gyrocotylidea

Monopisthocotylea

Polyopisthocotylea

Digenea

Aspidogastrea

Eucestoda

Amphilinidea

Trematoda

Cestoda

Monogenea

Monogenea

Gyrocotylidea

Monopisthocotylea

Polyopisthocotylea

Digenea

Aspidogastrea

Eucestoda

Amphilinidea

Trematoda

Cestoda

Gyrocotylidea

Monopisthocotylea

Polyopisthocotylea

Digenea

Aspidogastrea

Eucestoda

Amphilinidea

Trematoda

Cestoda

Monogenea

a. morphology b. complete SSU rDNA c. complete LSU rDNA

Protostomes and Platyhelminthes 219

First canal cell of protonephridium lacks cell gap and

desmosome

Reticulate protonephridial system in postlarvae

Cell bodies of protonephridial canal cells under basal

lamina

Larval epidermis is syncytial, neodermal tissue does

not reach body surface

10 larval hooks (Littlewood et al. 1999b)

Large body dimensions

Apical pit forms when in first host

Male copulatory organ a cirrus

Vertebrate host in life cycle

Gyrocotylidea

Gyrocotylideans are a small group (~10 species in one genus)

of monozoic worms found exclusively in the stomach

of holocephalan fishes. They are large worms, which normally

occur in pairs, attach by a posterior rosette organ,

which has complex folds that mesh with the folds of the

stomach wall (Bandoni and Brooks 1987b). The life cycle

is not known, but larval forms are found embedded in the

parenchyma of adults. Some early workers have considered

gyrocotylideans to be monogeneans, claiming that the

rosette is the homologue of the monogenean opisthaptor

(Williams et al. 1987). The consensus opinion on the

position is now that it is a basal cestode, based on morphological

apomorphies (Bandoni and Brooks 1987b) and

molecular results.

Apomorphies of Gyrocotylidea (Xylander 2001)

Lycophore (larva) epidermis without nuclei

Parasite of Holocephali

Parenchymatic postlarvae

Neodermal spine shape

No intraepithelial multiciliary sensory structures

Caudal rosette organ

Apical proboscis

Figure 14.13. Interrelationships

of Monogenea with autapomorphies

for Polyonchoinea and

Heteronchoinea, redrawn from

(Boeger and Kritsky, 2001).

Images courtesy of John Wiley

and Sons, Inc., with permission

from Yamaguti (1963).

Monocotylidae

Loimoidae

Dionchidae

Capsalidae

Lagarocotylidae

Euzetrema

Montchadskyellidae

Tetraonchoididae

Acanthocotylidae

Bothitrematidae

Udonellidae

Gyrodactylidae

Anoplodiscidae

Calceostomatidae

Neodactylodiscidae

Amphibdellatidae

Dactylogyridae

Diplectanidae

Pseudomurraytrematidae

Tetraonchidae

Sundanonchidae

Neotetraonchidae

Polystomatidae

Sphyranuridae

Chimaericolidae

Diclybothriidae

Hexabothriidae

Plectanocotylidae

Mazocraeidae

Mazoplectidae

Discocotylidae

Diplozoidae

Anthocotylidae

Pseudodiclidophoridae

Octomacridae

Chauhaneidae

Protomicrocotylidae

Gotocotylidae

Gastrocotylidae

Neothoracocotylidae

Bychowskycotylidae

Allodiscocotylidae

Rhinecotylidae

Pseudomazocraeidae

Hexostomatidae

Axinidae

Microcotylidae

Heteraxinidae

Diplasiocotylidae

Pterinotrematidae

Diclidophoridae

Allopyragraphoridae

Pyragraphoridae

Heteromicrocotylidae

POLYONCHOINEA HETERONCHOINEA

14 marginal, 2 central hooks in oncomiracidium

14 marginal, 2 central hooks in adult

bilateral osmoregulatory canals fused anteriorly

sclerotized male copulatory organ

dorsoventral microtubules absent in spermatozoan

intercentriolar body absent

striated rootlets absent

single testis (also in Octomacridae and Diplozoidae)

presence of a genitointestinal canal

2 ventrolateral ductus vaginalis

4 haptoral suckers associated with hooks

lateral microtubules in the spermatozoan

?

Benedenia sekii

Capsalidae

Choricotyle chrysophryi

Diclidophoridae

Neopolystoma orbiculare

Polystomatidae

220 The Relationships of Animals: Overview

Nephroposticophora (Amphilinidea + Eucestoda)

This relatively recently recognized group contains two superficially

dissimilar groups, the amphilinids and the “true”

tapeworms. It was originally recognized on morphological

grounds (Bandoni and Brooks 1987a, Ehlers 1985a) and has

been confirmed by several molecular studies (Littlewood et al.

1999a, Littlewood and Olson 2001).

Apomorphies of Nephroposticophora (Xylander 2001)

Unpaired excretory pore at postlarval posterior end

Larger nephridioduct unciliated

Amphilinidea

This small group (about eight genera, 20 species) consists of

leaflike monozoic forms found in the body cavity of chondrosteans,

teleosts, and freshwater chelonians (Bandoni and

Brooks 1987a). Crustaceans are used as intermediate hosts.

Some early workers (see Gibson et al. 1987, Janicki 1930)

considered amphilideans to be paedomorphic eucestode

plerocercoids, but later morphological (Brooks et al. 1985a,

Ehlers 1985a, Zamparo et al. 2001) and molecular (e.g.,

Baverstock et al. 1991, Littlewood et al. 1999a, 1999b, Littlewood

and Olson 2001) evidence has shown that they are very

likely to be the sister taxon to Eucestoda.

Apomorphies of Amphilinidea (Xylander 2001)

All stages coelomic parasites

Neodermal microvilli short and stubby

Uterus tripartite

Uterine pore at anterior end

Leaflike shape

Characteristic apical organ

Eucestoda (Cestoidea)

The Eucestoda, or “true” tapeworms, are a large group of

750 genera and up to 5000 species and includes all the

forms with proglottidization and segmentation as well as

the monozoic Caryophyllidea. Hoberg et al. (1999) reckoned

that true cestodes arose in basal teleosts and subsequently

have spread to elasmobranchs (where numerous

groups are found) and tetrapods. Numerous life cycles are

known (Beveridge 2001), giving evidence that arthropods

are the primitive intermediate host, which has been lost in

some terrestrial cestodes. With the exception of Caryophyllidea

and Spathebothriidea, the eucestodes are segmented.

They may be tiny with few segments or huge with

thousands of segments (in whales some tapeworms grow

to many tens of meters in length). The anterior attachment

organ, the scolex, has many forms and may use suckers,

hooks, proboscides, muscular pads, or folded ridges to

adhere to the intestinal wall of the host. Each segment contains

a full set of hermaphroditic sexual organs such that

vast numbers of eggs may be produced in the lifetime of

the worm (the human tapeworm Diphyllobothrium latum is

said to shed up to one million eggs per day). The serial repetition

of sexual organs (proglottidization) may not always

be reflected in surface segmentation, but it usually is.

The phylogeny of Eucestoda is probably better developed

than any of the other equivalent platyhelminth groups, and

the major internal taxa tend to be more satisfactorily delimited.

Brooks et al. (1991) and Hoberg et al. (1999, 1997) have

presented morphological phylogenies, Mariaux (1998) and

Olson and Caira (1999) produced molecular phylogenies

(summarized by Mariaux and Olson 2001) and Hoberg et al.

(2001) and Olson et al. (2001) used combined evidence.

A consensus is appearing on several significant features of

cestode phylogeny, including the possibility that some

apparently well-established groups (e.g., Tetraphyllidea,

Pseudophyllidea) are not monophyletic (fig. 14.14). The

monozoic Caryophyllidea are now recognized as the basal

eucestodes and it is likely that internal proglottidization developed

before external segmentation (Olson et al. 2001).

Apomorphies of Eucestoda (Xylander 2001)

Neodermis with typical microtriches

Spermatozoa without mitochondria

First larval stage without sensory structures and

cerebrum

Reduction of several tissues and organs in the primary

larval stage (coracidium)

Cercomer shed during larval development

Six caudal hooks

Note that proglottidization and segmentation are not apomorphies,

because they are lacking in the Caryophyllidea.

Trematoda

This taxon, erected in 1808, was recognized as containing

both the ectoparasitic and the endoparasitic flukes, until Baer

(1931) and Bychowsky (1937) proposed that the ectoparasitic

Monogenea was closer to Cestoda. Trematoda is now

recognized to contain two sister taxa, Aspidogastrea and

Digenea. Early workers have postulated that Aspidogastrea

were derived from within Digenea (Cable 1974, Poche 1926),

but morphological (Brooks et al. 1985b, Ehlers 1985a, Gibson

1987, Pearson 1992), molecular (Blair 1993, Littlewood and

Olson 2001), and combined (Cribb et al. 2001, Littlewood

et al. 1999b) evidence strongly indicates the sister-group relationship

of the taxa (fig. 14.15).

Apomorphies of Trematoda (Littlewood et al. 1999b)

Ciliated epidermal cells of larva separated by cytoplasm

of neodermis

Male copulatory organ a cirrus

Molluscan first host

Protostomes and Platyhelminthes 221

Aspidogastrea

This small group (~12 genera, 80 species) is generally considered

uncontroversially monophyletic, although the constituent

genera are morphologically diverse (Rohde 2001).

Despite the relatively small number of species, they are found

as adults in lamellibranchs, gastropods, holocephalans, elasmobranchs,

teleosts, and chelonians. A mollusk-inhabiting

stage is present in all known life cycles, and the presence of

aspidogastrean adults in mollusks is considered facultative

by Rohde (2001). The series of alveoli on the adhesive disk

or the rows of suckers on the ventral surface are considered

evidence of “pseudosegmentation” by Rohde (2001). Molecular

evidence confirms the basal status of Rugogastridae

(fig. 14.15).

Apomorphies of Aspidogastrea (Littlewood et al. 1999b)

Larva (cotylocidium) with ventrocaudal sucker,

becoming alveolated adhesive organ in adults

Few ciliated cells in larvae

Neodermis with characteristic microvilli

(= microtubercles)

Digenea

This is the largest group of flatworms, with some 18,000

nominal species and more than 2700 genera. Adults are

found in all types of jawed vertebrates, although they are less

common in elasmobranchs (Bray and Cribb 2003). The life

cycle is complex, usually with three hosts in sequence. The

first host is a mollusk, in which the parasite reproduces asexually,

producing numerous motile free-living cercariae (Cribb

et al. 2001). Infection of the final host is usually by way of

ingestion of a second intermediate host, which may be an

invertebrate or a vertebrate. The asexual reproduction in the

mollusk ensures the large number of offspring necessary for

such a precarious lifestyle. The relationship with the mollusk,

which they share with the aspidogastreans, has been

thought to be the primitive parasitological association in the

group, the vertebrate host having been acquired later. The

fact that all neodermatan groups parasitize vertebrates, and

that Neodermata is now convincingly demonstrated as

monophyletic, suggests, on the other hand, that the association

with the vertebrate is more primitive.

Digenea are considered to be clearly monophyletic, with

several convincing apomorphies. Relationships within the

taxon are less defined and are still controversial (e.g., Brooks

et al. 1985a, Pearson 1992). Molecular results and combined

molecular and morphological analyses (Cribb et al. 2001) do

not resolve the basal digeneans unequivocally. Early suggestions

that Heronimidae consist of basal digeneans (Brooks

et al. 1985a) have been criticized (Gibson 1987, Pearson

1992) and are at odds with most molecular results (Barker

et al. 1993, Cribb et al. 2001; but see Campos et al. 1998).

Cribb et al. (2001), using morphological, molecular, and

combined evidence approaches found different topologies.

In the molecular and combined evidence results (fig. 14.15),

Figure 14.14. Interrelationships of the major cestode groups redrawn from Olson et al. (2001);

images courtesy of Willi Xylander from Westheide and Rieger (1996) and courtesy of Taylor and

Francis from Williams and Jones (1994) with permission.

Caryophyllidea

Spathebothriidea

Haplobothriidea

'Pseudophyllidea'

'Pseudophyllidea'

Diphyllidea

'Trypanorhyncha'

'Trypanorhyncha'

Lecanicephalidea

Litobothriidea

'Tetraphyllidea'

'Tetraphyllidea'

'Tetraphyllidea'

Proteocephalidea

'Tetraphyllidea'

Cyclophyllidea

Tetrabothriidea

Nippotaeniidea

AMPHILINIDEA

GYROCOTYLIDEA

EUCESTODA

Caryophyllaeus

Caryophyllidea

Cyathocephalus

Spathebothriidea

Taenia solium

Cyclophyllidea

Nesolecithus africanus

Amphilinidea

Gyrocotyle fimbriata

Gyrocotylidea

scolex

222 The Relationships of Animals: Overview

Figure 14.15. Interrelationships of Trematoda, including Aspidogastrea, redrawn from Rohde

(2001), and Digenea, redrawn from Cribb et al. (2001). Inset shows life cycle of the most

common digenean, Derogenes varicus. Schistosomes, causative agents of schistosomiasis, are some

of the few flatworms with separate sexes, here shown in copula; image courtesy of Vaughan

Southgate and Kluwers, from Southgate et al. (1990) with permission.

the clade (Diplostomoidea + Schistosomatoidea) was found

basal, whereas various morphological analyses, based on

different premises, resolved Transversotrematidae and

Bivesiculidae as basal. A resolution of this point is crucial to

our understanding of the evolution of Digenea because members

of Transversotrematidae are ectoparasites and those of

Bivesiculidae lack suckers. Included in the group are the most

medically important flatworms, the schistosomes. Members

of Schistosomatidae infect one species of crocodile and many

species of birds and mammals, and among humans, five spe-

Strigeidae

Diplostomidae

Schistosomatidae

Sanguinicolidae

Transversotrematidae

Bivesiculidae

Fellodistomidae

Tandanicolidae

Heronimidae

Azygiidae

Hemiuridae

Lecithasteridae

Syncoeliidae

Accacoeliidae

Didymozoidae

Derogenidae

Sclerodistomidae

Notocotylidae

Angiodictyidae

Mesometridae

Diplodiscidae

Paramphistomidae

Haplosplanchnidae

Cyclocoelidae

Philophthalmidae

Echinostomatidae

Fasciolidae

Cryptogonimidae

Heterophyidae

Opisthorchiidae

Lepocreadiidae

Enenteridae

Gyliauchenidae

Apocreadiidae

Monorchiidae

Atractotrematidae

Haploporidae

Acanthocolpidae

Campulidae

Nasitrematidae

Dicrocoeliidae

Gorgoderidae

Orchipedidae

Bucephalidae

Paragonimidae

Opecoelidae

Opistholebetidae

Cephalogonimidae

Brachycoeliidae

Plagiorchiidae

Microphallidae

Pachypsolidae

Faustulidae

Zoogonidae

Stichocotylidae

Aspidogastridae

Multicalycidae

Rugogastridae

DIGENEA

ASPIDOGASTREA

Orthosplanchnus arcticus

Campulidae

Gymnophallus somateriae

Gymnophallidae

Catatropis verrucosa

Notocotylidae

Multicalyx elegans

Multicalycidae

Schistosoma nasale

Schistosomatidae

Cotylogaster occidentalis

Aspidogastridae

Life-cycle of Derogenes varicus (Hemiuridae)

2 3 4 9

5

7

6

8

1

1 snail: Natica spp.

2 calanoid copepod

3 harpacticoid copepod

4 hermit crabs,

barnacles

5 chaetognaths

6 small fishes

7 planktophagous

fishes

8 benthophagous &

piscivorous fishes

9 piscivorous fishes

TREMATODA

- ciliated epidermal cells of larva

separated by cytoplasm of neodermis

- male copulatory organ a cirrus

- molluscan first host

(male with female in gynecophoric canal)

Protostomes and Platyhelminthes 223

cies cause various forms of schistosomiasis, a debilitating

disease affecting more than 200 million people worldwide

but predominantly in the tropics.

Apomorphies of Digenea (Cribb et al. 2001,

Littlewood et al. 1999b)

Series of asexual generations in first intermediate

(mollusk) host

Ciliated epidermal cells of miracidium arranged in

regular transverse rows

Jawed vertebrates in complex life cycle

Cercaria

Miracidium and mother sporocyst without digestive

system

Nemertea: The Ribbonworms

There are currently about 1000 recognized species of nemerteans.

Their eversible (inside-out) proboscis used in food

capture and, in some cases locomotion, is perhaps the most

obvious unique character of this phylum; the proboscis is

separate from the gut and is connected to a rhynchocoel,

which serves to evert it rapidly through hydrostatic pressure

(Senz 1995). These predominantly marine worms (some are

found in freshwater and even in damp terrestrial environments)

are often brightly colored and can be extremely long

and thin, up to 30 m in the case of the appropriately named

Lineus longissimus. Their great length perhaps could not be

achieved without a circulatory system to distribute nutrients

throughout the body, and this is their second key innovation:

a closed blood system. Uniquely for invertebrates, their

blood vessels are lined with a cellular epithelium rather than

the more usual nonepithelial basement membrane (Ruppert

and Carle 1983). Their embryonic development is similar to

that of classic spiralians such as annelids and mollusks, and

some groups have a trochophore-like larval stage known as

a pilidium (Nielsen 2001).

Nemertea have traditionally been considered acoelomate

animals and have consequently been associated with the

acoelomate platyhelminths as an early branch within Bilateria

(Nielsen 2001). Ultrastructural analyses, however, have convincingly

homologized their closed circulatory system and

rhynchocoel with the coelomic cavities of other invertebrates,

showing they are not in fact acoelomate (Turbeville and Ruppert

1985). Molecular studies (both of SSU and LSU rRNA

and Hox genes) strongly support this contention and link the

nemerteans with other coelomate protostomes with spiral

cleavage and trochophore-type larvae such as the annelids,

mollusks, sipunculids, and echiurans as well as with Platyhelminthes

(Turbeville et al. 1992).

Within the phylum, two classes have been recognized on

the basis of morphology: Anopla, whose members have a post

oral brain and an unarmored proboscis, and Enopla, whose

members have a postoral brain and often have a proboscis

armored with stylets. Both classes are further divided into

two orders: Palaeonemertea and Heteronemertea within

Anopla, and Hoplonemertea and Bdellonemertea within

Enopla (Meglitsch and Schram 1991).

Molecular phylogenetic analysis supports some aspects

of these traditional divisions. In an analysis of SSU rRNA

sequences from 15 species representing all four classes,

Enopla, Hoplonemertea, and Bdellonemertea were robustly

grouped. This analysis suggested, however, that Anopla is

paraphyletic (Sundberg and Saur 1998, Sundberg et al. 1998,

2001; see fig. 14.16).

Figure 14.16. Interrelationships of Nemertea.

Bdellonemertea

Hoplonemertea

Heteronemertea

Palaeonemertea

Enopla

Anopla

Antiponemertes pantini

Hoplonemertea

224 The Relationships of Animals: Overview

Apomorphies of Nemertea

Reversible proboscis and rhynchocoel

Closed blood system lined with epithelium

Great powers of regeneration

Rotifera and Acanthocephala (Syndermata):

Rotifers and Thorny-Headed Worms

Syndermata is the name given to the taxon that includes the

two phyla Rotifera (the rotifers) and Acanthocephala (the

thorny-headed worms; fig. 14.17). Almost 2000 species have

been described within each group. Rotifers, at one time

known as “wheel-animalcules,” are common members of the

microscopic fauna in freshwater. They are extremely tiny, at

one time considered the “smallest of all Metazoa” (Borradaile

et al. 1963). On the other hand, acanthocephalans are robust

worms, up to 1 m long, and are obligate parasites of

vertebrates.

Apomorphies of Syndermata (Wallace et al. 1996,

Zrzavэ 2001)

Syncytial integument with intrasyncytial skeletal

lamina (includes Micrognathozoa)

Anteriorly directed sperm flagella (shared with

Myzostomida)

Sperm has acrosome

Primordial germ cells invaginated separately before

gastrulation

Loss of cilia in protonephridial canals

Jaw characters (shared with Gnathostomulida and

Micrognathozoa, lost in Acanthocephala)

Zrzavэ (2001) listed five morphological characters used

as evidence for the close relationship (monophyly) of Acanthocephala

and Rotifera, jointly forming Syndermata

(= Trochata). Gene trees based on SSU rDNA sequences

(Garcнa-Varela et al. 2000, Near et al. 1998) provide further

evidence for this conclusion. Garcнa-Varela et al. (2000)

found statistically significant evidence for Acanthocephala

as a sister group to Eurotatoria (Bdelloidea + Monogononta).

Rotifera, however, consists of Eurotatoria and Seisonida (Garey

et al. 1998, Melone et al. 1998), and evidence from a heatshock

protein gene (Hsp82; Mark Welch 2000) indicates

that, whereas Acanthocephala are the sister group to Eurotatoria,

Seisonidea may be the sister group to Acanthocephala

+ Eurotatoria, meaning that acanthocephalans are

rotifers. This is in conflict with earlier evidence, based on

relatively few SSU rDNA sequences, that Acanthocephala

are the sister group of Bdelloidea (Garey et al. 1996), forming

Lemniscea. The morphological evidence for the monophyly

of Lemniscea is also disputed (Ricci 1998). Zrzavэ

(2001) reckoned that monophyly of Seisonida + Acanthocephala

is supported by morphological data and possibly

Figure 14.17. Interrelationships

of Syndermata and their

proposed relationships among

Platyzoa. Image of Myzostoma

courtesy of Igor Eeckhaut,

reproduced with permission.

Catenulida

ROTIFERA

SYNDERMATA

Rhabditophora

Gnathostomulida

Gastrotricha

Cycliophora

Myzostomida

Monogononta

Seisonida

Bdelloida

Acanthocephala

PROSOMASTIGOZOA

Seisonidea

Habrotrochidae

Monogononta

Adinetidae

Philodinidae

Philodinavidae

Eurotatoria

Bdelloidea

ROTIFERA

Palaeacanthocephala

Archiacanthocephala

Eoacanthocephala

ACANTHOCEPHALA

Myzostoma ambiguum

MYZOSTOMIDA

Seison grubei

ROTIFERA

Acanthocephalus lucidus

ACANTHOCEPHALA

Protostomes and Platyhelminthes 225

by SSU rDNA, forming Pararotatoria, a sister group to Eurotatoria

in Syndermata.

The internal phylogeny of Acanthocephala appears quite

well resolved. Molecular evidence (Garcнa-Varela et al. 2000,

Near et al. 1998) indicates the relationship Archiacanthocephala

(Eoacanthocephala, Palaeacanthocephala) for its

major subgroups. The detailed morphological analysis of

Monks (2001) also finds Eoacanthocephala and Palaeacanthocephala

monophyletic and sister taxa but finds Archiacanthocephala

paraphyletic and with its constituent species

basal to the other groups. Herlyn (2001) provided further

evidence for the monophyly of Eoacanthocephala in recognizing

the apomorphic status of the epidermis cone in this

group.

Cycliophora

Composed of a single species (Symbion pandora, an ectocommensal

of the Norway lobster Nephrops norvegicus measuring

only 350 mm), this recently discovered phylum has been

shown to have syndermatan affinities using both SSU rDNA

(Giribet et al. 2000, Winnepenninckx et al. 1998) and morphology

(Funch and Kristensen 1995, Sшrensen et al. 2000).

Cycliophora may be the sister group to Entoprocta, sharing

the presence of mushroom-shaped extensions into the epidermis,

originating from the basal lamina, according to

Sшrensen et al. (2000), or from a combined molecular and

morphological analysis the sister group of Syndermata in

Platyzoa (Giribet et al. 2000; fig. 14.17). Unique features

include an anterior feeding region termed the buccal funnel

and a complicated life cycle with distinct sexual and asexual

phases and chordoid and pandora larval forms (Funch 1996).

Myzostomida

Myzostomida are composed of about 150 species, and all

are symbionts on echinoderms, predominantly Crinoida.

Through this lifestyle, they have become adapted so uniquely

that it is difficult to place the group among the Metazoa. The

animals are incompletely segmented, acoelomate, have five

pairs of parapodia with chaetae, and exhibit a trochophore

larva (see Eeckhaut et al. 2000). Morphology has dictated an

annelid affiliation, although sperm morphology and cladistic

analyses have variously placed them in a clade including

the Sipuncula, Echiura, and Annelida (Haszprunar 1996a),

within the polychaete annelids (Rouse and Fauchald 1997),

and in a clade including the Echiura, Pogonophora, and

Annelida (Zrzavэ et al. 1998). A recent but relatively sparsely

sampled molecular study using the gene for EF-1a protein

suggests that Myzostomida are sister group to Platyhelminthes

(Eeckhaut et al. 2000), although some doubt has been

cast on this (Littlewood et al. 2001b), not least because no

syndermatan taxa were included. The latest study combining

SSU rDNA, morphology, life cycle, and developmental

data places them as sister group to Cycliophora closely related

to the Rotifera + Acanthocephala (Syndermata) clade

(Zrzavэ et al. 2001). This latter study appears to be the most

exhaustive to date and is summarized in figure 14.17.

Chaetognatha: The Arrow Worms

The chaetognaths, or arrow worms, comprise a small, extremely

homogenous phylum (150–200 species) of strictly

marine worms. The majority are planktonic, and they occur

in huge numbers in the entire world’s oceans, where they are

important predators, eating large numbers of copepods and

fish fry. They have a torpedo-shaped body with one or two

fins laterally and a dorsoventrally flattened tail fin with which

they can propel themselves rapidly. They have large numbers

of sensory bristles on their bodies and anterodorsal eyes

that combine to enable them to find their prey, which they

grab with their impressive chitinous jaws.

Charles Darwin described the chaetognaths as being “remarkable

. . . from the obscurity of their affinities,” and this

remains true today (Darwin 1844). Because of similarities

in embryology (radial cleavage, deuterostomous mouth formation,

and formation of the mesoderm and coeloms by

outpocketing of the archenterons), they were long considered

relatives of the deuterostomes. Molecular studies have

rejected this possibility, but because of the fast rate of evolution

of their rRNA genes relative to most other animals, a

more accurate placement has not been possible (Telford and

Holland 1993). Halanych (1996) study of SSU linked them

to the nematodes, but this may be due to long-branch

attraction. Littlewood et al. (1998) likewise grouped

them with the nematodes and gnathostomulids within the

ecdysozoan clade. By contrast, other authors have linked

the chaetognaths to other phyla with similar jaws (e.g.,

rotifers and gnathostomulids within Lophotrochozoa,

Nielsen 2001).

Within the phylum a single extant class is recognized:

Sagittoidea (Bieri 1991, Casanova 1985, Tokioka 1965a,

1965b). The main division within Sagittoidea is among

three orders: Monophragmophora, Biphragmophora, and

Aphragmophora, the first two of which have a transverse

sheet of muscle (phragma) crossing the body (Bieri 1991,

Casanova 1985, Tokioka 1965a, 1965b). A single molecular

study of a rapidly evolving portion of the LSU from

26 species lends support to the division between Phragmophora

and the other two orders, at least for the species

sampled, but was unable to determine reliably further divisions

with the phylum (Telford and Holland 1997). This

partial LSU study suggested that all extant chaetognaths

derive from a relatively recent radiation, and the close grouping

of SSU sequences from members of the Aphragmophora

and Biphragmophora supports this view (Halanych 1996;

fig. 14.18).

226 The Relationships of Animals: Overview

Apomorphies of Chaetognatha

Mesoderm and coelom formation by enterocoely

Chitinous retractable jaws

Multilayered epithelium on body

Cephalic hood

Retrocerebral organ and ciliary loop of unknown

function

Ecdysozoa

The segmented, coelomate arthropods were long thought by

most zoologists to be most closely related to the segmented,

coelomate annelids. Analyses of SSU, most notably that of

Aguinaldo et al. (1997), have radically revised this view. It

now seems that the closest relatives of the arthropods is

an assortment of pseudocoelomate worms: Nematoda and

Nematomorpha (probably grouped together as Nematoida),

and Priapulida, Kinorhyncha, and Loricifera (probably related

within Cephalorhyncha). This entire assemblage (including

the arthropods) has been termed Ecdysozoa because

of the common character of ecdysis or periodic molting

(Aguinaldo et al. 1997). It follows that the annelid and arthropod

shared characters are either primitive within the

Metazoa or convergently derived in these two groups.

There is corroboration of the SSU results from a recent

study of the LSU molecule (Mallatt and Winchell 2002). In

addition, the nematodes share with the arthropods an unusual

triplicated b-thymosin molecule found nowhere else

in the Metazoa (Manuel et al. 2000). Common characteristics

of Hox gene amino acid sequences also support the

ecdysozoan clade (de Rosa et al. 1999, Telford 2000), as does

examination of the binding of an anti-HRP (horseradish peroxidase)

antibody that stains the nervous system only in

ecdysozoans (Haase et al. 2001). Potentially contradictory,

however, is the discovery of a fusion of prolyl and glutamyl

transfer RNA synthetase genes common to the arthropod

Drosophila melanogaster and vertebrates but unfused in the

nematode Caenorhabditis elegans and in outgroups. This observation

needs investigating in other potential ecdysozoan

phyla (Berthonneau and Mirande 2000). Other contradictory

evidence comes from Blair et al.’s (2002) study of 100

genes. Although in some sense less reliable because of the

small number of taxa sampled, these authors reject the idea

of a monophyletic ecdysozoan clade.

Apomorphies of Ecdysozoa

Lack of primary ciliated trochophore type larva

Chitinous cuticle molted under influence of

ecdysteroid hormones

Lack of locomotory cilia

Radial cleavage (may be primitive within Metazoa)?

Relationships within Ecdysozoa

There is no consensus regarding the relationships of the

ecdysozoan phyla. The nematodes and nematomorphs have

long been considered related, and some have even suggested

that the nematomorphs are derived from within the nematodes

and are sister group of the mermithoids, which are also

parasites of arthropods. This is not supported by analyses of

SSU rDNA, which do, however, support the monophyly of

Nematoida (M. J. Telford, unpubl. obs.). SSU rDNA also

supports the link between kinorhynchs and priapulids (loriciferans

have not been sampled; e.g., Littlewood et al. 1998).

The grouping of kinorhynch, priapulid, and loriciferans has

been named Cephalorhyncha (or Scalidophora after the

scalids or spines around their introverts). Some form of introvert

is shared by Nematoida and may be homologous with

the mouth cone of the tardigrades, which are likely basal

arthropods. Members of Cephalorhyncha share chitinous

cuticle, rings of scalids on their introvert, flosculi (sensory

pits of unique morphology), and characteristic musculature

for retracting the introvert (Nielsen 2001). The relationships

of all of these groups to the arthropods are unclear.

Nematoda: The Roundworms

and Thread Worms

Treated only very briefly here, roundworms are both ubiquitous

and numerous. Whether free-living or parasitic, they

have been found in almost every environment, and they range

in size from the microscopic (100 mm) to the enormous (~9

m, parasite of a sperm whale); estimated numbers of species

range from 40,000 to 10 million. With thin tapering, unsegmented,

cylindrical bodies and a muscular suctorial pharynx/

esophagus, it is perhaps their cuticle and cuticular

structures that have afforded them such success in so many

habitats (see chart in figure 14.19). Possession of a cuticle

places them in the molting clade Ecdysozoa, although this

placement was first recognized on the basis of SSU rDNA

Figure 14.18. Interrelationships of Chaetognatha.

Monophragmomorpha

Eukrohniidae

Spadellidae

Bathybelidae

Sagittidae

Krohnittidae

Krohnittelidae

Bathyspadellidae

Pterokrohniidae

Pterosagittidae

Heterokrohniidae

Biphragmomorpha

Aphragmomorpha

Spadella cephaloptera

Spadellidae

Protostomes and Platyhelminthes 227

(Aguinaldo et al. 1997). There seems little doubt that Nematoda

are a monophyletic phylum. According to SSU rDNA,

Nematoda do not separate into sister taxa Adenophorea and

Secernentea, a long-established split based principally on

trophic ecology and habitat, but instead five major clades are

identified, with Chromadorida paraphyletic (Blaxter et al.

1998, Dorris et al. 1999; fig. 14.19). The latest phylogenetic

estimates, based on SSU rDNA, support a monophyletic

Secernentea and resolve a paraphyletic Adenophorea but

have yet to be supported by additional gene sequencing (see

also Kampfer et al. 1998). Nevertheless, the solution has

prompted many reevaluations of morphology and biology

(Schierenberg 2000), which appear to lend support to the

new scheme. Parasitism evolved several times in the group

(Blaxter 2001, Schierenberg 2000), with many of the major

clades including novel associations of animal-parasitic, plantand

fungus-parasitic, and free-living groups. A number of

molecular studies, using LSU rDNA and mitochondrial gene

fragments, have been undertaken to elucidate further the

interrelationships of nematode groups, but there are no data

sets rivaling the SSU rDNA to estimate overall nematode

phylogeny.

Apomorphies of Nematoda

6 + 6 + 4 cephalic sensillae and amphids

Lateral epidermal cords with the perikarya

Nematomorpha: Horsehair Worms

The nematomorphs or horsehair worms are a phylum of

nematodelike worms all of which parasitize arthropods. Their

body is an extremely long and slender cylinder, in some species

more than 1 m long yet only 1 mm in diameter (Bresciani

1991, Nielsen 2001). Their similarities to other ecdysozoan

worms (especially nematodes) are perhaps seen most clearly

in their larvae, which have a retractable (although not invertible)

proboscis on an anterior introvert, which has backwardpointing

cuticular spines. Roughly 325 extant species have

been described in two orders. The marine order Nectonematoidea

has a single genus, Nectonema, with just four species.

Nectonema larvae parasitize marine decapods, and the

adults have bristles on the body that enable them to swim; they

have dorsal and ventral nerve cords and an unpaired gonad.

Species in the order Gordioidea are terrestrial, and their larval

stages parasitize insects; they have only a ventral nerve cord

and paired gonads (Schmidt-Rhaesa 1998).

Apomorphies of Nematomorpha

Parasites of arthropods during larval stage

Extremely long and thin

Periodic molting of collagenous cuticle

Reduced or no mouth; nutrient absorption via cuticle

Nonfeeding adults; adults without guts

Figure 14.19. Interrelationships of the wormlike ecdysozoan groups, with a phylogeny of

Nematoda, taken from Blaxter et al. (1998), indicating multiple origins of parasitism and feeding

habits.

Strongylida

Rhabditina

Diplogasterida

Strongyloididae

Steinernematidae

Panagrolaimidae

Aphelenchida

Tylenchida

Cephalobidae

Oxyurida

Spirurida

Ascaridida

Rhigonematida

'Chromadorida'

'Chromadorida'

'Chromadorida'

Enoplida

Triplonchida

Dorylaimida

Mermithida

Trichocephalida

Mononchida

Vertebrate parasite

Invertebrate parasite

Phytoparasite

Entomopathogen

Fungivore

Algivore-omnivore-predator

Bacterivore

Trophic ecology

III

IVb

IVa

V

I

II

Nematoda

Priapulus caudatus

PRIAPULIDA

Priapulida

Kinorhyncha

Loricifera

Cephalorhyncha

Nematomorpha

Nematoda

Nematoida

Arthropoda

Onychophora

Tardigrada

Allantonema mirabile

NEMATODA

Gordius sp.

NEMATOMORPHA

Echinoderes sp.

KINORHYNCHA

male

female

228 The Relationships of Animals: Overview

Apomorphies of Nematoida (Nematoda and Nematomorpha;

Nielsen 2001, Schmidt-Rhaesa 1998)

Cuticle with layers of crossing collagenous (not

chitinous) fibrils

Reduction of circular body muscles

Epidermal longitudinal nerve cords

Cloaca in both sexes

Spermatozoa without a flagellum

Priapulida

The priapulids are bottom-living marine worms ranging from

0.5 mm to >20 cm in length (Storch 1991). There are fewer

than 20 species currently recognized, but their characteristic

body plan can be recognized in numerous fossils from the

Cambrian onward. They have a cylindrical body with a significant

anterior introvert. The introvert can be everted by

contraction of the trunk muscles, with the fluid-filled body

cavity acting as a hydroskeleton and inverted through contraction

of two rings of retractor muscles (Nielsen 2001).

Eversion and inversion allow the animals to burrow through

the sands and muds where they live and are also used for

feeding. The posterior end has one or two caudal appendages

that are most probably for gas exchange. The body is

covered in a cuticle that contains chitin and is periodically

molted during growth. The embryology is poorly known, but

radial cleavage has been seen in Priapulus and Halicryptus.

Recent morphology-based phylogenies (Wills 1998) support

classification of the extant genera in three families. The

most speciose, Priapulidae, contains four living genera—

Acanthopriapulus, Priapulus, Priapulopsis, and Halicryptus—and

the Carboniferous fossil Priapulites. Maccabeidae have just one

genus, Maccabeus. Tubiluchidae have two genera, Tubiluchus

and Meiopriapulus. There are five fossil families: Ottoidae,

Selkirkiidae, Miskoiidae, Ancalagonidae, and Fieldidae. Morphological

cladistic analyses of the relationships between

these families group Priapulidae and Maccabeidae and furthermore

suggest that all families still extant are monophyletic

with respect to the Cambrian fossils (Wills 1998). We

are not aware of any molecular analyses of priapulid intraphyletic

relationships.

Apomorphies of Priapulida

Large, spiny, retractable presoma (introvert)

Terminal caudal appendage in most species

Large body cavity with amoebocytes and erythrocytes

Loricifera

Loricifera are a recently discovered (1983) phylum of microscopic

interstitial or infaunal marine animals. Very little

has been published on this phylum, and few members have

been thoroughly described, although more than 100 species

have been found (Nielsen 2001). Kristensen has placed

the described species in a single order, Nanaloricida, with

two families at present, Nanaloricidae and Pliciloricidae

(Kristensen 1991). Their body consists of a trunk covered

with a chitinous exoskeleton called a lorica (girdle) consisting

of 6–30 longitudinal cuticular plates and an anterior introvert

surrounded by several hundred complex cuticular

appendages or scalids in two to seven rows. These scalids

are of differing morphology and presumably function (sensory,

locomotory). The cuticle is molted repeatedly during

growth of the larva (known as a Higgins larva), which is

similar in morphology to the adult but has toes that serve

to propel it in Nanaloricidae and to act as adhesive pads in

Pliciloricidae.

Apomorphies of Loricifera (Kristensen 1991)

Higgins larva

Chitinous lorica on trunk

Scalids with muscles

Kinorhyncha

The kinorhynchs are a very uniform phylum of approximately

150 species. All are small (<1 mm long), marine, and

benthic, living in coastal bottom mud (Nielsen 2001). All

have a body consisting of 13 segments (with segmentation

of muscles and nervous system as well as external cuticle),

the anteriormost of which is an introvert with up to seven

rings of spines or scalids (sensory and locomotory), followed

by a neck and 11 trunk segments (Kristensen and Higgins

1991). The newly hatched larvae have just 11 segments (nine

in the trunk), with the two additional adult segments added

after periodic molts of the chitinous cuticle. Despite the homogeneity

of their morphology, they are classified in two

orders: Cyclorhagida (which contain four families and seven

genera) and Homalorhagida (two families and four genera;

Nielsen 2001). Members of Cyclorhagida (e.g., Pycnophyes)

have a circular pharynx and 14–16 cuticular plates (placids)

on their neck segment, and their body is round or oval in cross

section; members of Homalorhagida (e.g., Echinoderes) have a

triradiate pharynx and two to eight placids on their neck, and

their body is flattened ventrally and arched dorsally.

Apomorphies of Kinorhyncha (Kristensen 1991)

Truly segmented (including muscle, nervous system

and cuticle); 11 segments in larvae and 13 segments

in adults

Apomorphies of Cephalorhyncha/Scalidophora

(Kinorhyncha + Loricifera + Priapulida)

Neuropileous nerve ring in a terminal position

Introvert with scalids

Reversible foregut

Tanycytes (tonofibril-containing ectodermal cells in

brain; Nebelsick 1993)

Protostomes and Platyhelminthes 229

Summary

Although we cover metazoan taxa not mentioned elsewhere

in this volume, there are few features that unite them. Indeed,

it is this very problem that has prevented a phylogenetic resolution

for the protostome phyla based on morphology alone.

Of course, many phyla do share common features, and matrices

have been constructed in order to best estimate relationships.

However, molecular data have played a significant

role in generating independent estimates or as supplements

to morphology. The call for more genes and additional molecular

markers is as loud as ever. The so-called lesser phyla,

which are often poorly studied because they are few in number,

microscopic, cryptic, or mistakenly appear “simple,” are

in fact critical if we are to understand the interrelationships

of the Metazoa and their radiation. Simple does not necessarily

equate with primitive, and a common lack of characters

has suggested affiliation where little or none exists. As a

result, morphological matrices are arguably best used currently

as a source of mappable characters in order to establish

or confirm homology a posteriori. The distribution of

phyla on the tree enables the mapping of unique and shared

characters alike. Although a total evidence approach may be

possible or even preferred by some, reciprocal illumination

between independent data sets enlightens our understanding

of both morphological and molecular characters as we

learn how each has evolved. Acoelomorph flatworms appear

to be basal members of Bilateria, with some other taxa still

vying for the position and worthy of closer attention. True

flatworms (Platyhelminthes, composed of Catenulida and

Rhabditophora) appear to be derived bilaterians occupying

a position within Lophotrochozoa. The split in Protostomia

between Lophotrochozoa and Ecdysozoa is still not as simple

as rDNA would have us believe. Taxa such as Acoelomorpha,

Chaetognatha, Gastrotricha, and Xenoturbellida suggest the

need for other branches and fewer polytomies. Far greater

attention is required among the commercially and medically

unimportant, yet richly diverse and ecologically important

groups that comprise the lophotrochozoans. Meanwhile,

some stability is appearing among the major ecdysozoan

groups, helped by a healthy interaction between morphologists,

molecular systematists, and evolutionary developmental

geneticists. As molecular trees promote the reevaluation

of morphological characters and highly unexpected topologies

sometimes question the utility of types of molecular data,

affiliations throughout the protostomes at all taxonomic levels

within the tree will evolve by consensus and be resolved

only by a sustained effort with all taxa included neither prejudged

as lesser nor minor.

Acknowledgments

We are grateful to the following for permission to reproduce

figures: Lester Cannon and the Queensland Museum, Igor

Eeckhaut, Vaughan Southgate, Willi Xylander, and the following

publishers: Gustav Fischer Verlag, Kluwer Academic, Taylor

and Francis, and John Wiley and Sons. D.T.J.L. and M.J.T. are

funded individually through Wellcome Trust fellowships, for

which we are most grateful (D.T.J.L., 043965; M.J.T., 060503).

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VI

The Relationships of Animals: Lophotrochozoans

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