Annelids in Evolutionary Developmental Biology and Comparative Genomics Mcdougall C.*,**, Hui J.H.L.**, Monteiro A.**, Takahashi T.**,*** & Ferrier D.E.K.*,**
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Article available at http://www.parasite-journal.org or http://dx.doi.org/10.1051/parasite/2008153321 ANNELIDS IN EVOLUTIONARY DEVELOPMENTAL BIOLOGY AND COMPARATIVE GENOMICS MCDOUGALL C.*,**, HUI J.H.L.**, MONTEIRO A.**, TAKAHASHI T.**,*** & FERRIER D.E.K.*,** Summary: al., 1997; de Rosa et al., 1999). Although the precise Annelids have had a long history in comparative embryology and membership of each of these three super-clades is still morphology, which has helped to establish them in zoology being refined their existence seems well supported and textbooks as an ideal system to understand the evolution of the justifiable. The phylogeny within the Lophotrochozoa, typical triploblastic, coelomate, protostome condition. In recent years there has been a relative upsurge in embryological data, and the positions of the annelid groups within it is less particularly with regard to the expression and function of robustly resolved. However, a consensus that is rapidly developmental control genes. Polychaetes, as well as other gaining support is that the annelids now include the annelids such as the parasitic leech, are now also entering the polychaetes (bristle worms) and clitellates (the leeches age of comparative genomics. All of this comparative data has had an important impact on our views of the ancestral conditions and oligochaetes), along with other groups that have at various levels of the animal phylogeny, including the bilaterian had a rather nomadic phylogenetic history, including ancestor and the nature of the annelid ancestor. Here we review the Pogonophora/Siboglinidae (beard worms), the some of the recent advances made in annelid comparative Echiura (spoon worms), the Sipuncula (peanut worms) development and genomics, revealing a hitherto unsuspected level of complexity in these ancestors. It is also apparent that the and the Myzostomida (parasites and commensals of cri- transition to a parasitic lifestyle leads to, or requires, extensive noid feather stars). The emerging consensus from the modifications and derivations at both the genomic and molecular data is that the polychaetes are a paraphy- embryological levels. letic group with the Clitellata, Sipuncula, Echiura, Sibo- KEY WORDS : Polychaetes, clitellates, bilaterian, Hox, ParaHox. glinidae and Myzostomidae embedded within it (Blei- dorn et al., 2007; Struck et al., 2007). o understand the evolution of any taxon or cha- racter a phylogenetic framework is required to ANCESTRAL EMBRYOLOGY Tstructure any comparisons. Great strides have been AND DEVELOPMENT made in refining the phylogeny of the animals, and of the annelids, with the input of molecular data (reviewed in the accompanying paper of Bleidorn). In the context THE BILATERIAN ANCESTOR of the annelids (segmented worms) they are one of the he “new” phylogeny has led to the abandonment most prominent taxa within the Lophotrochozoa, one of the traditional prominence of the coelom as of the three great clades of the bilaterally symmetrical, a phylogenetically robust and informative cha- triploblastic animals (the Bilateria); the other two super- T racter, with the pseudocoelomate nematodes now clades being the Ecdysozoa (moulting animals inclu- being loosely related to the eucoelomate arthropods ding insects, crabs, nematodes/roundworms and pria- (in the Ecdysozoa) (Fig. 1). The well-established deve- pulids/penis worms) and the Deuterostomia (animals lopmental biology model system of the nematode Cae- whose mouth develops from a secondary opening norhabditis elegans can thus no longer be taken as an during embryogenesis, including sea urchins, acorn outgroup for comparison to the other traditional models worms, sea squirts and humans) (Fig. 1) (Aguinaldo et of fruit flies (Drosophila melanogaster) and vertebrates (such as the mouse, zebrafish, chick and frog). The * The Gatty Marine Laboratory, School of Biology, University of St importance of the development of model systems within Andrews, St Andrews, Fife, KY16 8LB, UK. ** Department of Zoology, University of Oxford, South Parks Road, the lophotrochozoans is now undeniable. Lophotro- Oxford, OX1 3PS, UK. chozoan models will help distinguish patterns of true *** Present address, Faculty of Life Sciences, Michael Smith Building, conservation between the ecdysozoans and deutero- University of Manchester, Oxford Road, Manchester, M13 9PT, UK. stomes from convergence, and reveal patterns of loss Correspondence: Ferrier D.E.K., The Gatty Marine Laboratory, School of Biology, University of St Andrews, St Andrews, Fife, KY16 8LB, UK. and derivation (Tessmar-Raible & Arendt, 2003; Weis- Tel.: +44 (0)1334 463480 – E-mail: [email protected] blat & Huang, 2001). Parasite, 2008, 15, 321-328 Xth EMOP, August 2008 321 MCDOUGALL C., HUI J. MONTEIRO A. ET AL. Kinorhyncha Priapula Ecdysozoa Nematomorpha Onychophora Nematoda Tardigrada Arthropoda Protostomia Mollusca Fig. 1. – Schematic of the animal phylo- Platyhelminthes geny, showing selected phyla and the loca- tion of the Annelida in the Lophotrochozoa group of protostomes. Brachiopoda Bilaterian Ancestor Lophotrochozoa Annelida (Polychaeta, Clitellata, Echiura, Siboglinidae, Myzostomida, Sipuncula) Ectoprocta Phoronida Nemertea Echinodermata Deuterostomia Chordata Inherent in this field of research are assessments of other lineages can confuse the picture. Such loss of whether similarities reflect convergence or conserva- characters is clearly a plausible and common pheno- tion. There are many pitfalls, but one guiding principle menon (e.g. Jenner 2004; Bleidorn 2007). At present is that if two characters resemble each other to a high we tend to then fall back on supposing that this rare degree of complexity (e.g. detailed gene expression retention of ancestral complexity can be revealed by and networks) then they are much more likely to the same complex genetic network being used in such reflect conservation from a common ancestor that also supposed non-derived lineages. The validity of this possessed the gene network(s), and possibly the mor- supposition will become clearer as more is revealed phological or developmental character specified by this about the developmental mechanisms and networks network. One proviso is that developmental gene net- operating in a greater diversity of taxa both across the works are often reused during development in non- animal kingdom and within phyla. homologous contexts (e.g. Lowe & Wray, 1997; Seaver A table of recent publications on annelid development et al., 2001 and references therein). Also retention of that impact on our understanding of the form of the an ancestral network and character in only a few ancestral bilaterian is given in Table I (see also Irvine lineages with repeated independent loss amongst many & Seaver, 2006). These deductions summarized in Table I Parasite, 2008, 15, 321-328 322 Xth EMOP, August 2008 ANNELID EVO-DEVO AND GENOMICS Ancestral bilaterian feature Reference Centralised nervous system Denes et al., 2007 Eyes – ciliary and rhabdomeric components Arendt et al., 2004 Sensory-Neurosecretory cells Tessmar-Raible et al., 2007 Beta-catenin in binary cell-fate decisions Schneider & Bowerman, 2007 Convergent extension of embryo Steinmetz et al., 2007 Germ cell specification by Vasa & Nanos Rebscher et al., 2007; Kang et al., 2002 Segmented? Yes – Prud’homme et al., 2003 No – Seaver et al., 2001 Mesoderm differentiation controlled by Twist and Snail Dill et al., 2007 Germ layer-specific differentiation by GATA genes Gillis et al., 2007 Posterior growth zone De Rosa et al., 2005; Seaver et al., 2005 Larval apical organ? Nielsen, 2005 Table I. – Some features of the ancestral bilaterian deduced with contributions of annelid molecular data. are based on the discovery of similar developmental 1999), a reproductive process has evolved which mechanisms between annelids and members of at involves the clitellum and the formation of a cocoon least one or other of the ecdysozoan or deuterostome in which the embryos are nourished on a supply of clades. Interestingly it is usually the deuterostomes, and yolk and have done away with the requirement for a even vertebrates, that show the greater degrees of simi- feeding trochophore larva. Further to this, development larity to annelids than the other traditional protostome (and specifically ecdysozoan) model systems of flies A C and nematodes. THE ANNELID ANCESTOR With these reconstructions of the bilaterian ancestor there are clearly implications for the nature and form B of the annelid ancestor. Undoubtedly the annelid ancestor was segmented, but there is still a debate as to whether the mechanism(s) producing this segmen- tation was(were) homologous to segmentation mecha- nisms operating elsewhere in the animal kingdom, in the arthropods or chordates. The annelid ancestor also had a centralized nervous system, built with deve- lopmental networks conserved with the vertebrates D E (Denes et al., 2007). Whether the annelid ancestor, or even the last common ancestor of the ecdysozoans and lophotrochozoans, underwent some degree of moul- ting is an intriguing possibility (Paxton, 2005). Fur- thermore the paraphyly of the polychaetes has impli- cations for the origin of the clitellates. Again segmentation is an issue, with different modes appa- rently operating in polychaetes versus clitellates (Shi- mizu & Nakamoto, 2001; Irvine & Seaver, 2006). Also Fig. 2. – Variety of form in the annelids. (A) Dorsal view of the scale the annelid ancestor clearly underwent indirect deve- worm, Lepidonotus (Polynoidae), bearing