Skip to main content

Annelida

  • Chapter

Abstract

Annelids are a taxon of protostomes comprising more than 17,000 worldwide-distributed species, which can be found in marine, limnic, and terrestrial habitats (Zhang 2011). Their phylogeny was under discussion for a long time, but recent phylogenomic analyses resulted in a solid backbone of this group (Struck et al. 2011; Weigert et al. 2014). According to these analyses, most of the annelid diversity is part of Errantia or Sedentaria, which both form reciprocally monophyletic sister groups (Fig. 9.1) and are now known as Pleistoannelida (Struck 2011). The Sedentaria also include the Clitellata, Echiura, and Pogonophora (Siboglinidae) as derived from the annelid taxa. Outside Sedentaria and Errantia, several groups can be found in the basal part of the annelid tree, namely, Sipuncula, Amphinomida, Chaetopteridae, Magelonidae, and Oweniidae. The latter two taxa together represent the sister taxon of all other annelids. Given this hypothesis, it has to be assumed that the early diversification of extant annelids took place at least in the Lower Cambrian (520 Ma ago) (Weigert et al. 2014). The phylogenetic position of Myzostomida, a group of commensals or parasites of echinoderms (and, rarely, cnidarians), remains still uncertain. Whereas there is strong support for an annelid ancestry, its exact position awaits to be determined (Bleidorn et al. 2014). Likewise, the phylogenetic position of several interstitial taxa is still under debate (Westheide 1987; Worsaae and Kristensen 2005; Worsaae et al. 2005; Struck 2006). A position of Diurodrilidae outside Annelida, as suggested by Worsaae and Rouse (2008), was rejected by molecular data (Golombek et al. 2013), and the position of the enigmatic Lobatocerebrum and Jennaria remains unresolved (Rieger 1980, 1991). Likewise, the position of Annelida within Protostomia is still uncertain. However, recent phylogenomic analyses recover a clade uniting annelids with Mollusca, Nemertea, Brachiopoda, and Phoronida, but without strong support for any sister group relationship (Edgecombe et al. 2011).

Chapter vignette artwork by Brigitte Baldrian.© Brigitte Baldrian and Andreas Wanninger.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   39.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   54.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Ackermann C, Dorresteijn A, Fischer A (2005) Clonal domains in postlarval Platynereis dumerilii (Annelida: Polychaeta). J Morphol 266:258–280

    PubMed  Google Scholar 

  • Aisemberg GO, Macagno ER (1994) Lox1, an Antennapedia-class homeobox gene, is expressed during leech gangliogenesis in both transient and stable central neurons. Dev Biol 161:455–465

    CAS  PubMed  Google Scholar 

  • Akam M (1998) Hox genes, homeosis and the evolution of segment identity: no need for hopeless monsters. Int J Dev Biol 42:445–451

    CAS  PubMed  Google Scholar 

  • Åkesson B (1967) The embryology of the polychaete Eunice kobiensis. Acta Zool 48:142–192

    Google Scholar 

  • Ambros V (2004) The functions of animal microRNAs. Nature 431:350–355

    CAS  PubMed  Google Scholar 

  • Amiel AR, Henry JQ, Seaver E (2013) An organizing activity is required for head patterning and cell fate specification in the polychaete annelid Capitella teleta: new insights into cell-cell signaling in Lophotrochozoa. Dev Biol 379:107–122

    CAS  PubMed  Google Scholar 

  • Anderson DT (1959) The embryology of the polychaete Scoloplos armiger. Q J Microsc Sci 100:89–166

    Google Scholar 

  • Anderson DT (1966) The comparative embryology of Polychaeta. Acta Zool 47:1–42

    Google Scholar 

  • Anderson DT (1973) Embryology and physiology in annelids and arthropods. Pergamon, Oxford

    Google Scholar 

  • Arai A, Nakamoto A, Shimizu T (2001) Specification of ectodermal teloblast lineages in embryos of the oligochaete annelid Tubifex: involvement of novel cell-cell interactions. Development 128:1211–1219

    CAS  PubMed  Google Scholar 

  • Arenas-Mena C (2007) Sinistral equal-size spiral cleavage of the indirectly developing polychaete Hydroides elegans. Dev Dyn 236:1611–1622

    PubMed  Google Scholar 

  • Arendt D, Nübler-Jung K (1997) Dorsal or ventral: similarities in fate maps and gastrulation patterns in annelids, arthropods and chordates. Mech Dev 61:7–21

    CAS  PubMed  Google Scholar 

  • Arendt D, Technau U, Wittbrodt J (2001) Evolution of the bilaterian larval foregut. Nature 409:81–85

    CAS  PubMed  Google Scholar 

  • Arendt D, Denes AS, Jékely G, Tessmar-Raible K (2008) The evolution of nervous system centralization. Philos Trans R Soc B Biol Sci 363:1523–1528

    Google Scholar 

  • Arendt D, Hausen H, Purschke G (2009) The ‘division of labour’ model of eye evolution. Philos Trans R Soc B Biol Sci 364:2809–2817

    Google Scholar 

  • Astrow SH, Holton B, Weisblat DA (1989) Teloplasm formation in a leech, Helobdella triserialis, is a microtubule-dependent process. Dev Biol 135:306–319

    CAS  PubMed  Google Scholar 

  • Bartolomaeus T (1998) Head kidneys in hatchlings of Scoloplos armiger (Annelida: Orbiniidae): implications for the occurrence of protonephridia in lecithotrophic larvae. J Mar Biol Assoc UK 78:183–192

    Google Scholar 

  • Bartolomaeus T (1999) Structure, function and development of segmental organs in Annelida. Hydrobiologia 402:21–37

    Google Scholar 

  • Bartolomaeus T, Quast B (2005) Structure and development of nephridia in Annelida and related taxa. In: Bartolomaeus T, Purschke G (eds) Morphology, molecules, evolution and phylogeny in polychaeta and related taxa, vol 179, Developments in Hydrobiology. Springer, Dordrecht, pp 139–165

    Google Scholar 

  • Bartolomaeus T, Purschke G, Hausen H (2005) Polychaete phylogeny based on morphological data—a comparison of current attempts. In: Bartolomaeus T, Purschke G (eds) Morphology, molecules, evolution and phylogeny in polychaeta and related taxa, vol 179, Developments in Hydrobiology. Springer, Dordrecht, pp 341–356

    Google Scholar 

  • Bely AE (2006) Distribution of segment regeneration ability in the Annelida. Integr Comp Biol 46:508–518

    PubMed  Google Scholar 

  • Bergter A, Paululat A (2007) Pattern of body-wall muscle differentiation during embryonic development of Enchytraeus coronatus (Annelida: Oligochaeta; Enchytraeidae). J Morphol 268:537–549

    PubMed  Google Scholar 

  • Bergter A, Hunnekuhl VS, Schniederjans M, Paululat A (2007) Evolutionary aspects of pattern formation during clitellate muscle development. Evol Dev 9:602–617

    PubMed  Google Scholar 

  • Bhaud M, Cazaux C (1982) Les larves de polychètes des côtes de France. Oceanis 8:57–160

    Google Scholar 

  • Bhaud M, Cazaux C (1987) Description and identification of polychaete larvae; their implications in current biological problems. Oceanis 13:596–753

    Google Scholar 

  • Bielen H, Houart C (2014) The Wnt cries many: wnt regulation of neurogenesis through tissue patterning, proliferation, and asymmetric cell division. Dev Neurobiol 74:772–780

    Google Scholar 

  • Blair SS (1982) Interactions between mesoderm and ectoderm in segment formation in the embryo of a glossiphoniid leech. Dev Biol 89:389–396

    CAS  PubMed  Google Scholar 

  • Blake JA, Kudenov JD (1981) Larval development, larval nutrition and growth for two Boccardia species (Polychaeta: Spionidae) from Victoria, Australia. Mar Ecol Prog Ser 6:175–282

    Google Scholar 

  • Bleidorn C (2007) The role of character loss in phylogenetic reconstruction as exemplified for the Annelida. J Zool Syst Evol Res 45:299–307

    Google Scholar 

  • Bleidorn C, Lanterbecq D, Eeckhaut I, Tiedemann R (2009) A PCR survey of Hox genes in the myzostomid Myzostoma cirriferum. Dev Genes Evol 219:211–216

    CAS  PubMed  Google Scholar 

  • Bleidorn C, Helm C, Weigert A, Eeckhaut I, Lanterbecq D, Struck T, Hartmann S, Tiedemann R (2014) From morphology to phylogenomics: placing the enigmatic Myzostomida in the tree of life. In: Wägele JW, Bartolomaeus T (eds) Deep metazoan phylogeny: the backbone of the tree of life. De Gruyter, Berlin, pp 161–172

    Google Scholar 

  • Boyle MJ, Seaver EC (2008) Developmental expression of foxA and gata genes during gut formation in the polychaete annelid, Capitella sp. I. Evol Dev 10:89–105

    CAS  PubMed  Google Scholar 

  • Boyle M, Seaver E (2010) Expression of FoxA and GATA transcription factors correlates with regionalized gut development in two lophotrochozoan marine worms: Chaetopterus (Annelida) and Themiste lageniformis (Sipuncula). EvoDevo 1:2

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bright M, Eichinger I, Salwini-Plawen LV (2013) The metatrochophore of a deep-sea hydrothermal vent vestimentiferan (Polychaeta: Siboglinidae). Org Divers Evol 13:163–188

    PubMed Central  PubMed  Google Scholar 

  • Brinkmann N, Wanninger A (2008) Larval neurogenesis in Sabellaria alveolata reveals plasticity in polychaete neural patterning. Evol Dev 10:606–618

    PubMed  Google Scholar 

  • Brinkmann N, Wanninger A (2009) Neurogenesis suggests independent evolution of opercula in serpulid polychaetes. BMC Evol Biol 9:270

    PubMed Central  PubMed  Google Scholar 

  • Brinkmann N, Wanninger A (2010a) Integrative analysis of polychaete ontogeny: cell proliferation patterns and myogenesis in trochphore larva of Sabellaria alveolata. Evol Dev 12:5–15

    PubMed  Google Scholar 

  • Brinkmann N, Wanninger A (2010b) Capitellid connections: contributions from neuromuscular development of the maldanid polychaete Axiothella rubrocincta (Annelida). BMC Evol Biol 10:168

    PubMed Central  PubMed  Google Scholar 

  • Brooke NM, Garcia-Fernandez J, Holland PWH (1998) The ParaHox gene cluster is an evolutionary sister of the Hox gene cluster. Nature 392:920–922

    CAS  PubMed  Google Scholar 

  • Bruce AEE, Shankland M (1998) Expression of the head gene Lox22-Otx in the leech Helobdella and the origin of the bilaterian body plan. Dev Biol 201:101–112

    CAS  PubMed  Google Scholar 

  • Bullock TH (1965) Annelida. In: Bullock TH, Horridgke GH (eds) Structure and function in the nervous system of invertebrates, vol 1. Freeman, San Francisco, pp 661–789

    Google Scholar 

  • Butts T, Holland PWH, Ferrier DEK (2008) The urbilaterian super-Hox cluster. Trends Genet 24:259–262

    CAS  PubMed  Google Scholar 

  • Cadigan KM, Nusse R (1997) Wnt signaling: a common theme in animal development. Genes Dev 11:3286–3305

    CAS  PubMed  Google Scholar 

  • Chia F, Gibson G, Qian P (1996) Poecilogony as a reproductive strategy of marine invertebrates. Oceanol Acta 19:203–208

    Google Scholar 

  • Child CM (1900) The early development of Arenicola and Sternaspis. Archiv für Entwicklungsmechanik der Organismen 9:587–723

    Google Scholar 

  • Chipman AD (2010) Parallel evolution of segmentation by co-option of ancestral gene regulatory networks. Bioessays 32:60–70

    CAS  PubMed  Google Scholar 

  • Cho S, Cho P, Lee M, Hur S, Lee J, Kim S, Koh K, Na Y, Choo J, Kim C-B, Park S (2003) Hox genes from the earthworm Perionyx excavatus. Dev Genes Evol 213:207–210

    CAS  PubMed  Google Scholar 

  • Cho S-J, Lee D-H, Kwon H-J, Park S, Shin K-S, Ahn C (2006) Hox genes in the echiuroid Urechis unicinctus. Dev Genes Evol 216:347–351

    CAS  PubMed  Google Scholar 

  • Cho S-J, Valles Y, Giani VC Jr, Seaver EC, Weisblat DA (2010) Evolutionary dynamics of the wnt gene family: a lophotrochozoan perspective. Mol Biol Evol 27:1645–1658

    CAS  PubMed Central  PubMed  Google Scholar 

  • Christodoulou F, Raible F, Tomer R, Simakov O, Trachana K, Klaus S, Snyman H, Hannon GJ, Bork P, Arendt D (2010) Ancient animal microRNAs and the evolution of tissue identity. Nature 463:1084–1088

    CAS  PubMed Central  PubMed  Google Scholar 

  • Conklin EG (1897) The embryology of Crepidula, a contribution to the cell lineage and early development of some marine gastropods. J Morphol 13:1–226

    Google Scholar 

  • Costello DP, Henley C (1976) Spiralian development: a perspective. Am Zool 16:277–291

    Google Scholar 

  • Couso JP (2009) Segmentation, metamerism and the Cambrian explosion. Int J Dev Biol 53:1305–1316

    PubMed  Google Scholar 

  • Damen WGM (2007) Evolutionary conservation and divergence of the segmentation process in arthropods. Dev Dyn 236:1379–1391

    CAS  PubMed  Google Scholar 

  • Damen P, Dictus WJAG (1994) Cell lineage of the prototroch of Patella vulgata (Gastropoda, Mollusca). Dev Biol 162:364–383

    CAS  PubMed  Google Scholar 

  • de Rosa R, Prud’homme B, Balavoine G (2005) Caudal and even-skipped in the annelid Platynereis dumerilii and the ancestry of posterior growth. Evol Dev 7:574–587

    PubMed  Google Scholar 

  • Demilly A, Steinmetz P, Gazave E, Marchand L, Vervoort M (2013) Involvement of the Wnt/β-catenin pathway in neurectoderm architecture in Platynereis dumerilii. Nat Commun 4:1915

    PubMed  Google Scholar 

  • Denes AS, Jékely G, Steinmetz PRH, Raible F, Snyman H, Prud’homme B, Ferrier DEK, Balavoine G, Arendt D (2007) Molecular architecture of annelid nerve cord supports common origin of nervous system centralization in Bilateria. Cell 129:277–288

    CAS  PubMed  Google Scholar 

  • Dick MH, Buss LW (1994) A PCR-based survey of homeobox genes in Ctenodrilus serratus (Annelida: Polychaeta). Mol Phylogenet Evol 3:146–158

    CAS  PubMed  Google Scholar 

  • Dohle W (1999) The ancestral cleavage pattern of the clitellates and its phylogenetic deviations. Hydrobiologia 402:267–283

    Google Scholar 

  • Dorresteijn AWC (1990) Quantitative analysis of cellular differentiation during early embryogenesis of Platynereis dumerilii. Roux Arch Dev Biol 199:14–30

    Google Scholar 

  • Dorresteijn A (2005) Cell lineage and gene expression in the development of polychaetes. Hydrobiologia 535–536:1–22

    Google Scholar 

  • Dray N, Tessmar-Raible K, Le Gouar M, Vibert L, Christodoulou F, Schipany K, Guillou A, Zantke J, Snyman H, Béhague J, Vervoort M, Arendt D, Balavoine G (2010) Hedgehog signaling regulates segment formation in the annelid Platynereis. Science 329:339–342

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dykes I, Macagno E (2006) Molecular characterization and embryonic expression of innexins in the leech Hirudo medicinalis. Dev Genes Evol 216:185–197

    CAS  PubMed  Google Scholar 

  • Eckberg WR (1981) An ultrastructural analysis of cytoplasmic localization in Chaetopterus pergamentaceus. Biol Bull 160:228–239

    Google Scholar 

  • Edgecombe G, Giribet G, Dunn C, Hejnol A, Kristensen R, Neves R, Rouse G, Worsaae K, Sørensen M (2011) Higher-level metazoan relationships: recent progress and remaining questions. Org Divers Evol 11:151–172

    Google Scholar 

  • Eeckhaut I, Jangoux M (1993) Life cycle and mode of infestation of Myzostoma cirriferum (Annelida), a symbiotic myzostomid of the comatulid crinoid Antedon bifida. Dis Aquat Org 15:207–217

    Google Scholar 

  • Eisig H (1898) Zur Entwicklungsgeschichte der Capitelliden. Mitt Zool Stn Neapel 13:1–292

    Google Scholar 

  • Fauchald K, Rouse G (1997) Polychaete systematics: past and present. Zool Scr 26:71–138

    Google Scholar 

  • Fernandez J, Olea N, Matte C (1987) Structure and development of the egg of the glossiphoniid leech Theromyzon rude: characterization of developmental stages and structure of the early uncleaved egg. Development 100:211–225

    Google Scholar 

  • Ferrier DEK (2012) Evolutionary crossroads in developmental biology: annelids. Development 139:2643–2653

    CAS  PubMed  Google Scholar 

  • Ferrier DEK, Holland PWH (2001) Sipunculan ParaHox genes. Evol Dev 3:263–270

    CAS  PubMed  Google Scholar 

  • Ferrier DEK, Minguillon C (2003) Evolution of the Hox/ParaHox gene clusters. Int J Dev Biol 47:605–611

    CAS  PubMed  Google Scholar 

  • Fischer AHL, Arendt D (2013) Mesoteloblast-like mesodermal stem cells in the polychaete annelid Platynereis dumerilii (Nereididae). J Exp Zool B Mol Dev Evol 320:94–104

    PubMed  Google Scholar 

  • Fischer A, Dorresteijn A (2004) The polychaete Platynereis dumerilii (Annelida): a laboratory animal with spiralian cleavage, lifelong segment proliferation and a mixed benthic/pelagic life cycle. Bioessays 26:314–325

    PubMed  Google Scholar 

  • Fischer AHL, Henrich T, Arendt D (2010) The normal development of Platynereis dumerilii (Nereididae, Annelida). Front Zool 7:31

    PubMed Central  PubMed  Google Scholar 

  • Franke H-D (1999) Reproduction of the Syllidae (Annelida: Polychaeta). Hydrobiologia 402:39–55

    Google Scholar 

  • Freeman G, Lundelius JW (1992) Evolutionary implications of the mode of D quadrant specification in coelomates with spiral cleavage. J Evol Biol 5:205–247

    Google Scholar 

  • Fröbius AC, Seaver EC (2006) ParaHox gene expression in the polychaete annelid Capitella sp. I. Dev Genes Evol 216:81–88

    PubMed  Google Scholar 

  • Fröbius AC, Matus DQ, Seaver EC (2008) Genomic organization and expression demonstrate spatial and temporal Hox gene collinearity in the lophotrochozoan Capitella sp. I. PloS ONE 3:e4004

    PubMed Central  PubMed  Google Scholar 

  • Gan W-B, Wong VY, Phillips A, Ma C, Gershon TR, Macagno ER (1999) Cellular expression of a leech netrin suggests roles in the formation of longitudinal nerve tracts and in regional innervation of peripheral targets. J Neurobiol 40:103–115

    CAS  PubMed  Google Scholar 

  • Garcia-Fernandez J (2004) Hox, ParaHox, ProtoHox: facts and guesses. Heredity 94:145–152

    Google Scholar 

  • Gazave E, Behague J, Laplane L, Guillou A, Preau L, Demilly A, Balavoine G, Vervoort M (2013) Posterior elongation in the annelid Platynereis dumerilii involves stem cells molecularly related to primordial germ cells. Dev Biol 382:246–267

    CAS  PubMed  Google Scholar 

  • Gazave E, Guillou A, Balavoine G (2014) History of a prolific family; the Hes/Hey-related genes of the annelid Platynereis. Evodevo 5:29

    PubMed Central  PubMed  Google Scholar 

  • Gellon G, McGinnis W (1998) Shaping animal body plans in development and evolution by modulation of Hox expression patterns. Bioessays 20:116–125

    CAS  PubMed  Google Scholar 

  • Gharbaran R, Aisemberg GO (2013) Identification of leech embryonic neurons that express a Hox gene required for the differentiation of a paired, segment-specific motor neuron. Int J Dev Neurosci 31:105–115

    CAS  PubMed  Google Scholar 

  • Gibson G, Carver D (2013) Effects of extra-embryonic provisioning on larval morphology and histogenesis in Boccardia proboscidea (Annelida, Spionidae). J Morphol 274:11–23

    PubMed  Google Scholar 

  • Gline SE, Nakamoto A, Cho S-J, Chi C, Weisblat DA (2011) Lineage analysis of micromere 4d, a super-phylotypic cell for Lophotrochozoa, in the leech Helobdella and the sludgeworm Tubifex. Dev Biol 353:120–133

    CAS  PubMed Central  PubMed  Google Scholar 

  • Golombek A, Tobergte S, Nesnidal MP, Purschke G, Struck TH (2013) Mitochondrial genomes to the rescue – Diurodrilidae in the myzostomid trap. Mol Phylogenet Evol 68:312–326

    CAS  PubMed  Google Scholar 

  • Goto A, Kitamura K, Arai A, Shimizu T (1999) Cell fate analysis of teloblasts in the Tubifex embryo by intracellular injection of HRP. Develop Growth Differ 41:703–713

    CAS  Google Scholar 

  • Häcker V (1896) Pelagische Polychäten-Larven. Zur Kenntnis des Neapler Frühjahr-Auftriebs. Z Wiss Zool 62:74–168

    Google Scholar 

  • Hartman O, Boss KJ (1965) Antonbruunia viridis, a new inquiline annelid with dwarf males, inhabiting a new species of pelecypod, Lucina fosteri, in the Mozambique channel. Ann Mag Nat Hist 8:177–186

    Google Scholar 

  • Haszprunar G, Salvini-Plawen LV, Rieger RM (1995) Larval planktotrophy – a primitive trait in the Bilateria? Acta Zool 76:141–154

    Google Scholar 

  • Hatschek B (1886) Zur Entwicklung des Kopfes von Polygordius. Arb. aus dem Zool. Inst. Univ. Wien 6: 236–277

    Google Scholar 

  • Hay-Schmidt A (1995) The larval nervous system of Polygordius lacteus Scheinder, 1868 (Polygordiidae, Polychaeta): immunocytochemical data. Acta Zool 76:121–140

    Google Scholar 

  • Hay-Schmidt A (2000) The evolution of the serotonergic nervous system. Proc. R. Soc. Lond. B 267:1071–1079

    Google Scholar 

  • Heimler W (1988) Larvae. In: Westheide W, Hermans CO (eds) The ultrastructure of Polychaeta. Gustav Fischer Verlag, Stuttgart, pp 352–371

    Google Scholar 

  • Hejnol A, Martindale MQ (2008) Acoel development indicates the independent evolution of the bilaterian mouth and anus. Nature 456:382–386

    CAS  PubMed  Google Scholar 

  • Hejnol A, Martindale MQ (2009) The mouth, the anus and the blastopore – open questions about questionable openings. In: Telford MJ, Littlewood DTJ (eds) Animal evolution: genes, genomes, fossils and trees. Oxford University Press, Oxford, pp 33–40

    Google Scholar 

  • Helm C, Schemel S, Bleidorn C (2013) Temporal plasticity in annelid development – ontogeny of Phyllodoce groenlandica (Phyllodocidae, Annelida) reveals heterochronous patterns. J Exp Zool B Mol Dev Evol 320B:166–178

    Google Scholar 

  • Helm C, Stevenson PA, Rouse GW, Bleidorn C (2014) Immunohistochemical investigations of Myzostoma cirriferum and Mesomyzostoma cf. katoi (Myzostomida, Annelida) with implications for the evolution of the myzostomid body plan. Zoomorphology 133:257–271

    Google Scholar 

  • Helm C, Adamo H, Hourdez S, Bleidorn C (2014) An immunocytochemical window into the developement of Platynereis massiliensis (Annelida, Nereididae). Int J Dev Biol 58:613–622

    Google Scholar 

  • Henry JJ (1986) The role of unequal cleavage and the polar lobe in the segregation of developmental potential during first cleavage in the embryo of Chaetopterus variopedatus. Roux Arch Dev Biol 195:103–116

    Google Scholar 

  • Henry JQ, Hejnol A, Perry KJ, Martindale MQ (2007) Homology of ciliary bands in spiralian trochophores. Integr Comp Biol 47:865–871

    PubMed  Google Scholar 

  • Hermans C (1964) The reproductive and developmental biology of the opheliid polychaete Armandia brevis (Moore). University of Washington, Seatle

    Google Scholar 

  • Hessling R (2002) Metameric organisation of the nervous system in developmental stages of Urechis caupo (Echiura) and its phylogenetic implications. Zoomorphology 121:221–234

    Google Scholar 

  • Hessling R (2003) Novel aspects of the nervous system of Bonellia viridis (Echiura) revealed by the combination of immunohistochemistry, confocal laser-scanning microscopy and three-dimensional reconstruction. In: Sigvaldadóttir E et al (eds) Advances in polychaete research, vol 170, Developments in Hydrobiology. Springer, Dordrecht, pp 225–239

    Google Scholar 

  • Hessling R, Westheide W (2002) Are Echiura derived from a segmented ancestor? Immunohistochemical analysis of the nervous system in developmental stages of Bonellia viridis. J Morphol 252:100–113

    PubMed  Google Scholar 

  • Heuer C, Muller C, Todt C, Loesel R (2010) Comparative neuroanatomy suggests repeated reduction of neuroarchitectural complexity in Annelida. Front Zool 7:13

    PubMed Central  PubMed  Google Scholar 

  • Hill SD (2001) Phalloidin labelling of developing musculature in embryos of the polychaete Capitella sp. I. Biol Bull 201:257–258

    CAS  PubMed  Google Scholar 

  • Holland PWH (2001) Beyond the Hox: how widespread is homeobox gene clustering? J Anat 199:13–23

    CAS  PubMed Central  PubMed  Google Scholar 

  • Holland L, Carvalho J, Escriva H, Laudet V, Schubert M, Shimeld S, Yu J-K (2013) Evolution of bilaterian central nervous systems: a single origin? EvoDevo 4:27

    PubMed Central  PubMed  Google Scholar 

  • Huebner E, Anderson E (1976) Comparative spiralian oogenesis—structural aspects: an overview. Am Zool 16:315–343

    Google Scholar 

  • Hui J, Raible F, Korchagina N, Dray N, Samain S, Magdelenat G, Jubin C, Segurens B, Balavoine G, Arendt D, Ferrier D (2009) Features of the ancestral bilaterian inferred from Platynereis dumerilii ParaHox genes. BMC Biol 7:43

    PubMed Central  PubMed  Google Scholar 

  • Hunnekuhl VS, Bergter A, Purschke G, Paululat A (2009) Development and embryonic pattern of body wall musculature in the crassiclitellate Eisenia andrei (Annelida, Clitellata). J Morphol 270:1122–1136

    PubMed  Google Scholar 

  • Irvine SQ, Martindale MQ (2000) Expression patterns of anterior Hox genes in the polychaete Chaetopterus: correlation with morphological boundaries. Dev Biol 217:333–351

    CAS  PubMed  Google Scholar 

  • Irvine SQ, Seaver EC (2006) Early annelid development, a molecular perspective. In: Rouse GW, Pleijel F (eds) Reproductive biology and phylogeny of annelida, vol 4, Reproductive Biology and Phylogeny. Science Publishers, Enfield, pp 93–140

    Google Scholar 

  • Irvine SQ, Warinner SA, Hunter JD, Martindale MQ (1997) A survey of homeobox genes in Chaetopterus variopedatus and analysis of polychaete homeodomains. Mol Phylogenet Evol 7:331–345

    CAS  PubMed  Google Scholar 

  • Irvine SQ, Chaga O, Martindale MQ (1999) Larval ontogenetic stages of Chaetopterus: developmental heterochrony in the evolution of chaetopterid polychaetes. Biol Bull 197:313–331

    Google Scholar 

  • Iwanoff PP (1928) Die Entwicklung der Larvalsegmente bei den Anneliden. Z Morphol Okol Tiere 10:62–161

    Google Scholar 

  • Iwasa JH, Suver DW, Savage RM (2000) The leech hunchback protein is expressed in the epithelium and CNS but not in the segmental precursor lineages. Dev Genes Evol 210:277–288

    CAS  PubMed  Google Scholar 

  • Jaeckle WB, Rice ME (2002) Phylum Sipuncula. In: Young CM (ed) Atlas of marine invertebrate larvae. Academic, San Diego, pp 375–396

    Google Scholar 

  • Jägersten G (1940) Zur Kenntnis der Morphologie, Entwicklung und Taxanomie der Myzostomida. Nova Acta Regiae Soc Sci Upsal 11:1–84

    Google Scholar 

  • Jägersten G (1972) Evolution of the metazoan life cycle. Academic, London

    Google Scholar 

  • Jagla K, Bellard M, Frasch M (2001) A cluster of Drosophila homeobox genes involved in mesoderm differentiation programs. Bioessays 23:125–133

    CAS  PubMed  Google Scholar 

  • Janssen R, Le Gouar M, Pechmann M, Poulin F, Bolognesi R, Schwager EE, Hopfen C, Colbourne JK, Budd GE, Brown SJ, Prpic N-M, Kosiol C, Vervoort M, Damen WGM, Balavoine G, McGregor AP (2010) Conservation, loss, and redeployment of Wnt ligands in protostomes: implications for understanding the evolution of segment formation. BMC Evol Biol 10:374

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jeffery WR (1985) The spatial distribution of maternal mRNA is determined by a cortical cytoskeletal domain in Chaetopterus eggs. Dev Biol 110:217–229

    CAS  PubMed  Google Scholar 

  • Jeffery WR, Wilson LJ (1983) Localization of messenger RNA in the cortex of Chaetopterus eggs and early embryos. J Embryol Exp Morphol 75:225–239

    CAS  PubMed  Google Scholar 

  • Jekely G, Colombelli J, Hausen H, Guy K, Stelzer E, Nedelec F, Arendt D (2008) Mechanism of phototaxis in marine zooplankton. Nature 456:395–399

    CAS  PubMed  Google Scholar 

  • Kato C (2012) Ultrastruktur der Kopfnieren (head kidneys) von sedentären Polychaeten und ihre Bedeutung für die Phylogenie der Annelida. Rheinische Friedrich-Wilhelms-Universität Bonn

    Google Scholar 

  • Kato C, Lehrke J, Quast B (2011) Ultrastructure and phylogenetic significance of the head kidneys in Thalassema thalassemum (Thalassematinae, Echiura). Zoomorphology 130:97–106

    Google Scholar 

  • Kerner P, Zelada González F, Le Gouar M, Ledent V, Arendt D, Vervoort M (2006) The expression of a hunchback ortholog in the polychaete annelid Platynereis dumerilii suggests an ancestral role in mesoderm development and neurogenesis. Dev Genes Evol 216:821–828

    PubMed  Google Scholar 

  • Kluge B, Lehmann-Greif M, Fischer A (1995) Long-lasting exocytosis and massive structural reorganisation in the egg periphery during cortical reaction in Platynereis dumerilii (Annelida, Polychaeta). Zygote 3:141–156

    CAS  PubMed  Google Scholar 

  • Koch M, Quast B, Bartolomaeus T (2014) Coeloms and nephridia in annelids and arthropods. In: Wägele JW, Bartolomaeus T (eds) Deep metazoan phylogeny: the backbone of the tree of life – new insights from analyses of molecules, morphology, and theory of data analysis. De Gruyter, Berlin, pp 173–284

    Google Scholar 

  • Kourakis MJ, Master VA, Lokhorst DK, Nardelli-Haefliger D, Wedeen CJ, Martindale MQ, Shankland M (1997) Conserved anterior boundaries of hox gene expression in the central nervous system of the leech Helobdella. Dev Biol 190:284–300

    CAS  PubMed  Google Scholar 

  • Kristof A, Wollesen T, Wanninger A (2008) Segmental mode of neural patterning in Sipuncula. Curr Biol 18:1129–1132

    CAS  PubMed  Google Scholar 

  • Kristof A, Wollesen T, Maiorova AS, Wanninger A (2011) Cellular and muscular growth patterns during sipunculan development. J Exp Zool B Mol Dev Evol 316B:227–240

    PubMed  Google Scholar 

  • Kudenov JD (1974) The reproductive biology of Eurythoe complanata (Pallas, 1766), (Polychaeta: Amphinomidae). University of Arizona

    Google Scholar 

  • Kulakova M, Bakalenko N, Novikova E, Cook C, Eliseeva E, Steinmetz PH, Kostyuchenko R, Dondua A, Arendt D, Akam M, Andreeva T (2007) Hox gene expression in larval development of the polychaetes Nereis virens and Platynereis dumerilii (Annelida, Lophotrochozoa). Dev Genes Evol 217:39–54

    CAS  PubMed  Google Scholar 

  • Kulakova M, Cook C, Andreeva T (2008) ParaHox gene expression in larval and postlarval development of the polychaete Nereis virens (Annelida, Lophotrochozoa). BMC Dev Biol 8:61

    PubMed Central  PubMed  Google Scholar 

  • Lacalli TC (1981) Structure and development of the apical organ in trochophores of Spirobranchus polycerus, Phyllodoce maculata and Phyllodoce mucosa. Proc R Soc Lond Part B 212:381–402

    Google Scholar 

  • Lacalli TC (1984) Structure and organization of the nervous system in the trochophore larva of Spirobranchus. Philos Trans R Soc B Biol Sci 306:79–135

    Google Scholar 

  • Lacalli TC (1986) Prototroch structure and innervation in the trochophore larva of Phyllodoce (Polychaeta). Can J Zool 64:176–184

    Google Scholar 

  • Lehmacher C, Fiege D, Purschke G (2014) Immunohistochemical and ultrastructural analysis of the muscular and nervous systems in the interstitial polychaete Polygordius appendiculatus (Annelida). Zoomorphology 133:21–41

    Google Scholar 

  • Levin LA (1984) Multiple patterns of development in Streblospio benedicti Webster (Spionidae) from three coasts of North America. Biol Bull 166:494–508

    Google Scholar 

  • Lidke AK, Bannister S, Lower AM, Apel DM, Podleschny M, Kollmann M, Ackermann CF, Garcia-Alonso J, Raible F, Rebscher N (2014) 17 beta-Estradiol induces supernumerary primordial germ cells in embryos of the polychaete Platynereis dumerilii. Gen Comp Endocrinol 196:52–61

    CAS  PubMed  Google Scholar 

  • Lillie FR (1906) Observations and experiments concerning the elementary phenomena of embryonic development in Chaetopterus. J Exp Zool 3:153–268

    Google Scholar 

  • Lillie FR (1909) Polarity and bilaterality of the annelid egg. Experiments with centrifugal force. Biol Bull 16:54–79

    Google Scholar 

  • Marlow H, Tosches M, Tomer R, Steinmetz P, Lauri A, Larsson T, Arendt D (2014) Larval body patterning and apical organs are conserved in animal evolution. BMC Biol 12:7

    PubMed Central  PubMed  Google Scholar 

  • Maslakova SA, Martindale MQ, Norenburg JL (2004a) Fundamental properties of the spiralian developmental program are displayed by the basal nemertean Carinoma tremaphoros (Palaeonemertea, Nemertea). Dev Biol 267:342–360

    CAS  PubMed  Google Scholar 

  • Maslakova SA, Martindale MQ, Norenburg JL (2004b) Vestigial prototroch in a basal nemertean, Carinoma tremaphoros (Nemertea; Palaeonemertea). Evol Dev 6:219–226

    CAS  PubMed  Google Scholar 

  • McDougall C, Chen WC, Shimeld SM, Ferrier DEK (2006) The development of the larval nervous system, musculature and ciliary bands of Pomatoceros lamarckii (Annelida): heterochrony in polychaetes. Front Zool 3:16

    PubMed Central  PubMed  Google Scholar 

  • McEdward LR, Janies DA (1993) Life cycle evolution in asteroids: what is a larva? Biol Bull 184:255–268

    Google Scholar 

  • Meyer NP, Seaver EC (2010) Cell lineage and fate map of the primary somatoblast of the polychaete annelid Capitella teleta. Integr Comp Biol 50:756–767

    PubMed  Google Scholar 

  • Meyer N, Boyle M, Martindale M, Seaver E (2010) A comprehensive fate map by intracellular injection of identified blastomeres in the marine polychaete Capitella teleta. EvoDevo 1:8

    PubMed Central  PubMed  Google Scholar 

  • Mileikovsky SA (1960) Appurtenance of a polychaete larva of the rostraria type from plankton of the Norwegian and Barents Seas of the species Euphrosyne borealis Oersted 1843 and of all larvae of this type to the families Euphrosynidae and Amphinomidae (Polychaeta, Errantia, Amphinomimorpha) [in Russian]. Dokl Akad Nauk SSSR 134:731–734

    Google Scholar 

  • Mileikovsky SA (1961) Assignment of two Rostraria-type polychaete larvae from the plankton of the Northwest Atlantic to species Amphinome passasi Quatrefages 1865 and Chloenea atlantica McIntosh 1885 (Polychaeta, Errantia, Amphinomimorpha) [in Russian]. Dokl Akad Nauk SSSR 141:1109–1112

    Google Scholar 

  • Miyamoto N, Shinozaki A, Fujiwara Y (2013) Neuroanatomy of the vestimentiferan tubeworm Lamellibrachia satsuma provides insights into the evolution of the polychaete nervous system. PLoS ONE 8:e55151

    CAS  PubMed Central  PubMed  Google Scholar 

  • Müller MCM (2006) Polychaete nervous systems: ground pattern and variations-cLS microscopy and the importance of novel characteristics in phylogenetic analysis. Integr Comp Biol 46:125–133

    PubMed  Google Scholar 

  • Nardelli-Haefliger D, Shankland M (1993) Lox10, a member of the NK-2 homeobox gene class, is expressed in a segmental pattern in the endoderm and in the cephalic nervous system of the leech Helobdella. Development 118:877–892

    CAS  PubMed  Google Scholar 

  • Nelson JA (1904) The early development of Dinophilus: a study in cell-lineage. Proc Acad Natl Sci Phila 56:687–737

    Google Scholar 

  • Nielsen C (2004) Trochophore larvae: cell-lineages, ciliary bands, and body regions. 1. Annelida and Mollusca. J Exp Zool B Mol Dev Evol 302B:35–68

    Google Scholar 

  • Nielsen C (2009) How did indirect development with planktotrophic larvae evolve? Biol Bull 216:203–215

    PubMed  Google Scholar 

  • Nielsen C (2012) Animal evolution – interrelationships of the living phyla, 3rd edn. Oxford University Press, New York

    Google Scholar 

  • Okada K (1957) Annelida. In: Kumé M, Dan K (eds) Invertebrate embryology. NOLIT, Belgrade, pp 192–241

    Google Scholar 

  • Orrhage L, Müller MCM (2005) Morphology of the nervous system of Polychaeta (Annelida). Hydrobiologia 535(536):79–111

    Google Scholar 

  • Osborn KJ, Rouse GW, Goffredi SK, Robison BH (2007) Description and relationships of Chaetopterus pugaporcinus, an unusual pelagic polychaete (Annelida, Chaetopteridae). Biol Bull 212:40–54

    CAS  PubMed  Google Scholar 

  • Park B, Cho S-J, Tak E, Lee B, Park S (2006) The existence of all three ParaHox genes in the clitellate annelid, Perionyx excavatus. Dev Genes Evol 216:551–553

    CAS  PubMed  Google Scholar 

  • Paxton H (2005) Molting polychaete jaws—ecdysozoans are not the only molting animals. Evol Dev 7:337–340

    PubMed  Google Scholar 

  • Pechenik JA (1999) On the advantages and disadvantages of larval stages in benthic marine invertebrate life cycles. Mar Ecol Prog Ser 177:269–297

    Google Scholar 

  • Pernet B (2003) Persistent ancestral feeding structures in nonfeeding annelid larvae. Biol Bull 205:295–307

    PubMed  Google Scholar 

  • Peterson KJ, Irvine SQ, Cameron RA, Davidson EH (2000) Quantitative assessment of Hox complex expression in the indirect development of the polychaete annelid Chaetopterus sp. Proc Natl Acad Sci 97:4487–4492

    CAS  PubMed Central  PubMed  Google Scholar 

  • Phillips NE, Pernet B (1996) Capture of large particles by suspension-feeding scaleworm larvae (Polychaeta: Polynoidae). Biol Bull 191:199–208

    Google Scholar 

  • Pilger JF (2002) Phylum Echiura. In: Young CM (ed) Atlas of marine invertebrate larvae. Academic, San Diego, pp 371–373

    Google Scholar 

  • Prevedelli D, Massamba N’Siala G, Ansaloni I, Simonini R (2007) Life cycle of Marphysa sanguinea (Polychaeta: Eunicidae) in the Venice Lagoon (Italy). Mar Ecol 28:384–393

    Google Scholar 

  • Prud’homme B, de Rosa R, Arendt D, Julien J-F, Pajaziti R, Dorresteijn AWC, Adoutte A, Wittbrodt J, Balavoine G (2003) Arthropod-like expression patterns of engrailed and wingless in the annelid Platynereis dumerilii suggest a role in segment formation. Curr Biol 13:1876–1881

    PubMed  Google Scholar 

  • Purschke G (1997) Ultrastructure of nuchal organs in polychaetes (Annelida)—new results and review. Acta Zool 78:123–143

    Google Scholar 

  • Purschke G (2002) On the ground pattern of Annelida. Org Div Evol 2:181–196

    Google Scholar 

  • Purschke G, Müller MCM (2006) Evolution of body wall musculature. Integr Comp Biol 46:497–507

    CAS  PubMed  Google Scholar 

  • Purschke G, Hessling R, Westheide W (2000) The phylogenetic position of the Clitellata and the Echiura – on the problematic assessment of absent characters. J Zool Syst Evol Res 38:165–173

    Google Scholar 

  • Purschke G, Arendt D, Hausen H, Müller MCM (2006) Photoreceptor cells and eyes in Annelida. Arthropod Struct Dev 35:211–230

    PubMed  Google Scholar 

  • Purschke G, Bleidorn C, Struck TH (2014) Systematics, evolution and phylogeny of Annelida – a morphological perspective. Mem Museum Victoria 71:247–269

    Google Scholar 

  • Qian P, Dahms HU (2006) Larval ecology of the Annelida. In: Rouse GW, Pleijel F (eds) Reproductive biology and phylogeny of Annelida, vol 4. Science Publisher, Enfield, pp 179–232

    Google Scholar 

  • Raible F, Tessmar-Raible K, Osoegawa K, Wincker P, Jubin C, Balavoine G, Ferrier DEK, Benes V, De Jong P, Weissenbach J, Bork P, Arendt D (2005) Vertebrate-type intron-rich genes in the marine annelid Platynereis dumerilii. Science 310:1325–1326

    CAS  PubMed  Google Scholar 

  • Rebscher N, Lidke AK, Ackermann CF (2012) Hidden in the crowd: primordial germ cells and somatic stem cells in the mesodermal posterior growth zone of the polychaete Platynereis dumerilii are two distinct cell populations. EvoDevo 3:1–11

    Google Scholar 

  • Rice ME (1976) Larval development and metamorphosis in Sipuncula. Am Zool 16:563–571

    Google Scholar 

  • Rieger RM (1980) A new group of interstitial worms, Lobatocerebridae nov. fam. (Annelida) and its significance for metazoan phylogeny. Zoomorphologie 95:41–84

    Google Scholar 

  • Rieger RM (1991) Jennaria pulchra, nov.gen. nov.spec., eine den psammobionten Anneliden nahestehende Gattung aus dem Küstengrundwasser von North Carolina. Ber Naturwiss-Med Ver Innsb 78:203–215

    Google Scholar 

  • Rivera A, Weisblat D (2009) And Lophotrochozoa makes three: Notch/Hes signaling in annelid segmentation. Dev Genes Evol 219:37–43

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rivera AS, Gonsalves FC, Song MH, Norris BJ, Weisblat DA (2005) Characterization of Notch-class gene expression in segmentation stem cells and segment founder cells in Helobdella robusta (Lophotrochozoa; Annelida; Clitellata; Hirudinida; Glossiphoniidae). Evol Dev 7:588–599

    CAS  PubMed  Google Scholar 

  • Rouse GW (1999) Trochophore concepts: ciliary bands and the evolution of larvae in spiralian Metazoa. Biol J Linn Soc 66:411–464

    Google Scholar 

  • Rouse GW (2000a) The epitome of hand waving? Larval feeding and hypothesis of metazoan phylogeny. Evol Dev 2:222–233

    Google Scholar 

  • Rouse GW (2000b) Bias? What bias? The evolution of downstream larval feeding in animals. Zool Scr 29:213–236

    Google Scholar 

  • Rouse GW (2006) Annelid larval morphology. In: Rouse GW, Pleijel F (eds) Reproductive biology and phylogeny of annelida, vol 4. Science Publisher, Enfield, pp 141–177

    Google Scholar 

  • Rouse GW, Wilson NG, Goffredi SK, Johnson SB, Smart T, Widmer C, Young CM, Vrijenhoek RC (2009) Spawning and development in Osedax boneworms (Siboglinidae, Annelida). Mar Biol 156:395–405

    Google Scholar 

  • Saudemont A, Dray N, Hudry B, Le Gouar M, Vervoort M, Balavoine G (2008) Complementary striped expression patterns of NK homeobox genes during segment formation in the annelid Platynereis. Dev Biol 317:430–443

    CAS  PubMed  Google Scholar 

  • Schneider SQ, Bowerman B (2007) β-Catenin asymmetries after all animal/vegetal- oriented cell divisions in Platynereis dumerilii embryos mediate binary cell-fate specification. Dev Cell 13:73–86

    CAS  PubMed  Google Scholar 

  • Schneider S, Fischer A, Dorresteijn AC (1992) A morphometric comparison of dissimilar early development in sibling species of Platynereis (Annelida, Polychaeta). Roux Arch Dev Biol 201:243–256

    Google Scholar 

  • Scholtz G (2002) The Articulata hypothesis – or what is a segment? Org Divers Evol 2:197–215

    Google Scholar 

  • Schulze A, Halanych K (2003) Siboglinid evolution shaped by habitat preference and sulfide tolerance. Hydrobiologia 496:199–205

    Google Scholar 

  • Seaver EC (2003) Segmentation: mono- or polyphyletic? Int J Dev Biol 47:583–595

    PubMed  Google Scholar 

  • Seaver EC, Kaneshige LM (2006) Expression of ‘segmentation’ genes during larval and juvenile development in the polychaetes Capitella sp. I and H. elegans. Dev Biol 289:179–194

    CAS  PubMed  Google Scholar 

  • Seaver EC, Shankland M (2001) Establishment of segment polarity in the ectoderm of the leech Helobdella. Development 128:1629–1641

    CAS  PubMed  Google Scholar 

  • Seaver EC, Paulson DA, Irvine SQ, Martindale MQ (2001) The spatial and temporal expression of Ch-en, the engrailed gene in the polychaete Chaetopterus, does not support a role in body axis segmentation. Dev Biol 236:195–209

    CAS  PubMed  Google Scholar 

  • Seaver EC, Thamm K, Hill SD (2005) Growth patterns during segmentation in the two polychaete annelids. Capitella sp. I and Hydroides elegans: comparisons at distinct life history stages. Evol Dev 7:312–326

    PubMed  Google Scholar 

  • Seaver E, Yamaguchi E, Richards G, Meyer N (2012) Expression of the pair-rule gene homologs runt, Pax3/7, even-skipped-1 and even-skipped-2 during larval and juvenile development of the polychaete annelid Capitella teleta does not support a role in segmentation. EvoDevo 3:1–18

    Google Scholar 

  • Shankland M, Martindale MQ, Nardelli-Haefliger D, Baxter E, Price DJ (1991) Origin of segmental identity in the development of the leech nervous system. Development 113:29–38

    Google Scholar 

  • Shearer C (1911) On the development and structure of the trochophore of Hydroides uncinatus (Eupomatus). Quart J Microsc Sci 56:543–590

    Google Scholar 

  • Shimizu T (1995) Role of the cytoskeleton in the generation of spatial patterns in Tubifex eggs. Curr Top Dev Biol 31:197–235

    CAS  PubMed  Google Scholar 

  • Shimizu T (1999) Cytoskeletal mechanisms of ooplasmic segregation in annelid eggs. Int J Dev Biol 43:11–18

    CAS  PubMed  Google Scholar 

  • Shimizu T, Nakamoto A (2001) Segmentation in annelids: cellular and molecular basis for metameric body plan. Zool Sci 18:285–298

    Google Scholar 

  • Simakov O, Marletaz F, Cho S-J, Edsinger-Gonzales E, Havlak P, Hellsten U, Kuo D-H, Larsson T, Lv J, Arendt D, Savage R, Osoegawa K, de Jong P, Grimwood J, Chapman JA, Shapiro H, Aerts A, Otillar RP, Terry AY, Boore JL, Grigoriev IV, Lindberg DR, Seaver EC, Weisblat DA, Putnam NH, Rokhsar DS (2013) Insights into bilaterian evolution from three spiralian genomes. Nature 493:526–531

    CAS  PubMed Central  PubMed  Google Scholar 

  • Smart TI, Von Dassow G (2009) Unusual development of the mitraria larva in the polychaete Owenia collaris. Biol Bull 217:253–268

    PubMed  Google Scholar 

  • Snow P, Buss LW (1994) HOM/Hox-type homeoboxes from Stylaria lacustris (Annelida: Oligochaeta). Mol Phylogenet Evol 3:360–364

    CAS  PubMed  Google Scholar 

  • Song MH, Huang FZ, Chang GY, Weisblat DA (2002) Expression and function of an even-skipped homolog in the leech Helobdella robusta. Development 129:3681–3692

    CAS  PubMed  Google Scholar 

  • Song MH, Huang FZ, Gonsalves FC, Weisblat DA (2004) Cell cycle-dependent expression of a hairy and enhancer of split (hes) homolog during cleavage and segmentation in leech embryos. Dev Biol 269:183–195

    CAS  PubMed  Google Scholar 

  • Southward EC (1999) Development of Perviata and Vestimentifera (Pogonophora). Hydrobilogia 402:185–202

    Google Scholar 

  • Spengel JW (1879) Beiträge zur Kenntnis der Gephyreen. I. Die Eibildung, die Entwicklung und das Männchen der Bonellia. Mitt Zool Stn Neapel 1:357–420

    Google Scholar 

  • Steinmetz PRH, Urbach R, Posnien N, Eriksson J, Kostyuchenko RP, Brena C, Guy K, Akam M, Bucher G, Arendt D (2010) Six3 demarcates the anterior-most developing brain region in bilaterian animals. EvoDevo 1:1–9

    Google Scholar 

  • Steinmetz PRH, Kostyuchenko RP, Fischer A, Arendt D (2011) The segmental pattern of otx, gbx, and Hox genes in the annelid Platynereis dumerilii. Evol Dev 13:72–79

    PubMed  Google Scholar 

  • Stollewerk A, Schoppmeier M, Damen WGM (2003) Involvement of Notch and Delta genes in spider segmentation. Nature 423:863–865

    CAS  PubMed  Google Scholar 

  • Strathmann RR (1993) Hypotheses on the origins of marine larvae. Annu Rev Ecol Syst 24:89–117

    Google Scholar 

  • Struck TH (2006) Progenetic species in polychaetes (Annelida) and problems assessing their phylogenetic affiliation. Integr Comp Biol 46:558–568

    PubMed  Google Scholar 

  • Struck TH (2011) Direction of evolution within Annelida and the definition of Pleistoannelida. J Zool Syst Evol Res 49:340–345

    Google Scholar 

  • Struck TH, Paul C, Hill N, Hartmann S, Hösel C, Kube M, Lieb B, Meyer A, Tiedemann R, Purschke G, Bleidorn C (2011) Phylogenomic analyses unravel annelid evolution. Nature 471:95–98

    CAS  PubMed  Google Scholar 

  • Tautz D (2004) Segmentation. Dev Cell 7:301–312

    CAS  PubMed  Google Scholar 

  • Tessmar-Raible K, Arendt D (2003) Emerging systems: between vertebrates and arthropods, the Lophotrochozoa. Curr Opin Genet Dev 13:331–340

    CAS  PubMed  Google Scholar 

  • Tessmar-Raible K, Raible F, Christodoulou F, Guy K, Rembold M, Hausen H, Arendt D (2007) Conserved sensory-neurosecretory cell types in annelid and fish forebrain: insights into hypothalamus evolution. Cell 129:1389–1400

    CAS  PubMed  Google Scholar 

  • Thamm K, Seaver EC (2008) Notch signaling during larval and juvenile development in the polychaete annelid Capitella sp. I. Dev Biol 320:304–318

    CAS  PubMed  Google Scholar 

  • Thorson G (1950) Reproductive and larval ecology of marine bottom invertebrates. Biol Rev 25:1–45

    CAS  PubMed  Google Scholar 

  • Tzetlin AB, Filippova AV (2005) Muscular system in polychaetes (Annelida). Hydrobiologia 535(536):113–126

    Google Scholar 

  • Tzetlin A, Purschke G (2005) Pharynx and intestine. Hydrobiologia 535(536):199–225

    Google Scholar 

  • Voronezhskaya EE, Tsitrin EB, Nezlin LP (2003) Neuronal development in larval polychaete Phyllodoce maculata (Phyllodocidae). J Comp Neurol 455:299–309

    PubMed  Google Scholar 

  • Wagner GP, Amemiya C, Ruddle F (2003) Hox cluster duplications and the opportunity for evolutionary novelties. Proc Natl Acad Sci 100:14603–14606

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wanninger A (2009) Shaping the things to come: ontogeny of lophotrochozoan neuromuscular systems and the tetraneuralia concept. Biol Bull 216:293–306

    PubMed  Google Scholar 

  • Wanninger A, Koop D, Bromham L, Noonan E, Degnan BM (2005) Nervous and muscle system development in Phascolion strombus (Sipuncula). Dev Genes Evol 215:509–518

    PubMed  Google Scholar 

  • Wanninger A (2008) Comparative lophotrochozoan neurogenesis and larval neuroanatomy: recent advances from previously neglected taxa. Acta Biologica Hungarica 59(Suppl.):127–136

    Google Scholar 

  • Wedeen CJ, Weisblat DA (1991) Segmental expression of an engrailed-class gene during early development and neurogenesis in an annelid. Development 113:805–814

    CAS  PubMed  Google Scholar 

  • Weigert A, Helm C, Meyer M, Nickel B, Arendt D, Hausdorf B, Santos SR, Halanych KM, Purschke G, Bleidorn C, Struck TH (2014) Illuminating the base of the annelid tree using transcriptomics. Mol Biol Evol 31:1391–1401

    CAS  PubMed  Google Scholar 

  • Weisblat DA, Blair SS (1984) Developmental interdeterminacy in embryos of the leech Helobdella triserialis. Dev Biol 101:326–335

    CAS  PubMed  Google Scholar 

  • Weisblat DA, Huang FZ (2001) An overview of glossiphoniid leech development. Can J Zool 79:218–232

    Google Scholar 

  • Werbrock AH, Meiklejohn DA, Sainz A, Iwasa JH, Savage RM (2001) A polychaete hunchback ortholog. Dev Biol 235:476–488

    CAS  PubMed  Google Scholar 

  • Westheide W (1987) Progenesis as a principle in meiofauna evolution. J Nat Hist 21:843–854

    Google Scholar 

  • Wilson EB (1890) The origin of the mesoblast-bands in annelids. J Morphol 4:205–219

    Google Scholar 

  • Wilson EB (1892) The cell lineage of Nereis: a contribution to the cytogeny of the annelid body. J Morphol 6:361–480

    Google Scholar 

  • Wilson EB (1898) Considerations on cell-lineage and ancestral reminiscence based on a re-examination of some points in the early development of annelids and polycladids. Ann N Y Acad Sci 11:1–27

    Google Scholar 

  • Wilson DP (1932) On the mitraria larva of Owenia fusiformis Delle Chiaje. Philos Trans R Soc B Biol Sci B221:231–334

    Google Scholar 

  • Wilson DP (1982) The larval development of three species of Magelona (Polychaeta) from localitites near Plymouth. J Mar Biol Ass UK 62:385–401

    Google Scholar 

  • Wilson WH (1991) Sexual reproductive modes in polychaetes: classification and diversity. Bull Mar Sci 48:500–516

    Google Scholar 

  • Winchell CJ, Valencia JE, Jacobs DK (2010) Confocal analysis of nervous system architecture in direct-developing juveniles of Neanthes arenaceodentata (Annelida, Nereididae). Front Zool 7:17

    PubMed Central  PubMed  Google Scholar 

  • Woltereck R (1904) Beiträge zur praktischen Analyse der Polygordius-Entwicklung nach dem “Nordsee-” und dem “Mittelmeertypus”. Wilhelm Roux Arch für Entwickl Mech Org 18:377–403

    Google Scholar 

  • Wong VY, Aisemberg GO, Gan WB, Macagno ER (1995) The leech homeobox gene Lox4 may determine segmental differentiation of identified neurons segmental differentiation of identified neurons. J Neurosci 15:5551–5559

    CAS  PubMed  Google Scholar 

  • Worsaae K, Kristensen R (2005) Evolution of interstitial Polychaeta (Annelida). In: Bartolomaeus T, Purschke G (eds) Morphology, molecules, evolution and phylogeny in polychaeta and related taxa. Developments in hydrobiology, vol 179. Springer, Dordrecht, pp 319–340

    Google Scholar 

  • Worsaae K, Rouse GW (2008) Is Diurodrilus an annelid? J Morphol 269:1426–1455

    PubMed  Google Scholar 

  • Worsaae K, Rouse GW (2010) The simplicity of males: dwarf males of four species of Osedax (Siboglinidae; Annelida) investigated by confocal laser scanning microscopy. J Morphol 271:127–142

    PubMed  Google Scholar 

  • Worsaae K, Nygren A, Rouse GW, Giribet G, Persson J, Sundberg P, Pleijel F (2005) Phylogenetic position of Nerillidae and Aberranta (Polychaeta, Annelida), analysed by direct optimization of combined molecular and morphological data. Zool Scr 34:313–328

    Google Scholar 

  • Wysocka-Diller J, Aisemberg GO, Macagno ER (1995) A novel homeobox cluster expressed in repeated strucutres of the midgut. Dev Biol 171:439–447

    CAS  PubMed  Google Scholar 

  • Zakas C, Wares JP (2012) Consequences of a poecilogonous life history for genetic structure in coastal populations of the polychaete Streblospio benedicti. Mol Ecol 21:5447–5460

    PubMed  Google Scholar 

  • Zhang Z-Q (2011) Animal biodiversity: an outline of higher-level classification and survey of taxonomic richness. Zootaxa 3147:1–237

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christoph Bleidorn .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer-Verlag Wien

About this chapter

Cite this chapter

Bleidorn, C., Helm, C., Weigert, A., Aguado, M.T. (2015). Annelida. In: Wanninger, A. (eds) Evolutionary Developmental Biology of Invertebrates 2. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1871-9_9

Download citation

Publish with us

Policies and ethics