The origin of annelids

Annelids are a phylum of segmented bilaterian animals that have become important components of ecosystems spanning terrestrial realms to the deep sea. Annelids are remarkably diverse, possessing high taxonomic diversity and exceptional morphological disparity, and have evolved numerous feeding strategies and ecologies. Their interrelationships and evolution have been the source of much controversy over the past century with the composition of the annelid crown group, the relationship of major groups and the body plan of the ancestral annelid having undergone major recent revisions. There is a convincing body of molecular evidence that polychaetes form a paraphyletic grade and that clitellates are derived polychaetes. The earliest stem group annelids from Cambrian Lagerstätten are errant, epibenthic polychaetes, confirming that biramous parapodia, head appendages and diverse, simple chaetae are primitive for annelids. Current evidence from molecular clocks and the fossil record suggest that crown group annelids are a Late Cambrian – Ordovician radiation, with clitellates radiating in the Late Palaeozoic. Their body fossil record is largely confined to deposits showing exceptional preservation and is punctuated by the acquisition of hard parts in major groups. The discovery of an Ordovician fossil with soft tissues has shown that machaeridians are in fact a clade of crown polychaetes. They were in existence for more than 200 million years and possess unique calcitic dorsal armour, allowing their mode of life and phylogeny to be interpreted in the context of the annelid body plan. We identify a novel clade of machaeridians, the Cuniculepadida, which exhibit a series of adaptations for burrowing.     

Convergent evolution of the ladder-like ventral nerve cord in Annelida

Background

A median, segmented, annelid nerve cord has repeatedly been compared to the arthropod and vertebrate nerve cords and became the most used textbook representation of the annelid nervous system. Recent phylogenomic analyses, however, challenge the hypothesis that a subepidermal rope-ladder-like ventral nerve cord (VNC) composed of a paired serial chain of ganglia and somata-free connectives represents either a plesiomorphic or a typical condition in annelids.

Results

Using a comparative approach by combining phylogenomic analyses with morphological methods (immunohistochemistry and CLSM, histology and TEM), we compiled a comprehensive dataset to reconstruct the evolution of the annelid VNC. Our phylogenomic analyses generally support previous topologies. However, the so far hard-to-place Apistobranchidae and Psammodrilidae are now incorporated among the basally branching annelids with high support. Based on this topology we reconstruct an intraepidermal VNC as the ancestral state in Annelida. Thus, a subepidermal ladder-like nerve cord clearly represents a derived condition.

Conclusions

Based on the presented data, a ladder-like appearance of the ventral nerve cord evolved repeatedly, and independently of the transition from an intraepidermal to a subepidermal cord during annelid evolution. Our investigations thereby propose an alternative set of neuroanatomical characteristics for the last common ancestor of Annelida or perhaps even Spiralia.

     

Phylogenetic position of Sipuncula derived from multi‐gene and phylogenomic data and its implication for the evolution of segmentation

The phylogenetic position of Sipuncula, a group of unsegmented marine worms, has been controversial for several decades: Especially based on morphological data, closer relationships to Mollusca or Annelida were among the most favoured hypotheses. Increasing amounts of molecular data in recent years have consistently placed Sipuncula either in close affinity to or even within Annelida, the segmented worms, and rejected a close relationship to Mollusca. Yet, it remained uncertain whether Sipuncula is the sister group of Annelida or an annelid subtaxon. Therefore, herein we gathered data for five nuclear genes, which have been rarely used regarding Annelida and Sipuncula, and combined these with data for six previously used genes to further elucidate the phylogenetic position of Sipuncula. We also compiled a data set for 78 ribosomal proteins from publicly available genomic data sets. These are the two largest data sets for annelids with more than 10 taxa to date. All analyses placed Sipuncula within Annelida. For the first time, topology tests significantly rejected the possibility that Sipuncula is sister to Annelida. Thus, our analyses revealed that Sipuncula had secondarily lost segmentation. Given that unsegmented Echiura is also an annelid subtaxon, segmentation, a key character of Annelida, is much more variable than previously thought. Yet, this conclusion does not support the hypothesis that the last common ancestor of Annelida, Arthropoda and Chordata was segmented, assuming several losses along the branches leading to them. As yet no traces of segmentation could be shown in taxa exhibiting serially organized organ systems such as certain Mollusca, while in Sipuncula and Echiura such traces could be demonstrated. An independent origin of segmentation in Annelida, Arthropoda and Chordata thus appears to be more plausible and parsimonious.     

Hox gene duplication and deployment in the annelid leech Helobdella

SUMMARY The segmented leeches are members of the phylum Annelida within the Lophotrochozoa. Here, we describe the isolation of a new Hox gene, Lox18 , in the leech Helobdella triserialis. Phylogenetic analysis indicates that Lox18 is a Deformed ( Dfd   ) ortholog. H. triserialis has at least two Dfd orthologs, Lox18 and the previously described Lox6 ( Kourakis et al. 1997 ; Wong and Macagno 1998 ), indicating that these genes duplicated after the last common ancestor of annelids and arthropods. Although the temporal appearance of Lox18 message is similar to that of Lox6 , the spatial pattern is different. Lox18 does not have a sharply defined anterior border of expression in the second neuromere of the subesophageal ganglion of the central nervous system (CNS) as does Lox6 , but is expressed uniformly in a small subset of cells in the longitudinal connectives and lateral roots in every segment of the CNS along the entire anterior-posterior (AP) axis. Even though Lox18 shares greater sequence similarity within the homeodomain and flanking regions to Drosophila Dfd than to the previously isolated Lox6 , its expression pattern suggests that its function has diverged from the ancestral Hox function. Previous sampling has indicated that the last common ancestor of protostomes and deuterostomes had as many as 10 clustered Hox genes representing distinct paralogy groups ( Irvine et al. 1997 ; de Rosa et al. 1999 ); leech Hox genes may have undergone subsequent and independent cluster or genome-wide duplication. These results point to the need for total genome level understanding for key members of the Lophotrochozoa.     

Comparative neuroanatomy suggests repeated reduction of neuroarchitectural complexity in Annelida

Background

Paired mushroom bodies, an unpaired central complex, and bilaterally arranged clusters of olfactory glomeruli are among the most distinctive components of arthropod neuroarchitecture. Mushroom body neuropils, unpaired midline neuropils, and olfactory glomeruli also occur in the brains of some polychaete annelids, showing varying degrees of morphological similarity to their arthropod counterparts. Attempts to elucidate the evolutionary origin of these neuropils and to deduce an ancestral ground pattern of annelid cerebral complexity are impeded by the incomplete knowledge of annelid phylogeny and by a lack of comparative neuroanatomical data for this group. The present account aims to provide new morphological data for a broad range of annelid taxa in order to trace the occurrence and variability of higher brain centers in segmented worms.

Results

Immunohistochemically stained preparations provide comparative neuroanatomical data for representatives from 22 annelid species. The most prominent neuropil structures to be encountered in the annelid brain are the paired mushroom bodies that occur in a number of polychaete taxa. Mushroom bodies can in some cases be demonstrated to be closely associated with clusters of spheroid neuropils reminiscent of arthropod olfactory glomeruli. Less distinctive subcompartments of the annelid brain are unpaired midline neuropils that bear a remote resemblance to similar components in the arthropod brain. The occurrence of higher brain centers such as mushroom bodies, olfactory glomeruli, and unpaired midline neuropils seems to be restricted to errant polychaetes.

Conclusions

The implications of an assumed homology between annelid and arthropod mushroom bodies are discussed in light of the 'new animal phylogeny'. It is concluded that the apparent homology of mushroom bodies in distantly related groups has to be interpreted as a plesiomorphy, pointing towards a considerably complex neuroarchitecture inherited from the last common ancestor, Urbilateria. Within the annelid radiation, the lack of mushroom bodies in certain groups is explained by widespread secondary reductions owing to selective pressures unfavorable for the differentiation of elaborate brains. Evolutionary pathways of mushroom body neuropils in errant polychaetes remain enigmatic.     

Annelids in evolutionary developmental biology and comparative genomics

Annelids have had a long history in comparative embryology and morphology, which has helped to establish them in zoology textbooks as an ideal system to understand the evolution of the typical triploblastic, coelomate, protostome condition. In recent years there has been a relative upsurge in embryological data, particularly with regard to the expression and function of developmental control genes. Polychaetes, as well as other annelids such as the parasitic leech, are now also entering the age of comparative genomics. All of this comparative data has had an important impact on our views of the ancestral conditions at various levels of the animal phylogeny, including the bilaterian ancestor and the nature of the annelid ancestor. Here we review some of the recent advances made in annelid comparative development and genomics, revealing a hitherto unsuspected level of complexity in these ancestors. It is also apparent that the transition to a parasitic lifestyle leads to, or requires, extensive modifications and derivations at both the genomic and embryological levels.     

Current status of annelid phylogeny

Annelida is an ecologically and morphologically diverse phylum within the Lophotrochozoa whose members occupy a wide range of environments and show diverse life styles. The phylogeny of this group comprising more than 17,000 species remained controversial for a long time. By using next-generation sequencing and phylogenomic analyses of huge data matrices, it was finally possible to reach a well-supported and resolved annelid backbone tree. Most annelid diversity is comprised in two reciprocal monophyletic groups, Sedentaria and Errantia, which are named after the predominant life style of their members. Errantia include Aciculata (Phyllodocida?+?Eunicida) and Protodriliformia, which is a taxon of interstitial polychaetes. Sedentaria comprise most of the polychaete families formerly classified as Canalipalpata or Scolecida, as well as the Clitellata. Six taxa branch as a basal grade outside of this major radiation: Oweniidae, Magelonidae, Chaetopteridae, Sipuncula, Amphinomida, and Lobatocerebrum. Oweniidae and Magelonidae form a monophyletic group which we name Palaeoannelida, which constitutes the sister taxon of the remaining annelids. The early splits of annelid phylogeny date back to the Cambrian. The new annelid phylogeny highlights the variability and lability of annelid body plans, and many instances of simplifications of body plan as adaptations to new life styles can be found. Therefore, annelids will be an appropriate model to understand major transitions in the evolution of Bilateria in general. Evolutionary developmental studies are one way to investigate macroevolutionary transition in annelids. We briefly summarize the state of developmental model organisms in Annelida and also propose new candidates on the background of the phylogeny.     

Origins of holopelagic Typhloscolecidae and Lopadorhynchidae within Phyllodocidae (Phyllodocida,Annelida)

Struck, T. H. & Halanych, K. M. (2010). Origins of holopelagic Typhloscolecidae and Lopadorhynchidae within Phyllodocidae (Phyllodocida, Annelida).—Zoologica Scripta, 39, 269–275. Several distinct lineages of annelids have evolved holopelagic life styles. Unfortunately, our knowledge of the biology and evolution of most of these groups is limited. Typhloscolecidae and Lopadorhynchidae are two such examples of recognized families of holopelagic annelids about which little is known. Both groups have a limited number of known species (13 and 15, respectively) and are rarely discussed in the literature other than to note occurrence. Placing these groups in a phylogenetic context has been difficult due to their seemingly unique morphology, and, to the best of our knowledge, lack of molecular data. Nonetheless, previous authors have suspected that they are members of Phyllodocida and perhaps within Phyllodocidae. To test such hypotheses, we have employed nuclear 18S and 28S ribosomal data in both a Bayesian inference and a maximum‐likelihood framework. The resultant topology indicates that typhloscolecids and lopadorhynchs are sister taxa nested within Phyllodocidae near another holopelagic taxon, alciopids. Whereas posterior probabilities strongly support this placement, an AU hypothesis testing approach and bootstrap values are more equivocal but both still strongly suggest Phyllodocidae affiliations. Recognition of Typhloscolecidae and Lopadorhynchidae as annelid families is called into question.     

Evolution of habitat preference in Clitellata (Annelida)

Clitellata (earthworms, leeches, and allies) is a clade of segmented annelid worms that comprise more than 5000 species found worldwide in many aquatic and terrestrial habitats. According to current views, the first clitellates were either aquatic (marine or freshwater) or terrestrial. To address this question further, we assessed the phylogenetic relationships among clitellates using parsimony, maximum likelihood and Bayesian analyses of 175 annelid 18S ribosomal DNA sequences. We then defined two ecological characters (Habitat and Aquatic‐environment preferences) and mapped those characters on the trees from the three analyses, using parsimony character‐state reconstruction (i.e. Fitch optimization). We accommodated phylogenetic uncertainty in the character mapping by reconstructing character evolution on all the trees resulting from parsimony and maximum likelihood bootstrap analyses and, in the Bayesian inference, on the trees sampled using the Markov chain Monte Carlo algorithm. Our analyses revealed that an ‘aquatic’ ancestral state for clitellates is a robust result. By using alterations of coding characters and constrained analyses, we also demonstrated that the hypothesis for a terrestrial origin of clitellates is not supported. Our analyses also suggest that the most recent ancestor of clitellates originated from a freshwater environment. However, we stress the importance of adding sequences of some rare marine taxa to more rigorously assess the freshwater origin of Clitellata. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 447–464.     

Unsegmented annelids? Possible origins of four lophotrochozoan worm taxa

In traditional classification schemes, the Annelida consists of the Polychaeta and the Clitellata (the latter including the Oligochaeta and Hirudinida). However, recent analyses suggest that annelids are much more diverse than traditionally believed, and that polychaetes are paraphyletic. Specifically, some lesser-known taxa (previously regarded as separate phyla) appear to fall within the annelid radiation. Abundant molecular, developmental, and morphological data show that the Siboglinidae, which includes the formerly recognized Pogonophora and Vestimentifera, are derived annelids; recent data from the Elongation Factor-1α (EF-1α) gene also suggest that echiurids are of annelid ancestry. Further, the phylogenetic origins of two other lesser-known groups of marine worms, the Myzostomida and Sipuncula, have recently been called into question. Whereas some authors advocate annelid affinities, others argue that these taxa do not fall within the annelid radiation. With advances in our understanding of annelid phylogeny, our perceptions of body plan evolution within the Metazoa are changing. The evolution of segmentation probably is more plastic than traditionally believed. However, as our understanding of organismal evolution is being revised, we are also forced to reconsider the specific characters being examined. Should segmentation be considered a developmental process or an ontological endpoint?     

Phylogenetic relationships of annelids,molluscs, and arthropods evidenced from molecules and morphology

Annelids and arthropods have long been considered each other's closest relatives, as evidenced by similarities in their segmented body plans. An alternative view, more recently advocated by investigators who have examined partial 18S ribosomal RNA data, proposes that annelids, molluscs, and certain other minor phyla with trochophore larva stages share a more recent common ancestor with one another than any do with arthropods. The two hypotheses are mutually exclusive in explaining spiralian relationships. Cladistic analysis of morphological data does not reveal phylogentic relationships among major spiralian taxa but does suggest monophyly for both the annelids and molluscs. Distance and maximum-likelihood analyses of 18S rRNA gene sequences from major spiralian taxa suggest a sister relationship between annelids and molluscs and provide a clear resolution within the major groups of the spiralians. The parsimonious tree based on molecular data, however, indicates a sister relationship of the Annelida and Bivalvia, and an earlier divergence of the Gastropoda than the Annelida–Bivalvia clade. To test further hypotheses on the phylogenetic relationships among annelids, molluscs, and arthropods, and the ingroup relationships within the major spiralian taxa, we combine the molecular and morphological data sets and subject the combined data matrix to parsimony analysis. The resulting tree suggests that the molluscs and annelids form a monophyletic lineage and unites the molluscan taxa to a monophyletic group. Therefore, the result supports the Eutrochozoa hypothesis and the monophyly of molluscs, and indicates early acquisition of segmented body plans in arthropods. Received: 25 September 1995 / Accepted: 15 March 1996     

Mitochondrial genomes of Clymenella torquata (Maldanidae) and Riftia pachyptila (Siboglinidae): evidence for conserved gene order in annelida

Mitochondrial genomes are useful tools for inferring evolutionary history. However, many taxa are poorly represented by available data. Thus, to further understand the phylogenetic potential of complete mitochondrial genome sequence data in Annelida (segmented worms), we examined the complete mitochondrial sequence for Clymenella torquata (Maldanidae) and an estimated 80% of the sequence of Riftia pachyptila (Siboglinidae). These genomes have remarkably similar gene orders to previously published annelid genomes, suggesting that gene order is conserved across annelids. This result is interesting, given the high variation seen in the closely related Mollusca and Brachiopoda. Phylogenetic analyses of DNA sequence, amino acid sequence, and gene order all support the recent hypothesis that Sipuncula and Annelida are closely related. Our findings suggest that gene order data is of limited utility in annelids but that sequence data holds promise. Additionally, these genomes show AT bias (approximately 66%) and codon usage biases but have a typical gene complement for bilaterian mitochondrial genomes.     

Developmental architecture of the nervous system in Themiste lageniformis (Sipuncula): New evidence from confocal laser scanning microscopy and gene expression

Sipuncula is a clade of unsegmented marine worms that are currently placed among the basal radiation of conspicuously segmented Annelida. Their new location provides a unique opportunity to reinvestigate the evolution and development of segmented body plans. Neural segmentation is clearly evident during ganglionic ventral nerve cord (VNC) formation across Sedentaria and Errantia, which includes the majority of annelids. However, recent studies show that some annelid taxa outside of Sedentaria and Errantia have a medullary cord, without ganglia, as adults. Importantly, neural development in these taxa is understudied and interpretation can vary widely. For example, reports in sipunculans range from no evidence of segmentation to vestigial segmentation as inferred from a few pairs of serially repeated neuronal cell bodies along the VNC. We investigated patterns of pan-neuronal, neuronal subtype, and axonal markers using immunohistochemistry and whole mount in situ hybridization (WMISH) during neural development in an indirect-developing sipunculan, Themiste lageniformis. Confocal imaging revealed two clusters of 5HT⁺ neurons, two pairs of FMRF⁺ neurons, and Tubulin⁺ peripheral neurites that appear to be serially positioned along the VNC, similar to other sipunculans, to other annelids, and to spiralian taxa outside of Annelida. WMISH of a synaptotagmin1 ortholog in T. lageniformis (Tl-syt1) showed expression throughout the centralized nervous system (CNS), including the VNC where it appears to correlate with mature 5HT⁺ and FMRF⁺ neurons. An ortholog of elav1 (Tl-elav1) showed expression in differentiated neurons of the CNS with continuous expression in the VNC, supporting evidence of a medullary cord, and refuting evidence of ontogenetic segmentation during formation of the nervous system. Thus, we conclude that sipunculans do not exhibit any signs of morphological segmentation during development.     

Annelid phylogeny and the status of Sipuncula and Echiura

Background  

Annelida comprises an ancient and ecologically important animal phylum with over 16,500 described species and members are the dominant macrofauna of the deep sea. Traditionally, two major groups are distinguished: Clitellata (including earthworms, leeches) and "Polychaeta" (mostly marine worms). Recent analyses of molecular data suggest that Annelida may include other taxa once considered separate phyla (i.e., Echiura, and Sipuncula) and that Clitellata are derived annelids, thus rendering "Polychaeta" paraphyletic; however, this contradicts classification schemes of annelids developed from recent analyses of morphological characters. Given that deep-level evolutionary relationships of Annelida are poorly understood, we have analyzed comprehensive datasets based on nuclear and mitochondrial genes, and have applied rigorous testing of alternative hypotheses so that we can move towards the robust reconstruction of annelid history needed to interpret animal body plan evolution.     

Myoanatomy of Myzostoma cirriferum (Annelida,Myzostomida): Implications for the evolution of the myzostomid body plan

Studies of rare genomic marker systems suggest that Myzostomida are a subgroup of Annelida and phylogenomic analyses indicate an early divergence of this taxon within annelids. However, adult myzostomids show a highly specialized body plan, which lacks typical annelid features, such as external body annulation, coelomic cavities with metanephridia, and segmental ganglia of the nervous system. The putative loss of these features might be due to the parasitic/symbiotic lifestyle of myzostomids associated with echinoderms. In contrast, the larval anatomy and adult locomotory system resemble those of annelids. To clarify whether the myoanatomy of myzostomids reflects their relationship to annelids, we analyzed the distribution of f‐actin, a common component of muscle fibers, in specimens of Myzostoma cirriferum using phalloidin‐rhodamine labeling in conjunction with confocal laser‐scanning microscopy. Our data reveal that the musculature of the myzostomid body comprises an outer circular layer, an inner longitudinal layer, numerous dorsoventral muscles, and prominent muscles of the parapodial complex. These features correspond well with the common organization of the muscular system in Annelida. In contrast to other annelids, however, several elements of the muscular system in M. cirriferum, including the musculature of the body wall, and the parapodial flexor muscles, exhibit radial symmetry overlaying a bilateral body plan. These findings are in line with the annelid affinity of myzostomids and suggest that the apparent partial radial symmetry of M. cirriferum arose secondarily in this species. Based on our data, we provide a scenario on the rearrangements of muscle fibers that might have taken place in the lineage leading to this species. J. Morphol., 2013. © 2012 Wiley Periodicals, Inc.     

The polychaete Platynereis dumerilii (Annelida): a laboratory animal with spiralian cleavage, lifelong segment proliferation and a mixed benthic/pelagic life cycle

Platynereis dumerilii, a marine polychaetous annelid with indirect development, can be continuously bred in the laboratory. Here, we describe its spectacular reproduction and development and address a number of open research problems. Oogenesis is easily studied because the oocytes grow while floating in the coelom. Unlike the embryos of other model spiralians, the Platynereis embryo is transparent giving insight into the dynamic structures and processes inside the cells that accompany the prevailing anisotropic cleavages. Functional studies on cell specification and differential gene expression in embryos, larvae, and later stages are underway. Lifelong proliferation of uniform trunk segments qualifies Platynereis as a model for the study of gene expression and of the functional circuitry of this process. Platynereis can also become a stepping stone in the comparison of segmentation between annelids and arthropods because it comes closer to the putative ancestral morphology and style of development than other model annelids.     

Arthropod-like expression patterns of engrailed and wingless in the annelid Platynereis dumerilii suggest a role in segment formation

The origin of animal segmentation, the periodic repetition of anatomical structures along the anteroposterior axis, is a long-standing issue that has been recently revived by comparative developmental genetics. In particular, a similar extensive morphological segmentation (or metamerism) is commonly recognized in annelids and arthropods. Mostly based on this supposedly homologous segmentation, these phyla have been united for a long time into the clade Articulata. However, recent phylogenetic analysis dismissed the Articulata and thus challenged the segmentation homology hypothesis. Here, we report the expression patterns of genes orthologous to the arthropod segmentation genes engrailed and wingless in the annelid Platynereis dumerilii. In Platynereis, engrailed and wingless are expressed in continuous ectodermal stripes on either side of the segmental boundary before, during, and after its formation; this expression pattern suggests that these genes are involved in segment formation. The striking similarities of engrailed and wingless expressions in Platynereis and arthropods may be due to evolutionary convergence or common heritage. In agreement with similarities in segment ontogeny and morphological organization in arthropods and annelids, we interpret our results as molecular evidence of a segmented ancestor of protostomes.     

The clade Ecdysozoa, perplexities and questions

A relatively new clade, the Ecdysozoa [Aguinaldo et al., 1997. Nature 387, 489-493] was raised based on the 18S ribosomal DNA sequences that indicate a close relationship between the moulting phyla (Arthropoda, Tardigrada, Onychophora, Nematoda, Nematomorpha, Kinorhyncha, Lorificera and Priapula), from which the Annelida, with other phyla, are excluded.However, the authors here expressed puzzlement about this conclusion. In particular they stressed that: (a) ecdysis might not be an autapomorphy for the Ecdysozoa; (b) some Ecdysozoa phyla are unrelated from one another with regard to morphology and embryogeny; (c) the annelids have a body architecture that is more similar to arthropods than some of the Ecdysozoa; (d) the annelids are moulting animals; (e) some phyla excluded from the new clade (e.g. the gastrotrichs), probably carry out a gradual ecdysis by flaking similar to that of the polychaetes.The authors concluded that the clade Ecdysozoa appears to be phylogenetically unconvincing.     

The coelom and the origin of the annelid body plan

The biphasic life cycle in annelids is characterized by two completely different types of organisation, i.e. the acoelomate/pseudocoelomate larva and the coelomate adult. Based on this observation the recent literature on the different assumptions on the organisation of the bilaterian stem species with special emphasis on the evolution of the annelid body plan is reviewed. The structure of the coelomic lining ranges between a simple myoepithelium composed of epithelio-muscle cells and a non-muscular peritoneum that covers the body wall muscles. The direction of the evolution of these linings is discussed with respect to coelomogenesis. As the coelom originates from mesodermal cell bands, different assumption on the acoelomate condition in Bilateria can be substantiated. The origin of segmentation in annelids is explained by current hypothesis. Although no final decision can be made concerning the origin of the annelid body plan and the organisation of the bilaterian stem species, this paper elaborates those questions that need to be resolved to unravel the relation between the different body plans.     

The articulation of annelids

The aim of this paper is to assess the monophyly of the Annelida. Also, recent cladistic analyses of metazoan taxa, using a variety of data, have shown incongruities with regards to annelids and associated taxa that should be resolved. The Platyhelminthes is selected as the taxon to root our minimal length trees and polarise our characters in a parsimony analysis; ingroup taxa being Mollusca, Nemertea, Sipuncula, Echiura, Pogonophora, Vestimentifera, Euarthropoda, Onycho-phora, and the groups most commonly regarded as true ‘annelids’, the Clitellata and Polychaeta. We use 13 characters and a total of 33 states. This results in 18 minimal length trees of 23 steps. The consensus tree has the topology (Platyhelminthes (Nemertea (Sipuncula Mollusca (Echiura (Polychaeta (Vestimcntifera Pogonophora) Clitellata (Euarthropoda Onychophora)))))). The name Articulata is applied to the Clitellata, Euarthropoda, Onychophora, Pogonophora, Polychaeta, and Vestimentifera. The Vestimentifera is the sister group to, or more likely a clade within, the frenulate pogonophores, and the name Pogonophora is retained for this group. In half of the 18 minimal length trees, the traditionally formulated Annelida, i.e. Polychaeta and Clitellata, is paraphyletic if the Pogonophora are excluded. In the remaining minimal length trees, a monophyletic Annelida cannot be formulated. The name Annelida should not be used unless relationships within the Articulata are resolved to show it is a monophyletic taxon. The taxon name Articulata, originally formulated to include the Annelida and Arthropoda by Cuvier, is defined as the clade stemming from the first ancestor to show repetition of homologous body structures derived by teloblastic growth with a pygidial growth zone (segmentation) and longitudinal muscles broken into bands. The Articulata is considered, on current evidence, to consist of four monophyletic groups; the Arthropoda, Clitellata, Polychaeta, and Pogonophora, though the latter group may be a clade of polychaetes. If this is shown, the Pogonophora should revert to the original family name Lamellisabellidae Uschakov, 1933. An indented classification reflective of the cladistic pattern is provided. Other recent hypotheses about metazoan systematics arc analysed.