Lophotrochozoa

The clade Lophotrochozoa (Figure 8) was originally proposed on the basis of SSU sequence data to designate the lophophorates (brachiopods, phoronids, and ectoprocts), annelids, and mollusks. Further investigations have increased lophotrochozoan membership also to include the echiurans, sipuncu-lans, entoprocts, platyhelminths, nemerteans, gnathostomulids, rotifers, acanthocephalans, cycliophorans, micrognathozoans, and possibly gas-trotrichs and chaetognaths. Lophotrochozoan monophyly is furthermore robustly supported by additional molecular evidence, including LSU data, Hox gene data, mitochondrial gene sequence and gene arrangement data, myosin heavy-chain type II data, intermediate filament data, and sodium-potassium ATPase a-subunit sequences.

The abundant molecular evidence for lophotro-chozoan monophyly stands in sharp contrast to the resolution of its internal phylogeny and the strength of its morphological support. Using SSU sequences, for example, the monophyly of even morphologically well-defined phyla, such as Mollusca, Ectoprocta, or Nemertea, may not be supported, and, with the exception of a few possible clades, relationships within the Lophotrochozoa remain largely unresolved with molecular evidence. As a consequence, resolution of lophotrochozoan phylo-geny is currently heavily dependent on morphological evidence analyzed either in isolation, or in combination with molecular sequence data.

1.02.3.5.1 Lophophorata: Phoronida, Brachiopoda, and Ectoprocta Adult phoronids are slender wormlike animals that live in secreted tubes, from which they protrude their ciliated feeding tentacles (lopho-phore) that surround the mouth. Like brachiopods and ectoprocts they possess a U-shaped gut, and some zoologists think that both ectoprocts and bra-chiopods have evolved from a phoronid-like ancestor. However, available phylogenetic evidence does not support this hypothesis.

Brachiopods, or lampshells, are sessile animals enclosed in a bivalved shell. However, their similarity to bivalves is only superficial since brachiopods are flattened dorsoventrally while bivalves are flattened laterally. Somewhat simplistically, architecturally brachiopods can be regarded as shelled phoronids. Similar to ectoprocts and phoronids, brachiopods possess a crown of ciliated feeding tentacles called a lophophore.

With the exception of two genera, one solitary and one nonsessile, ectoprocts are sessile colonial animals, with individuals (called zooids) that measure less than 0.5 mm in length, and that may be box-shaped, oval, or tubular. Ectoprocts superficially resemble entoprocts with their ciliated crown of tentacles commonly referred to as a lophophore (but see below), and the possession of a U-shaped gut. When the zooids in a colony extend their lophophores, the colony looks a little like a patch of moss, which has led to their general name moss animals.

As noted above, brachiopods, phoronids, and ectoprocts possess ciliated feeding tentacles traditionally referred to as a lophophore. However, the structural and functional uniqueness of the ecto-proct tentacles has served as the basis for denying their homology with those of the brachiopods and phoronids, lessening morphological support for Lophophorata. Indeed, available morphological and molecular evidence only supports a close relationship between brachiopods and phoronids (Figure 8), either as sister taxa or with phoronids derived from within brachiopods (Cohen and Weydmann, 2005). SSU sequences and Hox gene data suggest that ectoprocts are at least lophotro-chozoans, but of very uncertain phylogenetic position. So far, morphological evidence has not helped to pinpoint the phylogenetic position of the ectoprocts.

1.02.3.5.2 Eutrochozoa: Nemertea, Mollusca, Sipuncula, Annelida, Echiura, Siboglinidae, and Myzostomida Nemerteans, or ribbon or proboscis worms, are all (with the exception of one species) characterized by the possession of an eversible proboscis enclosed by a fluid-filled coelom, the rhynchocoel. The proboscis apparatus is used in prey capture, and the proboscis can be rapidly everted to coil around the prey. Secreted toxins will help subdue the prey that mainly consists of small crustaceans and annelids.

On the basis of molecular phylogenetic evidence alone it can be concluded that nemerteans are lophotrochozoans, but their precise position remains unclear. In contrast, most phylogenetic analyses based on morphology alone or in combination with molecular evidence place nemerteans together with the neotrochozoans: mollusks, sipunculids, echiurans, and annelids (plus groups derived from within the annelids) (Figure 8). This hypothesis is supported, among others, by the shared possession of mesodermal bandlets derived from a 4d cell, and the derivation of a schizocoelic coelom from these bandlets (Jenner, 2004b). Although nemerteans are generally thought to lack trochophore larvae, in contrast to the neotrochozoans, the recent discovery of a hidden trochophore larva in the life cycle of a basal nemertean (Maslakova et al., 2004) implies that the trochophore larva may be an additional synapomorphy of nemerteans and neotrochozoans.

Mollusca is a highly diverse but clearly defined group of animals. Familiar mollusks include snails, slugs, bivalves, chitons, and cephalopods. Molluscan synapomorphies include a coelomic pericardium, a mantle that secretes the shells, and a radula used in feeding. Mollusks have adapted to a wide range of marine, freshwater and terrestrial habitats, and can be considered one of the most successful groups of animals on earth.

The phylogenetic position of the mollusks remains unclear. On the basis of morphological evidence various sister groups have been suggested, including entoprocts, sipunculans, or a clade of varying membership, including neotrochozoans and panarthropods. Molecular evidence has so far not allowed the resolution of this problem, and broadly sampled rDNA sequences have frequently failed to support even a monophyletic Mollusca.

Sipunculans, or peanut or star worms, form a well-demarcated phylum. They are nonsegmented, coelomate worms that are denizens of marine benthic communities. Their bipartite body has a posterior widened trunk, an anterior slender part called the introvert, with a terminal ciliated tentacle crown that is arranged as a star around the mouth.

The precise phylogenetic position of sipunculans remains unclear. Morphology suggests an affinity to the mollusks, or to a clade of variable membership that includes various neotrochozoans and panar-thropods. Molecular evidence suggests sipunculans are closely related to annelids.

The annelids, or segmented worms, are among the most familiar invertebrates, and they principally comprise the polychaetes and the clitellates. The polychaetes encompass a great diversity of forms, and molecular phylogenetic evidence suggests that they probably also include the vestimentiferans and pogonophores (now united as Siboglinidae), and the echiurans. Clitellates include the oligochaetes, including earthworms, and the parasitic hirudi-neans, or leeches.

The phylogenetic position of annelids on the basis of morphology remains contentious, because of the difficulty of interpreting the characters related to segmentation in the annelids and the arthropods. Traditionally their shared segmentation has been interpreted to support a close relationship. In contrast, molecular evidence firmly places the annelids within the Lophotrochozoa and the arthropods in the Ecdysozoa, suggesting the possibility that their segmentation is not homologous. The sister group to the annelids remains unknown. However, molecular evidence has suggested a larger membership of the Annelida than was sometimes suspected on the basis of morphology alone. Molecular evidence now supports the inclusion of the echiurans, vestimenti-ferans, and pogonophores (together siboglinids) within the polychaete annelids as well.

Adult echiurans, or spoon worms, are unsegmen-ted, coelomate worms. They share the chaetae characteristic of annelids, and they possess a characteristic flat or grooved proboscis that can be stretched to extreme lengths in the search for food while the rest of the animal remains hidden in a protective burrow or rock crevice.

The lack of body segmentation has caused morphological phylogenetic analyses to place the echiurans outside the annelids, frequently as its sister group. In contrast, accumulating molecular evidence from various sources now support the inclusion of echiurans in the polychaete annelids. This implies that echiurans have secondarily lost such characters as parapodia and pronounced metamery of the body.

Pogonophores and vestimentiferans are now united on the basis of both molecular and morphological evidence as the family Siboglinidae that is placed within the polychaetes. They are long worms that live in secreted tubes. They have an occluded gut, and highly modified and reduced segmentation. Perhaps the most familiar examples are the large vestimentiferans (up to 1.5 m), which live associated with deep-sea hydrothermal vents. They harbor chemoautotrophic symbiotic bacteria from which they derive a significant amount of nourishment.

Myzostomids are peculiar worms that look like little pancakes with stubby legs with which they cling on to their echinoderm hosts on which they parasitize. They seem to lack a coelom, but they do exhibit signs of segmentation, and they possess several characters unique to polychaetes or subgroups of polychaetes, including parapodia adorned with modified chaetae reminiscent of annelid chaetae, internal chaetae (called aciculae and functioning as support rods inside the parapodia), a nectochaete larva, and nearly identical innervation patterns of the parapodia and cirri (marginal sensory organs) in polychaetes and myzostomids.

The phylogenetic position of the myzostomids remains contentious (Jenner, 2003), and affinities with polychaete annelids, platyhelminths, and cycliophorans have been suggested on the basis of morphological, molecular, or combined evidence. However, sampling of molecular sequences is sparse and should be extended.

1.02.3.5.3 Platyzoa: Platyhelminthes, Gnatho-stomulida, Rotifera, Acanthocephala, Entoprocta, Cycliophora, and Micrognathozoa Platyzoa is a clade recently proposed on the basis of molecular sequence data and some combined analyses of molecular and morphological evidence (Figure 8). Platyzoa encompasses noncoelomate lophotro-chozoans. Although minimally proposed to include platyhelminths, gnathostomulids, rotifers, and acanthocephalans, the broadest definition of this clade additionally includes entoprocts, cycliophor-ans, and micrognathozoans, and potentially gastrotrichs and myzostomids. However, phyloge-netic support for this clade is currently far from robust, and the exact membership and interrelationships of Platyzoa remain to be determined.

Platyhelminths, or flatworms, are typically dorso-ventrally flattened bilaterians that come in a diverse array of forms with an even more exuberant range of life cycles that may contain multiple hosts for parasitic species. About a quarter of described flat-worm species are grouped as Turbellaria, which forms a paraphyletic group of mainly free-living species from which the highly specialized parasitic groups such as cestodes and trematodes have been derived. Recent evidence suggests that the acoelo-morphs (acoels and nemertodermatids) are not platyhelminths, but basal crown group bilaterians. Instead Platyhelminthes now comprises Catenulida and Rhabditophora, the latter taxon containing the bulk of extant species, including all parasitic groups.

Gnathostomulids are minute noncoelomate worms that live in the interstitial spaces of marine sands (meiofauna). Their common name jaw worms refers to the set of complex cuticularized jaw elements that are found in all gnathostomulids. Gnathostomulids are invariably described as enigmatic in evolutionary studies.

Rotifers are small (most are not more than 1mm) and common animals in marine zooplankton, freshwater, and in association with terrestrial moss plants. Their common name, wheel animals, refers to the presence of a ring of cilia at the anterior end present in many species that is used for feeding and locomotion. When the cilia beat, the ciliated band superficially resembles a rotating wheel. Rotifers possess a cuticularized pharyngeal jaw apparatus

(trophi) that is very similar ultrastructurally to gnathostomulid jaw elements.

The acanthocephalans or spiny-headed worms are generally small endoparasites (not more than a few millimeters, although one species of up to 80 cm is known) that derive their name from the possession of a spiny proboscis with which they attach inside their host. All recent phylogenetic studies (based on both morphology and molecules) support a close relationship between the generally free-living rotifers and parasitic acanthocephalans, either as sister groups, or with acanthocephalans nested within a paraphyletic Rotifera. The key synapomor-phy is a syncytial epidermis with an intracellular skeletal layer, which unites these taxa as Syndermata. The possession of a syncytial epidermis may be an adaptation to living in osmotically challenging environments. Many rotifers live in freshwater and acanthocephalans live as parasites inside other animals. A syncytial skin would then provide an effective tight seal to prevent osmotic stress.

Entoprocta comprises a well-demarcated mono-phylum. Entoprocts are tiny animals, frequently not longer than 1 mm. Entoprocts are sessile, solitary, or colonial, and resemble little stalked cups with a crown of ciliated tentacles that protrude into the water column where they filter out small food particles. Entoprocts exhibit a superficial similarity to the ectoprocts, and together they have traditionally been grouped as Bryozoa.

Another phylum of very tiny animals (less than 1mm in length) is Cycliophora (described as a single species, Symbion pandora, but at least one other species awaits description). Symbion was described in 1995 from specimens attached to the mouthparts of the Norwegian lobster, Nephrops (Funch and Kristensen, 1995). One of their unique features is a very complex life cycle, with sessile and motile stages, feeding and nonfeeding stages, dwarf males and giant females, and enigmatic chordoid and Pandora larvae. The external shape of the sessile feeding stages hints at an entoproct affinity, being shaped like a minute urn attached to a stalk that ends in an adhesive disk. Ciliated tentacles, however, are lacking. Instead the animal has a bell-shaped buccal funnel with a mouth surrounded by cilia that produce a feeding current.

The first complete description of Micrognathozoa was published in October 2000, and is based on one species, Limnognathia maerski, which is one of the smallest metazoans ever described, measuring some 100-150 mm in length. Strikingly, its discoverers were the same zoologists who had first described Cycliophora 5 years previously (Kristensen and Funch, 2000). Its complex cuticularized jaw apparatus is very similar to both rotifer trophi and gnathostomulid jaws.

Although the precise relationships between the platyzoans remain uncertain at the moment, several tentative conclusions can be drawn (Halanych, 2004; Jenner, 2004b; Funch et al., 2005). Accumulating molecular evidence suggests that pla-tyhelminths (catenulids and rhabditophorans) are undeniably lophotrochozoans, but neither molecular nor morphological evidence, or a combination thereof, has reliably identified a sister group of the platyhelminths.

The striking similarities of the jaw elements in syndermates and gnathostomulids support a clade Gnathifera (Figure 8). Based on the possession of similar complex cuticularized jaws and shared ultrastructural similarities of the epidermis with the syndermates, Micrognathozoa may also be a member of Gnathifera. Available nuclear and mitochondrial sequence data paint a more ambiguous picture. They provide no unambiguous support for the monophyly of Gnathifera. Depending on data source and analysis parameters, the synder-mates are sometimes the sister group of Cycliophora, a clade of Cycliophora, Micrognathozoa, and Gnathostomulida, or a clade of gastrotrichs and platyhelminths. Placement of the other platyzoan taxa is equally sensitive to changes in data source and analysis parameters.

1.02.3.5.4 Gastrotricha and Chaetognatha

Gastrotrichs are microscopic, meiobenthic animals (generally < 1mm), including both freshwater and marine species. Their general biology and evolution remain poorly known. Gastrotrich monophyly is well supported, with one of the most conspicuous autapomorphies being an extracellular cuticle that covers the entire body surface, including the loco-motory and sensory cilia. Their name refers to the presence of a ventral creeping surface adorned with cilia.

The phylogenetic position of the gastrotrichs in the Metazoa remains highly contentious. Morphological evidence has been used to argue for a relationship with ecdysozoans, frequently as the sister group to the remaining ecdysozoans, or the scalidophorans and nematoidans if the Ecdysozoa was not supported as a clade. The use of molecular evidence, or a combination of morphology and molecules, has not greatly clarified their phyloge-netic position either, and they have been variously allied with platyhelminths, gnathostomulids, acanthocephalans, nematomorphs, or placed basal in the Bilateria. Clearly, significant research is required to resolve the phylogenetic affinities of these poorly understood creatures.

The unique morphology of chaetognaths makes it a well-demarcated group. Chaetognaths are slender marine predators between 2 and 120mm long, with fins lining their sides and tail. Their heads are equipped with a formidable array of grasping spines used in prey capture. This general morphology and their jerky or darting swimming behavior explain their common name of arrow worms.

The possession by chaetognaths of a mixture of characters traditionally conceived as broadly proto-stomian, such as the organization of the nervous system and the composition of the cuticle, and broadly deuterostomian, including radial cleavage and the mode of coelom development, have ensured enduring debate about their phylogenetic relationships. Recent morphological cladistic analyses have variously placed chaetognaths at the base of the Bilateria, Ecdysozoa, or Deuterostomia, while molecular (SSU, LSU, Hox genes, and mitochondrial genome) and combined morphological and molecular analyses have recently placed them among ecdysozoans, within Lophotrochozoa, as a sister group to onychophorans or nematodes, as a basal protostome, or a basal bilaterian. Thus the phyloge-netic position of the chaetognaths remains profoundly puzzling.

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