Organisms Diversity & Evolution

, Volume 16, Issue 2, pp 345–362

Current status of annelid phylogeny

Review

Abstract

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.

Keywords

Annelida Evo-devo Evolution Model organism Phylogenomics Polychaeta 

References

  1. Achim, K., Pettit, J.-B., Saraiva, L. R., Gavriouchkina, D., Larsson, T., Arendt, D., et al. (2015). High-throughput spatial mapping of single-cell RNA-seq data to tissue of origin. Nature Biotechnology, 33, 503–509.PubMedCrossRefGoogle Scholar
  2. Aguado, M. T., Capa, M., Oceguera-Figueroa, A., & Rouse, G. W. (2014). Annelida. In P. Vargas & R. Zardoya (Eds.), The tree of life: evolution and classification of living organisms (pp. 254–269). Sunderland: Sinauer.Google Scholar
  3. Aguado, M., Helm, C., Weidhase, M., & Bleidorn, C. (2015a). Description of a new syllid species as a model for evolutionary research of reproduction and regeneration in annelids. Organisms, Diversity and Evolution, 15, 1–21.CrossRefGoogle Scholar
  4. Aguado, M. T., Glasby, C. J., Schroeder, P. C., Weigert, A., & Bleidorn, C. (2015b). The making of a branching annelid: an analysis of complete mitochondrial genome and ribosomal data of Ramisyllis multicaudata. Scientific Reports, 5, 12072.PubMedPubMedCentralCrossRefGoogle Scholar
  5. Almeida, W., Christoffersen, M., Amorim, D., Garraffoni, A., & Silva, G. (2003). Polychaeta, Annelida and Articulata are not monophyletic: articulating the Metameria (Metazoa, Coelomata). Revista Brasileira de Zoologia, 20, 23–57.CrossRefGoogle Scholar
  6. Andrade, S. C. S., Novo, M., Kawauchi, G. Y., Worsaae, K., Pleijel, F., Giribet, G., et al. (2015). Articulating “archiannelids”: phylogenomics and annelid relationships, with emphasis on meiofaunal taxa. Molecular Biology and Evolution, 32, 2860–2875.PubMedCrossRefGoogle Scholar
  7. Arenas-Mena, C. (2007). Sinistral equal-size spiral cleavage of the indirectly developing polychaete Hydroides elegans. Developmental Dynamics, 23, 1611–1622.CrossRefGoogle Scholar
  8. Arendt, D. (2011). Annelids who's who. Nature, 471, 44–45.PubMedCrossRefGoogle Scholar
  9. Arendt, D., Denes, A. S., Jékely, G., & Tessmar-Raible, K. (2008). The evolution of nervous system centralization. Philosophical Transactions of the Royal Society, B: Biological Sciences, 363, 1523–1528.PubMedCentralCrossRefGoogle Scholar
  10. Arendt, D., Technau, U., & Wittbrodt, J. (2001). Evolution of the bilaterian larval foregut. Nature, 409, 81–85.PubMedCrossRefGoogle Scholar
  11. Arendt, D., Tessmar-Raible, K., Snyman, H., Dorresteijn, A. W., & Wittbrodt, J. (2004). Ciliary photoreceptors with a vertebrate-type opsin in an invertebrate brain. Science, 306, 869–871.PubMedCrossRefGoogle Scholar
  12. Arias, A., Barroso, R., Anadón, N., & Paiva, P. C. (2013). On the occurrence of the fireworm Eurythoe complanata complex (Annelida, Amphinomidae) in the Mediterranean Sea with an updated revision of the alien Mediterranean amphinomids. ZooKeys, 337, 19–33.PubMedCrossRefGoogle Scholar
  13. Backfisch, B., Kozin, V. V., Kirchmaier, S., Tessmar-Raible, K., & Raible, F. (2014). Tools for gene-regulatory analyses in the marine annelid Platynereis dumerilii. PLoS ONE, 9, e93076.PubMedPubMedCentralCrossRefGoogle Scholar
  14. Backfisch, B., Veedin Rajan, V. B., Fischer, R. M., Lohs, C., Arboleda, E., Tessmar-Raible, K., et al. (2013). Stable transgenesis in the marine annelid Platynereis dumerilii sheds new light on photoreceptor evolution. Proceedings of the National Academy of Sciences, 110, 193–198.CrossRefGoogle Scholar
  15. Bannister, S., Antonova, O., Polo, A., Lohs, C., Hallay, N., Valinciute, A., et al. (2014). TALENs mediate efficient and heritable mutation of endogenous genes in the marine annelid Platynereis dumerilii. Genetics, 197, 77–89.PubMedPubMedCentralCrossRefGoogle Scholar
  16. Barroso, R., Klautau, M., Solé-Cava, A., & Paiva, P. (2010). Eurythoe complanata (Polychaeta: Amphinomidae), the ‘cosmopolitan’ fireworm, consists of at least three cryptic species. Marine Biology, 157, 69–80.CrossRefGoogle Scholar
  17. Bartolomaeus, T. (1995). Secondary monociliarity in the Annelida: monociliated epidermal cells in larvae of Magelona mirabilis (Magelonida). Microfauna Marina, 10, 327–332.Google Scholar
  18. Bergter, A., Brubacher, J. L., & Paululat, A. (2008). Muscle formation during embryogenesis of the polychaete Ophryotrocha diadema (Dorvilleidae)—new insights into annelid muscle patterns. Frontiers in Zoology, 5, 1.PubMedPubMedCentralCrossRefGoogle Scholar
  19. Bernt, M., Bleidorn, C., Braband, A., Dambach, J., Donath, A., Fritzsch, G., et al. (2013). A comprehensive analysis of bilaterian mitochondrial genomes and phylogeny. Molecular Phylogenetics and Evolution, 69, 352–364.PubMedCrossRefGoogle Scholar
  20. Bleidorn, C. (2007). The role of character loss in phylogenetic reconstruction as exemplified for the Annelida. Journal of Zoological Systematics and Evolutionary Research, 45, 299–307.CrossRefGoogle Scholar
  21. Bleidorn, C. (2009). Annelid phylogeny—molecular analysis with emphasis on model annelids. In D. Shain (Ed.), Annelids as model systems in the biological sciences (pp. 13–29). Hoboken: Wiley.CrossRefGoogle Scholar
  22. Bleidorn, C., Eeckhaut, I., Podsiadlowski, L., Schult, N., McHugh, D., Halanych, K. M., et al. (2007). Mitochondrial genome and nuclear sequence data support Myzostomida as part of the annelid radiation. Molecular Biology and Evolution, 24, 1690–1701.PubMedCrossRefGoogle Scholar
  23. Bleidorn, C., Helm, C., Weigert, A., & Aguado, M. (2015). Annelida. In A. Wanninger (Ed.), Evolutionary developmental biology of invertebrates 2 (pp. 193–230). Vienna: Springer.CrossRefGoogle Scholar
  24. Bleidorn, C., Helm, C., Weigert, A., Eeckhaut, I., Lanterbecq, D., Struck, T. H., et al. (2014). From morphology to phylogenomics: Placing the enigmatic Myzostomida in the tree of life. In J. W. Wägele & T. Bartolomaeus (Eds.), Deep Metazoan phylogeny: the backbone of the tree of life. new insights from analyses of molecules, morphology, and theory of data analysis (pp. 161–172). Berlin: De Gruyter.Google Scholar
  25. Bleidorn, C., Hill, N., Erseus, C., & Tiedemann, R. (2009a). On the role of character loss in orbiniid phylogeny (Annelida): molecules vs. morphology. Molecular Phylogenetics and Evolution, 52, 57–69.PubMedCrossRefGoogle Scholar
  26. Bleidorn, C., Podsiadlowski, L., Zhong, M., Eeckhaut, I., Hartmann, S., Halanych, K. M., et al. (2009b). On the phylogenetic position of Myzostomida: can 77 genes get it wrong? BMC Evolutionary Biology, 9, 150.PubMedPubMedCentralCrossRefGoogle Scholar
  27. Bleidorn, C., Vogt, L., & Bartolomaeus, T. (2003a). A contribution to sedentary polychaete phylogeny using 18S rRNA sequence data. Journal of Zoological Systematics and Evolutionary Research, 41, 186–195.CrossRefGoogle Scholar
  28. Bleidorn, C., Vogt, L., & Bartolomaeus, T. (2003b). New insights into polychaete phylogeny (Annelida) inferred from 18S rDNA sequences. Molecular Phylogenetics and Evolution, 29, 279–288.PubMedCrossRefGoogle Scholar
  29. Bolker, J. A. (1995). Model systems in developmental biology. Bioessays, 17, 451–455.PubMedCrossRefGoogle Scholar
  30. Boore, J. L. (1999). Animal mitochondrial genomes. Nucleic Acids Research, 27(8), 1767–1780. doi:10.1093/nar/27.8.1767.
  31. Boore, J. L., & Brown, W. M. (1994). Mitochondrial genomes and the phylogeny of mollusks. Nautilus, 108, 61–78.Google Scholar
  32. Boore, J. L., & Brown, W. M. (2000). Mitochondrial genomes of Galathealinum, Helobdella, and Platynereis: sequence and gene arrangement comparisons indicate the Pogonophora is not a phylum and Annelida and Arthropoda are not sister taxa. Molecular Biology and Evolution, 17, 988–988.CrossRefGoogle Scholar
  33. Boore, J. L., & Staton, J. L. (2002). The mitochondrial genome of the sipunculid Phascolopsis gouldii supports its association with Annelida rather than Mollusca. Molecular Biology and Evolution, 19, 127–137.PubMedCrossRefGoogle Scholar
  34. Borda, E., Yáñez-Rivera, B., Ochoa, G. M., Kudenov, J. D., Sanchez-Ortiz, C., Schulze, A., et al. (2015). Revamping Amphinomidae (Annelida: Amphinomida), with the inclusion of Notopygos. Zoologica Scripta, 44, 324–333.CrossRefGoogle Scholar
  35. Boyle, M. J., & Rice, M. E. (2014). Sipuncula: an emerging model of spiralian development and evolution. International Journal of Developmental Biology, 58, 485–499.PubMedCrossRefGoogle Scholar
  36. Boyle, M. J., & Seaver, E. C. (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.PubMedPubMedCentralCrossRefGoogle Scholar
  37. Brown, S., Rouse, G., Hutchings, P., & Colgan, D. (1999). Assessing the usefulness of histone H3, U2 snRNA and 28S rDNA in analyses of polychaete relationships. Australian Journal of Zoology, 47, 499–516.CrossRefGoogle Scholar
  38. Brusca, R. C., & Brusca, G. J. (2003). Invertebrates (2nd ed.). Sunderland: Sinauer.Google Scholar
  39. Bubko, O. V., & Minichev, Y. S. (1972). Nervous system in Oweniidae (Polychaeta). Zoologichesky Zhurnal, 51, 1288–1299.Google Scholar
  40. Capa, M., Parapar, J., & Hutchings, P. (2012). Phylogeny of Oweniidae (Polychaeta) based on morphological data and taxonomic revision of Australian fauna. Zoological Journal of the Linnean Society, 166, 236–278.CrossRefGoogle Scholar
  41. Cho, S. J., Valles, Y., Giani, V. C., Jr., Seaver, E. C., & Weisblat, D. A. (2010). Evolutionary dynamics of the wnt gene family: a lophotrochozoan perspective. Molecular Biology and Evolution, 27, 1645–1658.PubMedPubMedCentralCrossRefGoogle Scholar
  42. Clark, R. B. (1964). Dynamics in metazoan evolution. The origin of the coelom and segments. Oxford: Clarendon.Google Scholar
  43. Colgan, D. J., Hutchings, P. A., & Braune, M. (2006). A multigene framework for polychaete phylogenetic studies. Organisms Diversity and Evolution, 6, 220–235.CrossRefGoogle Scholar
  44. Dales, R.P. (1963). Annelids (Hutchinson University Library). LondonGoogle Scholar
  45. De Robertis, E. M. (2008). Evo-Devo: variations on ancestral themes. Cell, 132, 185–195.PubMedPubMedCentralCrossRefGoogle Scholar
  46. Dordel, J., Fisse, F., Purschke, G., & Struck, T. H. (2010). Phylogenetic position of Sipuncula derived from multi-gene and phylogenomic data and its implication for the evolution of segmentation. Journal of Zoological Systematics and Evolutionary Research, 48, 197–207.Google Scholar
  47. Dozsa-Farxas, K., & Schlaghamersky, J. (2013). Hrabeiella periglandulata (Annelida: "Polychaeta")—do apparent differences in chaetal ultrastructure indicate the existence of several species in Europe? Acta Zoologica Academiae Scientiarum Hungaricae, 59, 143–156.Google Scholar
  48. Dray, N., Tessmar-Raible, K., Le Gouar, M., Vibert, L., Christodoulou, F., Schipany, K., et al. (2010). Hedgehog signaling regulates segment formation in the annelid Platynereis. Science, 329, 339–342.PubMedPubMedCentralCrossRefGoogle Scholar
  49. Dunn, C. W., Giribet, G., Edgecombe, G. D., & Hejnol, A. (2014). Animal phylogeny and its evolutionary implications. Annual Review of Ecology, Evolution, and Systematics, 45, 371–395.CrossRefGoogle Scholar
  50. Dunn, C. W., Hejnol, A., Matus, D. Q., Pang, K., Browne, W. E., Smith, S. A., et al. (2008). Broad phylogenomic sampling improves resolution of the animal tree of life. Nature, 452, 745–749.PubMedCrossRefGoogle Scholar
  51. Eeckhaut, I., McHugh, D., Mardulyn, P., Tiedemann, R., Monteyne, D., Jangoux, M., et al. (2000). Myzostomida: a link between trochozoans and flatworms? Proceedings of the Royal Society B, 267, 1383–1392.PubMedPubMedCentralCrossRefGoogle Scholar
  52. Eibye-Jacobsen, D. (2004). A reevaluation of Wiwaxia and the polychaetes of the Burgess Shale. Lethaia, 37, 317–335.CrossRefGoogle Scholar
  53. Eibye-Jacobsen, D., & Vinther, J. (2012). Reconstructing the ancestral annelid. Journal of Zoological Systematics and Evolutionary Research, 50, 85–87.CrossRefGoogle Scholar
  54. Fauchald, K. (1974). Polychaete phylogeny: a problem in protostome evolution. Systematic Zoology, 23, 493–506.CrossRefGoogle Scholar
  55. Fauchald, K. (1977). In The polychaete worms. Definitions and keys to the orders, families and genera. (Vol. Science Series 28): Natural History Museum of Los Angeles County.Google Scholar
  56. Fauchald, K., & Rouse, G. (1997). Polychaete systematics: past and present. Zoologica Scripta, 26, 71–138.CrossRefGoogle Scholar
  57. Fauvel, P. (1923). Polychètes errantes. Faune de France, 5, 1–488.Google Scholar
  58. Fauvel, P. (1927). Polychètes Sédentaires. Addenda aux Errantes, Archiannélides, Myzostomaires. Faune de France, 16, 1–494.Google Scholar
  59. Ferrier, D. E. K. (2012). Evolutionary crossroads in developmental biology: annelids. Development, 139, 2643–2653.PubMedCrossRefGoogle Scholar
  60. Ferrier, D. E. K., & Holland, P. W. H. (2001). Sipunculan ParaHox genes. Evolution & Development, 3, 263–270.CrossRefGoogle Scholar
  61. 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.PubMedCrossRefGoogle Scholar
  62. Fischer, A. H. L., Henrich, T., & Arendt, D. (2010). The normal development of Platynereis dumerilii (Nereididae, Annelida). Frontiers in Zoology, 7, 31.PubMedPubMedCentralCrossRefGoogle Scholar
  63. Frobius, A. C., Matus, D. Q., & Seaver, E. C. (2008). Genomic organization and expression demonstrate spatial and temporal Hox gene colinearity in the lophotrochozoan Capitella sp I. PLoS ONE, 3, e4004.PubMedPubMedCentralCrossRefGoogle Scholar
  64. Fröbius, A. C., & Seaver, E. C. (2006). ParaHox gene expression in the polychaete annelid Capitella sp. I. Development Genes and Evolution, 216, 81–88.PubMedCrossRefGoogle Scholar
  65. Gardiner, S. L. (1978). Fine structure of the ciliated epidermis on the tentacles of Owenia fusiformis (Polychaeta, Oweniidae). Zoomorphologie, 91, 37–48.CrossRefGoogle Scholar
  66. Giani, V. C., Yamaguchi, E., Boyle, M. J., & Seaver, E. C. (2011). Somatic and germline expression of piwi during development and regeneration in the marine polychaete annelid Capitella teleta. Evodevo, 2, 10Google Scholar
  67. Giere, O., & Erseus, C. (1998). A systematic account of the Questidae (Annelida, Polychaeta), with description of new taxa. Zoologica Scripta, 27, 345–360.CrossRefGoogle Scholar
  68. Giere, O. W., & Riser, N. W. (1981). Questidae—Polychaetes with oligochaetoid morphology and development. Zoologica Scripta, 10, 95–103.CrossRefGoogle Scholar
  69. Glasby, C., & Timm, T. (2008). Global diversity of polychaetes (Polychaeta; Annelida) in freshwater. In E. V. Balian, C. Lévêque, H. Segers, & K. Martens (Eds.), Freshwater Animal Diversity Assessment (Vol. 198, pp. 107–115, Developments in Hydrobiology). Netherlands: Springer.Google Scholar
  70. Golombek, A., Tobergte, S., Nesnidal, M. P., Purschke, G., & Struck, T. H. (2013). Mitochondrial genomes to the rescue—Diurodrilidae in the myzostomid trap. Molecular Phylogenetics and Evolution, 68, 312–326.PubMedCrossRefGoogle Scholar
  71. Graff, L. v. (1877). Das Genus Myzostoma (F.S. Leuckart). Leipzig: Wilhelm Engelmann.Google Scholar
  72. Grube, A. E. (1850). Die Familien der Anneliden. Archiv für Naturgeschichte Berlin, 1691, 249–364.Google Scholar
  73. Halanych, K. M., Dahlgren, T. G., & McHugh, D. (2002). Unsegmented Annelids? Possible origins of four lophotrochozoan worm taxa. Integrative and Comparative Biology, 42, 678–684.PubMedCrossRefGoogle Scholar
  74. Hatschek, B. (1878). Studien über Entwicklungsgeschichte der Anneliden. Ein Beitrag zur Morphologie der Bilaterien. Arbeiten aus den Zoologischen Instituten der Universität Wien, 1, 277–404Google Scholar
  75. Hausdorf, B., Helmkampf, M., Meyer, A., Witek, A., Herlyn, H., Bruchhaus, I., et al. (2007). Spiralian phylogenomics supports the resurrection of Bryozoa comprising Ectoprocta and Entoprocta. Molecular Biology and Evolution, 24, 2723–2729.PubMedCrossRefGoogle Scholar
  76. Helm, C., Adamo, H., Hourdez, S., & Bleidorn, C. (2014). An immunocytochemical window into the development of Platynereis massiliensis (Annelida, Nereididae). International Journal of Developmental Biology, 58, 613–622.PubMedCrossRefGoogle Scholar
  77. Hermans, C. O. (1969). The systematic position of the Archiannelida. Systematic Zoology, 18, 85–102.CrossRefGoogle Scholar
  78. Hessling, R., & Purschke, G. (2000). Immunohistochemical (cLSM) and ultrastructural analysis of the central nervous system and sense organs in Aeolosoma hemprichi (Annelida, Aeolosomatidae). Zoomorphology, 120, 65–78.CrossRefGoogle Scholar
  79. Hill, S. D., & Savage, R. M. (2009). Evolution, development and ecology of Capitella sp. I: A Waxing Model for Polychaete Studies. In Annelids in Modern Biology (pp. 88–115): WileyGoogle Scholar
  80. Hints, O., & Eriksson, M. E. (2007). Diversification and biogeography of scolecodont bearing polychaetes in the Ordovician. Palaeogeography, Palaeoclimatology, Palaeoecology, 245, 95–114.CrossRefGoogle Scholar
  81. Huang, D. Y., Chen, J. Y., Vannier, J., & Salinas, J. I. S. (2004). Early Cambrian sipunculan worms from southwest China. Proceedings of the Royal Society B, 271, 1671–1676.PubMedPubMedCentralCrossRefGoogle Scholar
  82. Irvine, S. Q., & Martindale, M. Q. (2000). Expression patterns of anterior Hox genes in the polychaete Chaetopterus: correlation with morphological boundaries. Developmental Biology, 217, 333–351.PubMedCrossRefGoogle Scholar
  83. Irvine, S. Q., Warinner, S. A., Hunter, J. D., & Martindale, M. Q. (1997). A survey of homeobox genes in Chaetopterus variopedatus and analysis of polychaete homeodomains. Molecular Phylogenetics and Evolution, 7, 331–345.PubMedCrossRefGoogle Scholar
  84. Iwasa, J. H., Suver, D. W., & Savage, R. M. (2000). The leech hunchback protein is expressed in the epithelium and CNS but not in the segmental precursor lineages. Development Genes and Evolution, 210, 277–288.PubMedCrossRefGoogle Scholar
  85. Jenner, R. A. (2014). Macroevolution of animal body plans: is there science after the tree? BioScience, 64, 653–664.CrossRefGoogle Scholar
  86. Jenner, R. A., & Wills, M. A. (2007). The choice of model organisms in evo-devo. Nature Reviews Genetics, 8(4), 311–314.PubMedCrossRefGoogle Scholar
  87. Jennings, R. M., & Halanych, K. M. (2005). Mitochondrial genomes of Clymenella torquata (Maldanidae) and Riftia pachyptila (Siboglinidae): evidence for conserved gene order in Annelida. Molecular Biology and Evolution, 22, 210–222.PubMedCrossRefGoogle Scholar
  88. Johansson, K. E. (1937). Über Lamellisabella zachsi und ihre systematische Stellung. Zoologischer Anzeiger, 117, 23–26.Google Scholar
  89. Jolly, M. T., Viard, F., Gentil, F., Thiebaut, E., & Jollivet, D. (2006). Comparative phylogeography of two coastal polychaete tubeworms in the Northeast Atlantic supports shared history and vicariant events. Molecular Ecology, 15, 1841–1855.PubMedCrossRefGoogle Scholar
  90. 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. Development Genes and Evolution, 216, 821–828.PubMedCrossRefGoogle Scholar
  91. Kerbl, A., Bekkouche, N., Sterrer, W., & Worsaae, K. (2015). Detailed reconstruction of the nervous and muscular system of Lobatocerebridae with an evaluation of its annelid affinity. BMC Evolutionary Biology, 15, 277.PubMedPubMedCentralCrossRefGoogle Scholar
  92. Kim, C. B., Moon, S. Y., Gelder, S. R., & Kim, W. (1996). Phylogenetic relationships of annelids, molluscs, and arthropods evidenced from molecules and morphology. Journal of Molecular Evolution, 43, 207–215.PubMedCrossRefGoogle Scholar
  93. Koh, B. S., & Bhaud, M. (2001). Description of Owenia gomsoni n. sp. (Oweniidae, Annelida Polychaeta) from the Yellow Sea and evidence that Owenia fusiformis is not a cosmopolitan species. Vie et milieu, 51, 77–87.Google Scholar
  94. Kojima, S. (1998). Paraphyletic status of Polychaeta suggested by phylogenetic analysis based on the amino acid sequences of elongation factor-1 alpha. Molecular Phylogenetics and Evolution, 9, 255–261.PubMedCrossRefGoogle Scholar
  95. Kristensen, R. M., & Niilonen, T. (1982). Structural studies on Diurodrilus Remane (Diurodrilidae fam. n.), with description of Diurodrilus westheidei sp. n. from the Arctic interstitial meiobenthos, W. Greenland. Zoologica Scripta, 11, 1–12.CrossRefGoogle Scholar
  96. Kristof, A., Wollesen, T., Maiorova, A. S., & Wanninger, A. (2011). Cellular and muscular growth patterns during sipunculan development. Journal of Experimental Zoology Part B, Molecular and Developmental Evolution, 316B, 227–240.PubMedCrossRefGoogle Scholar
  97. Kristof, A., Wollesen, T., & Wanninger, A. (2008). Segmental mode of neural patterning in Sipuncula. Current Biology, 18, 1129–1132.PubMedCrossRefGoogle Scholar
  98. Kudenov, J. D. (1974). The reproductive biology of Eurythoe complanata (Pallas, 1766), (Polychaeta: Amphinomidae). Tucson: University of Arizona.Google Scholar
  99. Kulakova, M., Bakalenko, N., Novikova, E., Cook, C. E., Eliseeva, E., Steinmetz, P. R. H., et al. (2007). Hox gene expression in larval development of the polychaetes Nereis virens and Platynereis dumerilii (Annelida, Lophotrochozoa). Development Genes and Evolution, 217, 39–54.PubMedCrossRefGoogle Scholar
  100. Kulakova, M. A., Cook, C. E., & Andreeva, T. F. (2008). ParaHox gene expression in larval and postlarval development of the polychaete Nereis virens (Annelida, Lophotrochozoa). BMC Developmental Biology, 8, 61.PubMedPubMedCentralCrossRefGoogle Scholar
  101. Kupriyanova, E. K., ten Hove, H. A., Sket, B., Zakšek, V., Trontelj, P., & Rouse, G. W. (2009). Evolution of the unique freshwater cave-dwelling tube worm Marifugia cavatica (Annelida: Serpulidae). Systematics and Biodiversity, 7, 389–401.CrossRefGoogle Scholar
  102. Kvist, S., & Siddall, M. E. (2013). Phylogenomics of Annelida revisited: a cladistic approach using genome-wide expressed sequence tag data mining and examining the effects of missing data. Cladistics, 29, 435–448.CrossRefGoogle Scholar
  103. Lamarck, J.-B. M. (1818). Histoire naturelle des animaux sans vertebres. Deterville/Verdiere, Paris Google Scholar
  104. Laumer, C. E., Bekkouche, N., Kerbl, A., Goetz, F., Neves, R. C., Sorensen, M. V., et al. (2015). Spiralian phylogeny informs the evolution of microscopic lineages. Current Biology, 25, 2000–2006.PubMedCrossRefGoogle Scholar
  105. Lauri, A., Brunet, T., Handberg-Thorsager, M., Fischer, A. H. L., Simakov, O., Steinmetz, P. R. H., et al. (2014). Development of the annelid axochord: insights into notochord evolution. Science, 345, 1365–1368.PubMedCrossRefGoogle Scholar
  106. Li, Y., Kocot, K. M., Schander, C., Santos, S. R., Thornhill, D. J., & Halanych, K. M. (2015). Molecular Phylogenetics and Evolution, 85, 221–229.PubMedCrossRefGoogle Scholar
  107. Liu, J., Ou, Q., Han, J., Li, J., Wu, Y., Jiao, G., et al. (2015). Lower Cambrian polychaete from China sheds light on early annelid evolution. The Science of Nature, 102, 1–7.CrossRefGoogle Scholar
  108. Martindale, M. Q., & Hejnol, A. (2009). A developmental perspective: changes in the position of the blastopore during bilaterian evolution. Developmental Cell, 17, 162–174.PubMedCrossRefGoogle Scholar
  109. McCormack, J. E., Hird, S. M., Zellmer, A. J., Carstens, B. C., & Brumfield, R. T. (2013). Applications of next-generation sequencing to phylogeography and phylogenetics. Molecular Phylogenetics and Evolution, 66, 526–538.PubMedCrossRefGoogle Scholar
  110. McDougall, C., Korchagina, N., Tobin, J. L., & Ferrier, D. E. K. (2011). Annelid Distalless/Dlx duplications reveal varied post-duplication fates. BMC Evolutionary Biology, 11, 241.PubMedPubMedCentralCrossRefGoogle Scholar
  111. McHugh, D. (1997). Molecular evidence that echiurans and pogonophorans are derived annelids. Proceedings of the National Academy of Sciences of the United States of America, 94, 8006–8009.PubMedPubMedCentralCrossRefGoogle Scholar
  112. McHugh, D. (2000). Molecular phylogeny of the Annelida. Canadian Journal of Zoology, 78, 1873–1884.CrossRefGoogle Scholar
  113. Mehr, S., Verdes, A., DeSalle, R., Sparks, J., Pieribone, V., & Gruber, D. F. (2015). Transcriptome sequencing and annotation of the polychaete Hermodice carunculata (Annelida, Amphinomidae). BMC Genomics, 16, 445.PubMedPubMedCentralCrossRefGoogle Scholar
  114. Meyer, N., Carrillo-Baltodano, A., Moore, R., & Seaver, E. (2015). Nervous system development in lecithotrophic larval and juvenile stages of the annelid Capitella teleta. Frontiers in Zoology, 12, 15.PubMedPubMedCentralCrossRefGoogle Scholar
  115. Milinkovitch, M. C., & Tzika, A. (2007). Escaping the mouse trap: the selection of new Evo-Devo model species. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 308B, 337–346.CrossRefGoogle Scholar
  116. Moon, S., Kim, C., Gelder, S., & Kim, W. (1996). Phylogenetic positions of the aberrant branchiobdellidans and aphanoneurans within the Annelida as derived from 18S ribosomal RNA gene sequences. Hydrobiologia, 324, 229–236.CrossRefGoogle Scholar
  117. Mortimer, K., & Mackie, A. S. Y. (2014). Morphology, feeding and behaviour of British Magelona (Annelida: Magelonidae), with discussions on the form and function of abdominal lateral pouches. Memoirs of Museum Victoria, 71, 177–201.Google Scholar
  118. Müller, M. C. M., Berenzen, A., & Westheide, W. (2003). Experiments on anterior regeneration in Eurythoe complanata (“Polychaeta”, Amphinomidae): reconfiguration of the nervous system and its function for regeneration. Zoomorphology, 122, 95–103.CrossRefGoogle Scholar
  119. Mwinyi, A., Meyer, A., Bleidorn, C., Lieb, B., Bartolomaeus, T., & Podsiadlowski, L. (2009). Mitochondrial genome sequence and gene order of Sipunculus nudus give additional support for an inclusion of Sipuncula into Annelida. BMC Genomics, 10, 27.PubMedPubMedCentralCrossRefGoogle Scholar
  120. Newby, W. W. (1940). The embryology of the echiuroid worm, Urechis caupo. (Vol. 16, Memoirs of the American Philosophical Society). Philadelphia: American Philosophical Society.Google Scholar
  121. Oakley, T., & Speiser, D. I. (2015). How complexity originates: the evolution of animal eyes. Annual Review of Ecology, Evolution, and Systematics, 46, 237–260.CrossRefGoogle Scholar
  122. Oyama, A., & Shimizu, T. (2007). Transient occurrence of vasa-expressing cells in nongenital segments during embryonic development in the oligochaete annelid Tubifex tubifex. Development Genes and Evolution, 217, 675–690.PubMedCrossRefGoogle Scholar
  123. Parry, L., Tanner, A., & Vinther, J. (2014). The origin of annelids. Palaeontology, 57, 1091–1103.CrossRefGoogle Scholar
  124. Parry, L., Vinther, J., & Edgecombe, G. D. (2015). Cambrian stem-group annelids and a metameric origin of the annelid head. Biology Letters, 11, 20150763.PubMedPubMedCentralCrossRefGoogle Scholar
  125. Pfeifer, K., Dorresteijn, A. W. C., & Frobius, A. C. (2012). Activation of Hox genes during caudal regeneration of the polychaete annelid Platynereis dumerilii. Development Genes and Evolution, 222, 165–179.PubMedCrossRefGoogle Scholar
  126. Prud'homme, B., de Rosa, R., Arendt, D., Julien, J. F., Pajaziti, R., Dorresteijn, A. W. C., et al. (2003). Arthropod-like expression patterns of engrailed and wingless in the annelid Platynereis dumerilii suggest a role in segment formation. Current Biology, 13, 1876–1881.PubMedCrossRefGoogle Scholar
  127. Prud'homme, B., Latillot, N., Balavoine, G., Adoutte, A., & Vervoort, M. (2002). Phylogenetic analysis of the wnt gene family: Insights from lophotrochozoan members. Current Biology, 12, 1395–1400.PubMedCrossRefGoogle Scholar
  128. Purschke, G. (1999). Terrestrial polychaetes—models for the evolution of the Clitellata (Annelida)? Hydrobiologia, 406, 87–99.CrossRefGoogle Scholar
  129. Purschke, G. (2002). On the ground pattern of Annelida. Organisms, Diversity and Evolution, 2, 181–196.CrossRefGoogle Scholar
  130. Purschke, G. (2003). Is Hrabeiella periglandulata (Annelida, "Polychaeta") the sister group of Clitellata? Evidence from an ultrastructural analysis of the dorsal pharynx in H. periglandulata and Enchytraeus minutus (Annelida, Clitellata). Zoomorphology, 122, 55–66.Google Scholar
  131. Purschke, G., Bleidorn, C., & Struck, T. H. (2014). Systematics, evolution and phylogeny of Annelida—a morphological perspective. Memoirs of Museum Victoria, 71, 247–269.Google Scholar
  132. Purschke, G., Hessling, R., & Westheide, W. (2000). The phylogenetic position of the Clitellata and the Echiura—on the problematic assessment of absent characters. Journal of Zoological Systematics and Evolutionary Research, 38, 165–173.CrossRefGoogle Scholar
  133. Purschke, G., & Jouin, C. (1988). Anatomy and ultrastructure of the ventral pharyngeal organs of Saccocirrus (Saccocirridae) and Protodriloides (Protodriloidae fam. n.) with remarks on the phylogenetic relationships within the Protodrilida (Annelida: Polychaeta). Journal of Zoology, 215, 405–432.CrossRefGoogle Scholar
  134. de Quatrefages, A. (1865). Note sur la classification des Annélides. Comptes rendus hebdomadaires des séances de l'Académie des sciences. Paris, 60, 586–600.Google Scholar
  135. Richter, S., Schwarz, F., Hering, L., Böggemann, M., & Bleidorn, C. (2015). The utility of genome skimming for phylogenomic analyses as demonstrated for glycerid relationships (Annelida, Glyceridae). Genome Biology and Evolution, 7, 3443–3462.PubMedPubMedCentralCrossRefGoogle Scholar
  136. Rieger, R. M. (1980). A new group of interstitial worms, Lobatocerebridae nov. fam. (Annelida) and its significance for metazoan phylogeny. Zoomorphologie, 95, 41–84.CrossRefGoogle Scholar
  137. Rieger, R. M. (1981). Fine structure of the body wall, nervous system, and digestive tract in the Lobatocerebridae Rieger and the organization of the gliointerstitial system in Annelida. Journal of Morphology, 167, 139–165.CrossRefGoogle Scholar
  138. Rieger, R. M. (1988). Comparative ultrastructure and the Lobatocerebridae: keys to understand the phylogenetic relationship of Annelida and the acoelomates. Microfauna Marina, 4, 373–382.Google Scholar
  139. Rivera, A. S., & Weisblat, D. A. (2009). And Lophotrochozoa makes three: Notch/Hes signaling in annelid segmentation. Development Genes and Evolution, 219, 37–43.PubMedPubMedCentralCrossRefGoogle Scholar
  140. Rota, E., Martin, P., & Erseus, C. (2001). Soil-dwelling polychaetes: enigmatic as ever? Some hints on their phylogenetic relationships as suggested by a maximum parsimony analysis of 18S rRNA gene sequences. Contributions to Zoology, 70, 127–138.Google Scholar
  141. Rouse, G. W., & Fauchald, K. (1997). Cladistics and polychaetes. Zoologica Scripta, 26, 139–204.CrossRefGoogle Scholar
  142. Rouse, G. W., & Fauchald, K. (1998). Recent views on the status, delineation and classification of the Annelida. American Zoologist, 38, 953–964.CrossRefGoogle Scholar
  143. Rouse, G. W., & Pleijel, F. (2001). Polychaetes (Polychaetes): Oxford University PressGoogle Scholar
  144. Rouse, G. W., & Pleijel, F. (2006). Annelid phylogeny and systematics. In G. W. Rouse & F. Pleijel (Eds.), Reproductive biology and phylogeny of Annelida (Vol. 4, pp. 3–21). Enfield: Science.Google Scholar
  145. Rousset, V., Pleijel, F., Rouse, G. W., Erseus, C., & Siddall, M. E. (2007). A molecular phylogeny of annelids. Cladistics, 23, 41–63.CrossRefGoogle Scholar
  146. Rousset, V., Rouse, G. W., Siddall, M. E., Tillier, A., & Pleijel, F. (2004). The phylogenetic position of Siboglinidae (Annelida) inferred from 18S rRNA, 28S rRNA and morphological data. Cladistics, 20, 518–533.CrossRefGoogle Scholar
  147. Rudel, D., & Sommer, R. J. (2003). The evolution of developmental mechanisms. Developmental Biology, 264, 15–37.PubMedCrossRefGoogle Scholar
  148. Seaver, E. C. (2003). Segmentation: mono- or polyphyletic? The International Journal of Developmental Biology, 47, 583–595.PubMedGoogle Scholar
  149. Seaver, E. C., & Kaneshige, L. M. (2006). Expression of ‘segmentation’ genes during larval and juvenile development in the polychaetes Capitella sp. I and H. elegans. Developmental Biology, 289, 179–194.PubMedCrossRefGoogle Scholar
  150. Seaver, E. C., Paulson, D. A., Irvine, S. Q., & Martindale, M. Q. (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. Developmental Biology, 236, 195–209.PubMedCrossRefGoogle Scholar
  151. Seaver, E. C., & Shankland, M. (2001). Establishment of segment polarity in the ectoderm of the leech Helobdella. Development, 128, 1629–1641.PubMedGoogle Scholar
  152. Seaver, E. C., Thamm, K., & Hill, S. D. (2005). Growth patterns during segmentation in the two polychaete annelids, Capitella sp. I and Hydroides elegans: comparisons at distinct life history stages. Evolution & Development, 7, 312–326.CrossRefGoogle Scholar
  153. Seaver, E. C., Yamaguchi, E., Richards, G. S., & Meyer, N. P. (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, 8.PubMedPubMedCentralCrossRefGoogle Scholar
  154. Shen, X., Ma, X. Y., Ren, J. F., & Zhao, F. Q. (2009). A close phylogenetic relationship between Sipuncula and Annelida evidenced from the complete mitochondrial genome sequence of Phascolosoma esculenta. BMC Genomics, 10, 136.PubMedPubMedCentralCrossRefGoogle Scholar
  155. Simakov, O., Marletaz, F., Cho, S.-J., Edsinger-Gonzales, E., Havlak, P., Hellsten, U., et al. (2013). Insights into bilaterian evolution from three spiralian genomes. Nature, 493, 526–531.PubMedPubMedCentralCrossRefGoogle Scholar
  156. Smart, T. I., & Von Dassow, G. (2009). Unusual development of the Mitraria larva in the polychaete Owenia collaris. Biological Bulletin, 217, 253–268.PubMedGoogle Scholar
  157. Smith, P. R., Ruppert, E. E., & Gardiner, S. L. (1987). A deuterostome-like nephridium in the Mitraria larva of Owenia fusiformis (Polychaeta, Annelida). Biological Bulletin, 172(3), 315–323.CrossRefGoogle Scholar
  158. Song, M. H., Huang, F. Z., Chang, G. Y., & Weisblat, D. A. (2002). Expression and function of an even-skipped homolog in the leech Helobdella robusta. Development, 129, 3681–3692.PubMedGoogle Scholar
  159. Sperling, E. A., Vinther, J., Moy, V. N., Wheeler, B. M., Semon, M., & Briggs, D. E. G. (2009). MicroRNAs resolve an apparent conflict between annelid systematics and their fossil record. Proceedings of the Royal Society B, 276, 4315–4322.PubMedPubMedCentralCrossRefGoogle Scholar
  160. Struck, T., Hessling, R., & Purschke, G. (2002a). The phylogenetic position of the Aeolosomatidae and Parergodrilidae, two enigmatic oligochaete-like taxa of the 'Polychaeta', based on molecular data from 18S rDNA sequences. Journal of Zoological Systematics and Evolutionary Research, 40, 155–163.CrossRefGoogle Scholar
  161. Struck, T. H., Westheide, W., & Purschke, G. (2002b). Progenesis in Eunicida ("Polychaeta," Annelida)—separate evolutionary events? Evidence from molecular data. Molecular Phylogenetics and Evolution, 25, 190–199.PubMedCrossRefGoogle Scholar
  162. Struck, T. H. (2011). Direction of evolution within Annelida and the definition of Pleistoannelida. Journal of Zoological Systematics and Evolutionary Research, 49, 340–345.CrossRefGoogle Scholar
  163. Struck, T. H. (2013a). The impact of paralogy on phylogenomic studies—a case study on annelid relationships. PLoS ONE, 8, e62892.PubMedPubMedCentralCrossRefGoogle Scholar
  164. Struck, T. H. (2013b). Phylogeny. In W. Westheide, & G. Purschke (Eds.), Handbook of Zoology. Annelida. Berlin: DeGruyter.Google Scholar
  165. Struck, T. H., Golombek, A., Weigert, A., Franke, F. A., Westheide, W., Purschke, G., et al. (2015). The evolution of annelids reveals two adaptive routes to the interstitial realm. Current Biology, 25, 1993–1999.PubMedCrossRefGoogle Scholar
  166. Struck, T. H., Nesnidal, M. P., Purschke, G., & Halanych, K. M. (2008). Detecting possibly saturated positions in 18S and 28S sequences and their influence on phylogenetic reconstruction of Annelida (Lophotrochozoa). Molecular Phylogenetics and Evolution, 48, 628–645.PubMedCrossRefGoogle Scholar
  167. Struck, T. H., Paul, C., Hill, N., Hartmann, S., Hosel, C., Kube, M., et al. (2011). Phylogenomic analyses unravel annelid evolution. Nature, 471, 95–98.PubMedCrossRefGoogle Scholar
  168. Struck, T. H., & Purschke, G. (2005). The sister group relationship of Aeolosomatidae and Potamodrilidae (Annelida:"Polychaeta")—a molecular phylogenetic approach based on 18S rDNA and cytochrome oxidase I. Zoologischer Anzeiger, 243, 281–293.CrossRefGoogle Scholar
  169. Struck, T. H., Schult, N., Kusen, T., Hickman, E., Bleidorn, C., McHugh, D., et al. (2007). Annelid phylogeny and the status of Sipuncula and Echiura. BMC Evolutionary Biology, 7, 57.PubMedPubMedCentralCrossRefGoogle Scholar
  170. Struck, T. H., Wey-Fabrizius, A. R., Golombek, A., Hering, L., Weigert, A., Bleidorn, C., et al. (2014). Platyzoan paraphyly based on phylogenomic data supports a noncoelomate ancestry of Spiralia. Molecular Biology and Evolution, 31, 1833–1849.PubMedCrossRefGoogle Scholar
  171. Tautz, D. (2004). Segmentation. Developmental Cell, 7, 301–312.PubMedCrossRefGoogle Scholar
  172. Telford, M. J., & Budd, G. E. (2003). The place of phylogeny and cladistics in Evo-Devo research. International Journal of Developmental Biology, 47, 479–490.PubMedGoogle Scholar
  173. Tessmar-Raible, K., & Arendt, D. (2003). Emerging systems: between vertebrates and arthropods, the Lophotrochozoa. Current Opinion in Genetics & Development, 13, 331–340.CrossRefGoogle Scholar
  174. Tessmar-Raible, K., Steinmetz, P. R. H., Snyman, H., Hassel, M., & Arendt, D. (2005). Fluorescent two-color whole mount in situ hybridization in Platynereis dumerilii (Polychaeta, Annelida), an emerging marine molecular model for evolution and development. Biotechniques, 39, 460–464.PubMedCrossRefGoogle Scholar
  175. Wanninger, A., Koop, D., Bromham, L., Noonan, E., & Degnan, B. M. (2005). Nervous and muscle system development in Phascolion strombus (Sipuncula). Development Genes and Evolution, 215, 509–518.PubMedCrossRefGoogle Scholar
  176. Weidhase, M., Bleidorn, C.; Beckers, P., & Helm, C. (in press) Myoanatomy and anterior muscle regeneration of the fireworm Eurythoe cf. complanata (Annelida: Amphinomidae). Journal of Morphology.Google Scholar
  177. Weigert, A., Golombek, A., Gerth, M., Schwarz, F., Struck, T. H., & Bleidorn, C. (2016). Evolution of mitochondrial gene order in Annelida. Molecular Phylogenetics and Evolution, 94, 196–206.PubMedCrossRefGoogle Scholar
  178. Weigert, A., Helm, C., Meyer, M., Nickel, B., Arendt, D., Hausdorf, B., et al. (2014). Illuminating the base of the annelid tree using transcriptomics. Molecular Biology and Evolution, 31, 1391–1401.PubMedCrossRefGoogle Scholar
  179. Weisblat, D. A., & Kuo, D. H. (2009). Helobdella (leech): a model for developmental studies. Cold Spring Harbor Protocols, 2009(4), pdb emo121.Google Scholar
  180. Werbrock, A. H., Meiklejohn, D. A., Sainz, A., Iwasa, J. H., & Savage, R. M. (2001). A polychaete hunchback ortholog. Developmental Biology, 235, 476–488.PubMedCrossRefGoogle Scholar
  181. Westheide, W. (2008). Polychaetes: interstitial families: keys and notes for the identification of the species. Synopses of the British fauna (New Series), 44 (second edition). Field Studies Council: Shrewsbury, UKGoogle Scholar
  182. Wilson, D. P. (1982). The larval development of three species of Magelona (Polychaeta) from localities near Plymouth. Journal of the Marine Biological Association of the United Kingdom, 62, 385–401.CrossRefGoogle Scholar
  183. Winchell, C. J., & Jacobs, D. K. (2013). Expression of the Lhx genes apterous and lim1 in an errant polychaete: implications for bilaterian appendage evolution, neural development, and muscle diversification. EvoDevo, 4, 4.PubMedPubMedCentralCrossRefGoogle Scholar
  184. Winnepenninckx, B., Backeljau, T., & De Wachter, R. (1995). Phylogeny of protostome worms derived from 18S rRNA sequences. Molecular Biology and Evolution, 12, 641–649.PubMedGoogle Scholar
  185. Winnepenninckx, B. M. H., Van de Peer, Y., & Backeljau, T. (1998). Metazoan relationships on the basis of 18S rRNA sequences: a few years late. American Zoologist, 38, 888–906.CrossRefGoogle Scholar
  186. Worsaae, K., & Kristensen, R. M. (2005). Evolution of interstitial Polychaeta (Annelida). Hydrobiologia, 535, 319–340.Google Scholar
  187. Worsaae, K., & Rouse, G. W. (2008). Is Diurodrilus an Annelid? Journal of Morphology, 269, 1426–1455.PubMedCrossRefGoogle Scholar
  188. Wu, Z. G., Shen, X., Sun, M. A., Ren, J. F., Wang, Y. J., Huang, Y. L., et al. (2009). Phylogenetic analyses of complete mitochondrial genome of Urechis unicinctus (Echiura) support that echiurans are derived annelids. Molecular Phylogenetics and Evolution, 52, 558–562.PubMedCrossRefGoogle Scholar
  189. Zantke, J., Bannister, S., Rajan, V. B. V., Raible, F., & Tessmar-Raible, K. (2014). Genetic and genomic tools for the marine annelid Platynereis dumerilii. Genetics, 197, 19–31.PubMedPubMedCentralCrossRefGoogle Scholar
  190. Zhang, Z.-Q. (2011). Animal biodiversity: an introduction to higher-level classification and taxonomic richness. Zootaxa, 3148, 7–12.Google Scholar
  191. Zrzavý, J. (2001). Myzostomida are not annelids: molecular and morphological support for a clade of animals with anterior sperm flagella. Cladistics, 17, 170–198.CrossRefGoogle Scholar
  192. Zrzavy, J., Riha, P., Pialek, L., & Janouskovec, J. (2009). Phylogeny of Annelida (Lophotrochozoa): total-evidence analysis of morphology and six genes. BMC Evolutionary Biology, 9, 189.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Gesellschaft für Biologische Systematik 2016

Authors and Affiliations

  1. 1.Molecular Evolution and Animal SystematicsUniversity of LeipzigLeipzigGermany
  2. 2.German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-LeipzigLeipzigGermany

Personalised recommendations