Organisms Diversity & Evolution

, Volume 11, Issue 2, pp 151–172 | Cite as

Higher-level metazoan relationships: recent progress and remaining questions

  • Gregory D. EdgecombeEmail author
  • Gonzalo Giribet
  • Casey W. Dunn
  • Andreas Hejnol
  • Reinhardt M. Kristensen
  • Ricardo C. Neves
  • Greg W. Rouse
  • Katrine Worsaae
  • Martin V. Sørensen


Metazoa comprises 35–40 phyla that include some 1.3 million described species. Phylogenetic analyses of metazoan interrelationships have progressed in the past two decades from those based on morphology and/or targeted-gene approaches using single and then multiple loci to the more recent phylogenomic approaches that use hundreds or thousands of genes from genome and transcriptome sequencing projects. A stable core of the tree for bilaterian animals is now at hand, and instability and conflict are becoming restricted to a key set of important but contentious relationships. Acoelomorph flatworms (Acoela + Nemertodermatida) and Xenoturbella are sister groups. The position of this clade remains controversial, with different analyses supporting either a sister-group relation to other bilaterians (=Nephrozoa, composed of Protostomia and Deuterostomia) or membership in Deuterostomia. The main clades of deuterostomes (Ambulacraria and Chordata) and protostomes (Ecdysozoa and Spiralia) are recovered in numerous analyses based on varied molecular samples, and also receive anatomical and developmental support. Outstanding issues in protostome phylogenetics are the position of Chaetognatha within the protostome clade, and the monophyly of a group of spiralians collectively named Platyzoa. In contrast to the broad consensus over key questions in bilaterian phylogeny, the relationships of the five main metazoan lineages—Porifera, Ctenophora, Placozoa, Cnidaria and Bilateria—remain subject to conflicting topologies according to different taxonomic samples and analytical approaches. Whether deep bilaterian divergences such as the split between protostome and deuterostome clades date to the Cryogenian or Ediacaran (and, thus, the extent to which the pre-Cambrian fossil record is incomplete) is sensitive to dating methodology.


Phylogenomics Expressed sequence tags Animal evolution Bilateria Ecdysozoa Spiralia 



Rudolf Meier requested this review and handled the paper for the journal. We thank him, Olaf Bininda-Emonds, Andreas Schmidt-Rhaesa and a second, anonymous reviewer for providing comments that helped to improve an earlier version of this manuscript. Claus Nielsen and Akiko Okusu kindly made the line drawings used in Figure 1 available, which improved upon earlier versions by Miquel A. Arnedo. The Carlsberg Foundation provided funding for collecting in Greenland (grant 2009_01_0053). This work is supported by the National Science Foundation under the AToL program (grants EF05-31757, EF05-31558 and EF05-31677).

Supplementary material

13127_2011_44_MOESM1_ESM.doc (70 kb)
ESM 1 (DOC 70 kb)


  1. Adoutte, A., Balavoine, G., Lartillot, N., Lespinet, O., Prud’homme, B., & de Rosa, R. (2000). The new animal phylogeny: reliability and implications. Proceedings of the National Academy of Sciences of the USA, 97, 4453–4456.PubMedCrossRefGoogle Scholar
  2. Aguinaldo, A. M. A., Turbeville, J. M., Lindford, L. S., Rivera, M. C., Garey, J. R., Raff, R. A., et al. (1997). Evidence for a clade of nematodes, arthropods and other moulting animals. Nature, 387, 489–493.PubMedCrossRefGoogle Scholar
  3. Ahlrichs, W. H. (1995). Seison annulatus und Seison nebaliae—Ultrastruktur und Phylogenie. Verhandlungen der Deutschen Zoologischen Gesellschaft, 88, 155.Google Scholar
  4. Aldridge, R. J., Hou, X.-G., Siveter, D. J., Siveter, D. J., & Gabbott, S. E. (2007). The systematics and phylogenetic relationships of vetulicolians. Palaeontology, 50, 131–168.CrossRefGoogle Scholar
  5. Arendt, D., Technau, U., & Wittbrodt, J. (2001). Evolution of the bilaterian larval foregut. Nature, 409, 81–85.PubMedCrossRefGoogle Scholar
  6. 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
  7. Ax, P. (1996). Multicellular animals. A new approach to the phylogenetic order in nature. Volume I. Berlin: Springer.Google Scholar
  8. Ax, P. (2001). Das System der Metazoa III. Ein Lehrbuch der phylogenetischen Systematik. Stuttgart: Spektrum Akademischer Verlag.Google Scholar
  9. Backeljau, T., Winnepenninckx, B., & De Bruyn, L. (1993). Cladistic analysis of metazoan relationships: a reappraisal. Cladistics, 9, 167–181.CrossRefGoogle Scholar
  10. Baguñà, J., Martinez, P., Paps, J., & Riutort, M. (2008). Back in time: a new systematic proposal for the Bilateria. Proceedings of the Royal Society / B, 363, 1481–1491.Google Scholar
  11. Balavoine, G., de Rosa, R., & Adoutte, A. (2002). Hox clusters and bilaterian phylogeny. Molecular Phylogenetics and Evolution, 24, 266–373.CrossRefGoogle Scholar
  12. de Beauchamp, P. (1965). Classe des Rotifères. In P. P. Grassé (Ed.), Traité de Zoologie IV, 3 (pp. 1225–1379). Paris: Masson.Google Scholar
  13. Bergström, J. (2010). The earliest arthropods and other animals. In M.-Y. Long (Ed.), Darwin’s heritage today. Proceedings of the Darwin 200 International Conference (pp. 29–42). Beijing: Higher Education Press.Google Scholar
  14. Blair, J. E. (2009). Animals (Metazoa). In S. B. Hedges & S. Kumar (Eds.), The timetree of life (pp. 223–230). Oxford: Oxford University Press.Google Scholar
  15. Blair, J. E., Ikeo, K., Gojobori, T., & Hedges, S. B. (2002). The evolutionary position of nematodes. BMC Evolutionary Biology, 2, 1–7.CrossRefGoogle Scholar
  16. 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
  17. Bleidorn, C., Podsiadlowski, L., Zhong, M., Eeckhaut, I., Hartmann, S., Halanych, K. M., et al. (2009). On the phylogenetic position of Myzostomida: can 77 genes get it wrong? BMC Evolutionary Biology, 9, 150.PubMedCrossRefGoogle Scholar
  18. Bourlat, S. J., Nielsen, C., Lockyer, A. E., Littlewood, D. T., & Telford, M. J. (2003). Xenoturbella is a deuterostome that eats molluscs. Nature, 424, 925–928.PubMedCrossRefGoogle Scholar
  19. Bourlat, S. J., Juliusdottir, T., Lowe, C. J., Freeman, R., Aronowicz, J., Kirschner, M., et al. (2006). Deuterostome phylogeny reveals monophyletic chordates and the new phylum Xenoturbellida. Nature, 444, 85–88.PubMedCrossRefGoogle Scholar
  20. Bourlat, S. J., Nielsen, C., Economou, A. D., & Telford, M. J. (2008). Testing the new animal phylogeny: a phylum level molecular analysis of the animal kingdom. Molecular Phylogenetics and Evolution, 49, 23–31.PubMedCrossRefGoogle Scholar
  21. Bourlat, S. J., Rota-Stabelli, O., Lanfear, R., & Telford, M. J. (2009). The mitochondrial genome structure of Xenoturbella bocki (phylum Xenoturbellida) is ancestral within the deuterostomes. BMC Evolutionary Biology, 9, 107.PubMedCrossRefGoogle Scholar
  22. Brown, F. D., Prendergast, A., & Swalla, B. J. (2008). Man is but a worm: chordate origins. Genesis, 46, 605–613.PubMedCrossRefGoogle Scholar
  23. Budd, G. E. (2001). Tardigrades as ‘stem-group arthropods’: the evidence from the Cambrian fauna. Zoologischer Anzeiger, 240, 265–279.CrossRefGoogle Scholar
  24. Cannon, J. T., Rychel, A. L., Eccleston, H., Halanych, K. M., & Swalla, B. J. (2009). Molecular phylogeny of Hemichordata, with updated status of deep-sea enteropneusts. Molecular Phylogenetics and Evolution, 52, 17–24.PubMedCrossRefGoogle Scholar
  25. Caron, J.-B., Conway Morris, S., & Shu, D. (2010). Tentaculate fossils from the Cambrian of Canada (British Columbia) and China (Yunnan) reinterpreted as primitive deuterostomes. PLoS ONE, 5, e9586.PubMedCrossRefGoogle Scholar
  26. Carranza, S., Baguñà, J., & Riutort, M. (1997). Are Platyhelminthes a monophyletic group? An assessment using 18S rDNA sequences. Molecular Biology and Evolution, 14, 485–497.PubMedGoogle Scholar
  27. Cavalier Smith, T. (1998). A revised six-kingdom system of life. Biological Reviews, 73, 203–266.PubMedCrossRefGoogle Scholar
  28. Conway Morris, S. (2000). The Cambrian “explosion”: slow-fuse or megatonnage? Proceedings of the National Academy of Sciences of the USA, 97, 4426–4429.PubMedCrossRefGoogle Scholar
  29. Copley, R. R., Aloy, P., Russell, R. B., & Telford, M. J. (2004). Systematic searches for synapomorphies in the model metazoan genomes give some support for Ecdysozoa after accounting for the idiosyncrasies of Caenorhabditis elegans. Evolution & Development, 6, 164–169.CrossRefGoogle Scholar
  30. Danovaro, R., Dell’Anno, A., Pusceddu, A., Gambi, C., Heiner, I., & Kristensen, R. M. (2010). The first Metazoa living in permanently anoxic conditions. BMC Biology, 8, 30.PubMedCrossRefGoogle Scholar
  31. Dellaporta, S. L., Xu, A., Sagasser, S., Jakob, W., Moreno, M. A., Buss, L. W., et al. (2006). Mitochondrial genome of Trichoplax adhaerens supports Placozoa as the basal lower metazoan phylum. Proceedings of the National Academy of Sciences of the USA, 103, 8751–8756.PubMedCrossRefGoogle Scholar
  32. Delsuc, F., Brinkmann, H., & Philippe, H. (2005). Phylogenomics and the reconstruction of the tree of life. Nature Reviews / Genetics, 6, 361–375.CrossRefGoogle Scholar
  33. Delsuc, F., Brinkmann, H., Chourrout, D., & Philippe, H. (2006). Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature, 439, 965–668.PubMedCrossRefGoogle Scholar
  34. Delsuc, F., Tsagkogeorga, G., Lartillot, N., & Philippe, H. (2008). Additional molecular support for the new chordate phylogeny. Genesis, 46, 592–604.PubMedCrossRefGoogle Scholar
  35. von Döhren, J., & Bartolomaeus, T. (2007). Ultrastructure and development of the rhabdomeric eyes in Lineus viridis (Heteronemertea, Nemertea). Zoology (Jena), 110, 430–438.Google Scholar
  36. Dong, X. (2007). Developmental sequence of Cambrian embryo Markuelia. Chinese Science Bulletin, 52, 929–935.CrossRefGoogle Scholar
  37. Dopazo, H., & Dopazo, J. (2005). Genome-scale evidence of the nematode-arthropod clade. Genome Biology, 6, R41.PubMedCrossRefGoogle Scholar
  38. Dopazo, H., Santoyo, J., & Dopazo, J. (2004). Phylogenomics and the number of characters required for obtaining an accurate phylogeny of eukaryote model species. Bioinformatics, 20(Supplement 1), I116–I121.PubMedCrossRefGoogle Scholar
  39. 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
  40. 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
  41. Edgecombe, G. D. (2010). Arthropod phylogeny: an overview from the perspectives of morphology, molecular data and the fossil record. Arthropod Structure & Development, 39, 74–87.CrossRefGoogle Scholar
  42. 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 of London, Series B, 267, 1383–1392.CrossRefGoogle Scholar
  43. Eernisse, D. J., Albert, J. S., & Anderson, F. E. (1992). Annelida and Arthropoda are not sister taxa: a phylogenetic analysis of spiralian metazoan morphology. Systematic Biology, 41, 305–330.Google Scholar
  44. Egger, B., Steinke, D., Tarui, H., De Mulder, K., Arendt, D., Borgonie, G., et al. (2009). To be or not to be a flatworm: the acoel controversy. PLoS ONE, 4, e5502.PubMedCrossRefGoogle Scholar
  45. Farris, J. S. (1970). Methods for computing Wagner trees. Systematic Zoology, 19, 83–92.CrossRefGoogle Scholar
  46. Farris, J. S., Kluge, A. G., & Eckhardt, M. J. (1970). A numerical approach to phylogenetic systematics. Systematic Zoology, 19, 172–189.CrossRefGoogle Scholar
  47. Felsenstein, J. (1973). Maximum-likelihood estimation of evolutionary trees from continuous characters. American Journal of Human Genetics, 25, 471–492.PubMedGoogle Scholar
  48. Field, K. G., Olsen, G. J., Lane, D. J., Giovannoni, S. J., Ghiselin, M. T., Raff, E. C., et al. (1988). Molecular phylogeny of the animal kingdom. Science, 239, 748–753.PubMedCrossRefGoogle Scholar
  49. Franzén, Å., & Afzelius, B. A. (1987). The ciliated epidermis of Xenoturbella bocki (Platyhelminthes, Xenoturbellida) with some phylogenetic considerations. Zoologica Scripta, 16, 9–17.CrossRefGoogle Scholar
  50. Funch, P. (1996). The chordoid larva of Symbion pandora (Cycliophora) is a modified trochophore. Journal of Morphology, 230, 231–263.CrossRefGoogle Scholar
  51. Funch, P., & Kristensen, R. M. (1995). Cycliophora is a new phylum with affinities to Entoprocta and Ectoprocta. Nature, 378, 711–714.CrossRefGoogle Scholar
  52. Gamulin, V., Muller, I. M., & Muller, W. E. (2000). Sponge proteins are more similar to those of Homo sapiens than to Caenorhabditis elegans. Biological Journal of the Linnean Society, 71, 821–828.CrossRefGoogle Scholar
  53. Ghiselin, M. T. (1988). The origin of molluscs in the light of molecular evidence. Oxford Surveys in Evolutionary Biology, 5, 66–95.Google Scholar
  54. Giribet, G. (1999). Ecdysozoa versus Articulata, dos hipótesis alternativas sobre la posición de los Artrópodos en el reino Animal. In A. Melic, J. J. de Haro, M. Méndez, & I. Ribera (Eds.), Evolución y filogenia de Arthropoda (pp. 145–160). Zaragoza: Sociedad Entomológica Aragonesa.Google Scholar
  55. Giribet, G. (2002). Current advances in the phylogenetic reconstruction of metazoan evolution. A new paradigm for the Cambrian explosion? Molecular Phylogenetics and Evolution, 24, 345–357.PubMedCrossRefGoogle Scholar
  56. Giribet, G. (2003). Molecules, development and fossils in the study of metazoan evolution; Articulata versus Ecdysozoa revisited. Zoology, 106, 303–326.PubMedCrossRefGoogle Scholar
  57. Giribet, G. (2004). ¿Articulata o Ecdysozoa?: una revisión crítica sobre la posición de los artrópodos en el reino animal. In J. E. Llorente Bousquets, J. J. Morrone, O. Yáñez Ordóñez, & I. Vargas Fernández (Eds.), Biodiversidad, taxonomía y biogeografía de artrópodos de México: Hacia una síntesis de su conocimiento. Volúmen IV (pp. 45–62). Mexico: UNAM, Facultad de Ciencias.Google Scholar
  58. Giribet, G. (2008). Assembling the lophotrochozoan (=spiralian) tree of life. Philosophical Transactions of the Royal Society, Series B, 363, 1513–1522.CrossRefGoogle Scholar
  59. Giribet, G., & Ribera, C. (1998). The position of arthropods in the animal kingdom: a search for a reliable outgroup for internal arthropod phylogeny. Molecular Phylogenetics and Evolution, 9, 481–488.PubMedCrossRefGoogle Scholar
  60. Giribet, G., & Wheeler, W. C. (1999). The position of arthropods in the animal kingdom: Ecdysozoa, islands, trees, and the “parsimony ratchet”. Molecular Phylogenetics and Evolution, 13, 619–623.PubMedCrossRefGoogle Scholar
  61. Giribet, G., Distel, D. L., Polz, M., Sterrer, W., & Wheeler, W. C. (2000). Triploblastic relationships with emphasis on the acoelomates and the position of Gnathostomulida, Cycliophora, Plathelminthes, and Chaetognatha: a combined approach using 18S rDNA sequences and morphology. Systematic Biology, 49, 539–562.PubMedCrossRefGoogle Scholar
  62. Giribet, G., Sørensen, M. V., Funch, P., Kristensen, R. M., & Sterrer, W. (2004). Investigations into the phylogenetic position of Micrognathozoa using four molecular loci. Cladistics, 20, 1–13.CrossRefGoogle Scholar
  63. Giribet, G., Dunn, C. W., Edgecombe, G. D., & Rouse, G. W. (2007). A modern look at the animal tree of life. Zootaxa, 1668, 61–79.Google Scholar
  64. Giribet, G., Dunn, C. W., Edgecombe, G. D., Hejnol, A., Martindale, M. Q., & Rouse, G. W. (2009). Assembling the spiralian tree of life. In M. J. Telford & D. T. J. Littlewood (Eds.), Animal evolution: Genes, genomes, fossils and trees (pp. 53–64). Oxford: Oxford University Press.Google Scholar
  65. Glenner, H., Hansen, A. J., Sørensen, M. V., Ronquist, F., Huelsenbeck, J. P., & Willerslev, E. (2004). Bayesian inference of metazoan phylogeny: a combined molecular and morphological approach. Current Biology, 14, 1644–1649.PubMedCrossRefGoogle Scholar
  66. Haase, A., Stern, M., Wächtler, K., & Bicker, G. (2001). A tissue-specific marker of Ecdysozoa. Development Genes and Evolution, 211, 428–433.PubMedCrossRefGoogle Scholar
  67. Haeckel, E. (1866). Generelle Morphologie der Organismen. Berlin: Georg Reimer.Google Scholar
  68. Halanych, K. M. (2004). The new view of animal phylogeny. Annual Reviews of Ecology, Evolution and Systematics, 35, 229–256.CrossRefGoogle Scholar
  69. Halanych, K. M., Bacheller, J. M., Aguinaldo, A. M. A., Liva, S. M., Hillis, D. M., & Lake, J. A. (1995). Evidence from 18S ribosomal DNA that lophophorates are protostome animals. Science, 267, 1641–1643.PubMedCrossRefGoogle Scholar
  70. Harvey, T. H. P., Dong, X., & Donoghue, P. C. J. (2010). Are palaeoscolecids ancestral ecdysozoans? Evolution & Development, 12, 177–200.CrossRefGoogle Scholar
  71. Harzsch, S., & Müller, C. H. G. (2007). A new look at the ventral nerve centre of Sagitta: implications for the phylogenetic position of Chaetognatha (arrow worms) and the evolution of the bilaterian nervous system. Frontiers in Zoology, 4, 14.PubMedCrossRefGoogle Scholar
  72. Haszprunar, G. (1996). The Mollusca: coelomate turbellarians or mesenchymate annelids? In J. D. Taylor (Ed.), Origin and evolutionary radiation of the Mollusca (pp. 1–28). Oxford: Oxford University Press.Google Scholar
  73. Haszprunar, G. (2000). Is the Aplacophora monophyletic? A cladistic point of view. American Malacological Bulletin, 15, 115–130.Google Scholar
  74. Haszprunar, G., & Wanninger, A. (2008). On the fine structure of the creeping larva of Loxosomella murmanica: additional evidence for a clade of Kamptozoa (Entoprocta) and Mollusca. Acta Zoologica, 89, 137–148.CrossRefGoogle 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. Hausdorf, B., Helmkampf, M., Nesnidal, M. P., & Bruchhaus, I. (2010). Phylogenetic relationships within the lophophorate lineages (Ectoprocta, Brachiopoda and Phoronida). Molecular Phylogenetics and Evolution, 55, 121–1127.CrossRefGoogle Scholar
  77. Hejnol, A. (2010). A twist in time—the evolution of spiral cleavage in the light of animal phylogeny. Integrative and Comparative Biology, 50, 695–706.PubMedCrossRefGoogle Scholar
  78. Hejnol, A., & Schnabel, R. (2005). The eutardigrade Thulinia stephaniae has an indeterminate development and the potential to regulate early blastomere ablations. Development, 132, 1349–1361.PubMedCrossRefGoogle Scholar
  79. Hejnol, A., & Schnabel, R. (2006). What a couple of dimensions can do for you: comparative developmental studies using 4D-microscopy—examples from tardigrade development. Integrative and Comparative Biology, 46, 151–161.CrossRefPubMedGoogle Scholar
  80. Hejnol, A., & Martindale, M. Q. (2008a). Acoel development supports a simple planula-like urbilaterian. Philosophical Transactions of the Royal Society, Series B, 363, 1493–1501.CrossRefGoogle Scholar
  81. Hejnol, A., & Martindale, M. Q. (2008b). Acoel development indicates the independent evolution of the bilaterian mouth and anus. Nature, 456, 382–386.PubMedCrossRefGoogle Scholar
  82. Hejnol, A., Martindale, M. Q., & Henry, J. Q. (2007). High-resolution fate map of the snail Crepidula fornicata: the origins of ciliary bands, nervous system, and muscular elements. Developmental Biology, 305, 63–76.PubMedCrossRefGoogle Scholar
  83. Hejnol, A., Obst, M., Stamatakis, A., Ott, M., Rouse, G. W., Edgecombe, G. D., et al. (2009). Assessing the root of bilaterian animals with scalable phylogenomic methods. Proceedings of the Royal Society, Series B, 276, 4261–4270.CrossRefGoogle Scholar
  84. Helmkampf, M., Bruchhaus, I., & Hausdorf, B. (2008a). Multigene analysis of lophophorate and chaetognath phylogenetic relationships. Molecular Phylogenetics and Evolution, 46, 206–214.PubMedCrossRefGoogle Scholar
  85. Helmkampf, M., Bruchhaus, I., & Hausdorf, B. (2008b). Phylogenomic analyses of lophophorates (brachiopods, phoronids and bryozoans) confirm the Lophotrochozoa concept. Proceedings of the Royal Society, Series B, 275, 1927–1933.CrossRefGoogle Scholar
  86. Hennig, W. (1950). Grundzüge einer Theorie der phylogenetischen Systematik. Berlin: Deutscher Zentralverlag.Google Scholar
  87. Hennig, W. (1965). Phylogenetic systematics. Annual Review of Entomology, 10, 97–166.CrossRefGoogle Scholar
  88. Hennig, W. (1966). Phylogenetic systematics. Urbana: University of Illinois Press.Google Scholar
  89. Henry, J. Q., Hejnol, A., Perry, K. J., & Martindale, M. Q. (2007). Homology of ciliary bands in spiralian trochophores. Integrative and Comparative Biology, 47, 865–871.CrossRefPubMedGoogle Scholar
  90. Hochberg, R., & Atherton, S. (2011). A new species of Lepidodasys (Gastrotricha, Macrodasyida) from Panama with a description of its peptidergic nervous system using, CLSM, anti-FMRFamide and anti-SCPB. Zoologischer Anzeiger. doi: 10.1016/j.jcz.2010.12.002.
  91. Holland, N. D., Jones, W. J., Ellena, J., Ruhl, H. A., & Smith, K. L. (2009). A new deep-sea species of epibenthic acorn worm (Hemichordata, Enteropneusta). Zoosystema, 31, 333–346.CrossRefGoogle Scholar
  92. Holton, T. A., & Pisani, D. (2010). Deep genomic-scale analyses of the Metazoa reject Coelomata: evidence from single- and multigene families analyzed under a supertree and supermatrix paradigm. Genome Biology and Evolution, 2, 310–324.PubMedCrossRefGoogle Scholar
  93. Hou, X., & Bergström, J. (2006). Dinocarids—anomalous arthropods or arthropod-like worms. In J. Rong, Z. Fang, Z. Zhou, R. Zhan, X. Wang, & X. Yuan (Eds.), Originations, radiations and biodiversity changes—Evidences from the Chinese fossil record (pp. 139–158, 847–850). Beijing: Science.Google Scholar
  94. Irimia, M., Maeso, L., Penny, D., García-Fernandez, J., & Roy, S. W. (2007). Rare coding sequence changes are consistent with Ecdysozoa, not Coelomata. Molecular Biology and Evolution, 24, 604–1607.CrossRefGoogle Scholar
  95. Janssen, R., Eriksson, J. B., Budd, G. E., Akam, M., & Prpic, N.-M. (2010). Gene expression patterns in onychophorans reveal that regionalization predates limb segmentation in pan-arthropods. Evolution & Development, 12, 363–372.CrossRefGoogle Scholar
  96. Jenner, R. A. (2001). Bilaterian phylogeny and uncritical recycling of morphological data sets. Systematic Biology, 50, 730–742.PubMedCrossRefGoogle Scholar
  97. Jenner, R. A. (2004a). The scientific status of metazoan cladistics: why current research practice must change. Zoologica Scripta, 33, 293–310.CrossRefGoogle Scholar
  98. Jenner, R. A. (2004b). Towards a phylogeny of the Metazoa: evaluating alternative phylogenetic positions of Platyhelminthes, Nemertea, and Gnathostomulida, with a critical reappraisal of cladistic characters. Contributions to Zoology, 73, 3–163.Google Scholar
  99. Jenner, R. A., & Scholtz, G. (2005). Playing another round of metazoan phylogenetics: historical epistemology, sensitivity analysis, and the position of Arthropoda within the Metazoa on the basis of morphology. In S. Koenemann, & R. A. Jenner (Eds.), Crustacea and arthropod relationships. Crustacean Issues, 16, 355–385.Google Scholar
  100. Jensen, S., Droser, M. L., & Gehling, J. G. (2005). Trace fossil preservation and the early evolution of animals. Palaeogeography, Palaeoclimatology, Palaeoecology, 220, 19–29.CrossRefGoogle Scholar
  101. Jondelius, U., Ruiz-Trillo, I., Baguñà, J., & Riutort, M. (2002). The Nemertodermatida are basal bilaterians and not members of the Platyhelminthes. Zoologica Scripta, 31, 201–215.CrossRefGoogle Scholar
  102. Kapp, H. (2000). The unique embryology of Chaetognatha. Zoologischer Anzeiger, 239, 263–266.Google Scholar
  103. Kaul, S., & Stach, T. (2010). Ontogeny of the collar cord: neurulation in the hemichordate Saccoglossus kowalevskii. Journal of Morphology, 271, 1240–1259.PubMedCrossRefGoogle Scholar
  104. Kluge, A. G., & Farris, J. S. (1969). Quantitative phyletics and the evolution of anurans. Systematic Zoology, 18, 1–32.CrossRefGoogle Scholar
  105. Kristensen, R. M. (2003). Comparative morphology: do the ultrastructural investigations of Loricifera and Tardigrada support the clade Ecdysozoa? In A. Legakis, S. Sfenthourakis, R. Polymeni, & M. Thessalou-Legaki (Eds.), The new panorama of animal evolution. Proceedings of the 18th International Congress of Zoology (pp. 467–477). Sofia: Pensoft.Google Scholar
  106. Kristensen, R. M., & Funch, P. (2000). Micrognathozoa: a new class with complicated jaws like those of Rotifera and Gnathostomulida. Journal of Morphology, 246, 1–49.PubMedCrossRefGoogle Scholar
  107. Kusche, K., Bangel, N., Mueller, C., Hildebrandt, J.-P., & Weber, W.-M. (2005). Molecular cloning and sequencing of the Na+/K+-ATPase α-subunit of the medical leech Hirudo medicinalis (Annelida)—implications for modeling protostomian evolution. Journal of Zoological Systematics and Evolutionary Research, 43, 339–342.CrossRefGoogle Scholar
  108. Kusserow, A., Pang, K., Sturm, C., Hrouda, M., Lentfer, J., Schmidt, H. A., et al. (2005). Unexpected complexity of the Wnt gene family in a sea anemone. Nature, 433, 156–160.PubMedCrossRefGoogle Scholar
  109. Lake, J. A. (1990). Origin of the metazoa. Proceedings of the National Academy of Sciences of the USA, 87, 763–766.PubMedCrossRefGoogle Scholar
  110. Lartillot, N., & Philippe, H. (2008). Improvement of molecular phylogenetic inference and phylogeny of Bilateria. Proceedings of the Royal Society, Series B, 363, 1463–1472.CrossRefGoogle Scholar
  111. Lemmons, D., Fritzenwanker, J. H., Gerhart, J., Lowe, C. J., & McGinnis, W. (2010). Co-option of an anteroposterior head axis patterning system for proximodistal patterning of appendages in early bilaterian evolution. Developmental Biology, 344, 358–362.CrossRefGoogle Scholar
  112. Longhorn, S. J., Foster, P. G., & Vogler, A. P. (2007). The nematode-arthropod clade revisited: phylogenomic analyses from ribosomal protein genes misled by shared evolutionary biases. Cladistics, 23, 130–144.CrossRefGoogle Scholar
  113. Love, G. D., Grosjean, E., Stalvies, C., Fike, D. A., Grotzinger, J. P., Bradley, A. S., et al. (2009). Fossil steroids record the appearance of Demospongiae during the Cryogenian period. Nature, 457, 718–722.PubMedCrossRefGoogle Scholar
  114. Lundin, K. (1998). The epidermal ciliary rootlets of Xenoturbella bocki (Xenoturbellida) revisited: new support for a possible kinship with the Acoelomorpha (Platyhelminthes). Zoologica Scripta, 27, 263–270.CrossRefGoogle Scholar
  115. Lundin, K. (2001). Degenerating epidermal cells in Xenoturbella bocki (phylum uncertain), Nemertodermatida and Acoela (Platyhelminthes). Belgian Journal of Zoology, 131, 153–157.Google Scholar
  116. Lüter, C. (2000). Ultrastructure of larval and adult setae of Brachiopoda. Zoologischer Anzeiger, 239, 75–90.Google Scholar
  117. Maas, A., Waloszek, D., Haug, J. T., & Müller, K. J. (2009). Loricate larvae (Scalidophora) from the Middle Cambrian of Australia. Memoirs of the Association of Australasian Palaeontologists, 37, 281–302.Google Scholar
  118. Mallatt, J., & Winchell, C. J. (2002). Testing the new animal phylogeny: first use of combined large-subunit and small-subunit rRNA gene sequences to classify the protostomes. Molecular Biology and Evolution, 19, 289–301.PubMedGoogle Scholar
  119. Mallatt, J., & Chen, J.-Y. (2003). Fossil sister group of craniates: predicted and found. Journal of Morphology, 258, 1–31.PubMedCrossRefGoogle Scholar
  120. Mallatt, J., & Giribet, G. (2006). Further use of nearly complete 28S and 18S rRNA genes to classify Ecdysozoa: 37 more arthropods and a kinorhynch. Molecular Biology and Evolution, 40, 772–794.Google Scholar
  121. Mallatt, J., & Winchell, C. J. (2007). Ribosomal RNA genes and deuterostome phylogeny revisited: more cyclostomes, elasmobranchs, reptiles, and a brittle star. Molecular Phylogenetics and Evolution, 43, 1005–1022.PubMedCrossRefGoogle Scholar
  122. Mallatt, J., Garey, J. R., & Shultz, J. W. (2004). Ecdysozoan phylogeny and Bayesian inference: first use of nearly complete 28S and 18S rRNA gene sequences to classify the arthropods and their kin. Molecular Phylogenetics and Evolution, 31, 179–191.CrossRefGoogle Scholar
  123. Mallatt, J., Craig, C. W., & Yoder, M. J. (2010). Nearly complete rRNA genes assembled from across the metazoan animals: effects of more taxa, a structure-based alignment, and paired-sites evolutionary models on phylogenetic reconstruction. Molecular Phylogenetics and Evolution, 55, 1–17.PubMedCrossRefGoogle Scholar
  124. Marlétaz, F., Martin, E., Perez, Y., Papillon, D., Caubit, X., Lowe, C. J., et al. (2006). Chaetognath phylogenomics: a protostome with deuterostome-like development. Current Biology, 16, R578.CrossRefGoogle Scholar
  125. Martindale, M. Q., Pang, K., & Finnerty, J. R. (2004). Investigating the origins of triploblasty: ‘mesodermal’ gene expression in a diploblastic animal, the sea anemone Nematostella vectensis (phylum, Cnidaria; class, Anthozoa). Development, 131, 2463–2474.PubMedCrossRefGoogle Scholar
  126. Maslakova, S. A., Martindale, M. Q., & Norenburg, J. L. (2004a). Fundamental properties of the spiralian developmental program are displayed by the basal nemertean Carinoma tremaphoros (Palaeonemertea, Nemertea). Developmental Biology, 267, 342–360.PubMedCrossRefGoogle Scholar
  127. Maslakova, S. A., Martindale, M. Q., & Norenburg, J. L. (2004b). Vestigial prototroch in a basal nemertean, Carinoma tremaphoros (Nemertea; Palaeonemertea). Evolution & Development, 6, 219–226.CrossRefGoogle Scholar
  128. Matus, D. Q., Copley, R. R., Dunn, C. W., Hejnol, A., Eccleston, H., Halanych, K. M., et al. (2006). Broad taxon and gene sampling indicate that chaetognaths are protostomes. Current Biology, 16, R575–R576.PubMedCrossRefGoogle Scholar
  129. Meusemann, K., von Reumont, B. M., Simon, S., Roeding, F., Strauss, S., Kuck, P., et al. (2010). A phylogenomic approach to resolve the arthropod tree of life. Molecular Biology and Evolution, 27, 2451–2464.PubMedCrossRefGoogle Scholar
  130. Meyer, N. P., Boyle, M. J., Martindale, M. Q., & Seaver, E. C. (2010). A comprehensive fate map by intracellular injection of identified blastomeres in the marine polychaete Capitella teleta. EvoDevo, 1/8.Google Scholar
  131. 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.PubMedCrossRefGoogle Scholar
  132. Neuhaus, B., & Higgins, R. P. (2002). Ultrastructure, biology, and phylogenetic relationships of Kinorhyncha. Integrative and Comparative Biology, 42, 619–632.CrossRefPubMedGoogle Scholar
  133. Neves, R. C., Cunda, M. R., Kristensen, R. M., & Wanninger, A. (2010). Expression of synapsin and co-localization with serotonin and Rfamide-like immunoreactivity in the nervous system of the chordoid larva of Symbion pandora (Cycliophora). Invertebrate Biology, 129, 17–26.CrossRefGoogle Scholar
  134. Nickel, M. (2010). Evolutionary emergence of synaptic nervous systems: what can we learn from the non-synaptic, nerveless Porifera? Invertebrate Biology, 129, 1–16.CrossRefGoogle Scholar
  135. Nielsen, C. (1995). Animal evolution. Interrelationships of the living phyla (1st ed.). Oxford: Oxford University Press.Google Scholar
  136. Nielsen, C. (2001). Animal evolution. Interrelationships of the living phyla (2nd ed.). Oxford: Oxford University Press.Google Scholar
  137. Nielsen, C. (2010). After all: Xenoturbella is an acoelomorph! Evolution & Development, 12, 241–243.CrossRefGoogle Scholar
  138. Nielsen, C., Scharff, N., & Eibye-Jacobsen, D. (1995). Cladistic analysis of the animal kingdom. Biological Journal of the Linnean Society, 57, 385–410.CrossRefGoogle Scholar
  139. Paps, J., Baguñà, J., & Riutort, M. (2009a). Lophotrochozoa internal phylogeny: new insights from an up-to-date analysis of nuclear ribosomal genes. Proceedings of the Royal Society, Series B, 276, 1245–1254.Google Scholar
  140. Paps, J., Baguñà, J., & Riutort, M. (2009b). Bilaterian phylogeny: a broad sampling of 13 nuclear genes provides a new Lophotrochozoa phylogeny and supports a paraphyletic basal Acoelomorpha. Molecular Biology and Evolution, 26, 2397–2406.PubMedCrossRefGoogle Scholar
  141. Pardos, F. (1988). Fine structure and function of pharynx cilia in Glossobalanus minutus Kowalewsky (Enteropneusta). Acta Zoologica, 69, 1–12.CrossRefGoogle Scholar
  142. Park, J.-K., Rho, H. S., Kristensen, R. M., Kim, W., & Giribet, G. (2006). First molecular data on the phylum Loricifera—an investigation into the phylogeny of Ecdysozoa with emphasis on the positions of Loricifera and Priapulida. Zoological Science, 23, 943–954.PubMedCrossRefGoogle Scholar
  143. Passamaneck, Y. J., Furchheim, N., Hejnol, A., Martindale, M. Q., & Lüter, C. (2011). Ciliary photoreceptors in the cerebral eyes of a protostome larva. EvoDevo, 2: 6.Google Scholar
  144. Pedersen, K. J., & Pedersen, L. R. (1986). Fine structural observations on the extracellular matrix (ECM) of Xenoturbella bocki Westblad, 1949. Acta Zoologica, 67, 103–113.CrossRefGoogle Scholar
  145. Pedersen, K. J., & Pedersen, L. R. (1988). Ultrastructural observations on the epidermis of Xenoturbella bocki Westblad, 1949, with a discusion of epidermal cytoplasmic filament systems of invertebrates. Acta Zoologica, 69, 231–246.CrossRefGoogle Scholar
  146. Peel, J. S. (2010). A corset-like fossil from the Cambrian Sirius Passet Lagerstätte of North Greenland and its implications for cycloneuralian evolution. Journal of Paleontology, 84, 332–340.CrossRefGoogle Scholar
  147. Perseke, M., Hankeln, T., Weich, B., Fritzsch, G., Stadler, P. F., Israelsson, O., et al. (2007). The mitochondrial DNA of Xenoturbella bocki: genomic architecture and phylogenetic analysis. Theory in Biosciences, 126, 35–42.PubMedCrossRefGoogle Scholar
  148. Peterson, K. J., & Eernisse, D. J. (2001). Animal phylogeny and the ancestry of bilaterians: inference from morphology and 18S rDNA gene sequences. Evolution & Development, 3, 170–205.CrossRefGoogle Scholar
  149. Peterson, K. J., Cotton, J. A., Gehling, J. G., & Pisani, D. (2008). The Ediacaran emergence of bilaterians: congruence between the genetic and the geological fossil records. Philosophical Transactions of the Royal Society / Biological Sciences, 1496, 1435–1444.CrossRefGoogle Scholar
  150. Petrov, N. B., & Vladychenskaya, N. S. (2005). Phylogeny of molting protostomes (Ecdysozoa) as inferred from 18S and 28S rRNA gene sequences. Molecular Biology, 39, 503–513.CrossRefGoogle Scholar
  151. Philip, G. K., Creevey, C. J., & McInerney, J. O. (2005). The Opisthokonta and the Ecdysozoa may not be clades: stronger support for the grouping of plant and animal than for animal and fungi and stronger support for the Coelomata than Ecdysozoa. Molecular Biology and Evolution, 22, 1175–1184.PubMedCrossRefGoogle Scholar
  152. Philippe, H., Snell, E. A., Bapteste, E., Lopez, P., Holland, P. W. H., & Casane, D. (2004). Phylogenomics of eukaryotes: impact of missing data on large alignments. Molecular Biology and Evolution, 21, 1740–1752.PubMedCrossRefGoogle Scholar
  153. Philippe, H., Lartillot, N., & Brinkmann, H. (2005). Multigene analyses of bilaterian animals corroborate the monophyly of Ecdysozoa, Lophotrochozoa, and Protostomia. Molecular Biology and Evolution, 22, 1246–1253.PubMedCrossRefGoogle Scholar
  154. Philippe, H., Brinkmann, H., Martinez, P., Riutort, M., & Baguñà, J. (2007). Acoel flatworms are not Platyhelminthes: evidence from phylogenomics. PloS ONE, 8, e717.CrossRefGoogle Scholar
  155. Philippe, H., Derelle, R., Lopez, P., Pick, K., Borchianelli, C., Boury-Esnault, N., et al. (2009). Phylogenomics revives traditional views on deep animal relationships. Current Biology, 19, 706–712.PubMedCrossRefGoogle Scholar
  156. Philippe, H., Brinkmann, H., Copley, R. R., Moroz, L. L., Nakano, H., Poustka, A. J., et al. (2011). Acoelomorph flatworms are deuterostomes related to Xenoturbella. Nature, 470, 255–258.PubMedCrossRefGoogle Scholar
  157. Pick, K. S., Philippe, H., Schreiber, F., Erpenbeck, D., Jackson, D. J., Wrede, P., et al. (2010). Improved phylogenomic taxon sampling noticeably affects non-bilaterian relationships. Molecular Biology and Evolution, 27, 1983–1987.PubMedCrossRefGoogle Scholar
  158. Pilato, G., Binda, M. G., Biondi, O., D’Urso, V., Lisi, O., Marletta, A., et al. (2005). The clade Ecdysozoa, perplexities and questions. Zoologischer Anzeiger, 244, 43–50.CrossRefGoogle Scholar
  159. Podar, M., Haddock, S. H. D., Sogin, M. L., & Harbison, G. R. (2001). A molecular phylogenetic framework for the phylum Ctenophora using 18S rRNA genes. Molecular Phylogenetics and Evolution, 21, 218–230.PubMedCrossRefGoogle Scholar
  160. Prendini, L. (2001). Species or supraspecific taxa as terminals in cladistic analysis? Groundplans versus exemplars revisited. Systematic Biology, 50, 290–300.PubMedCrossRefGoogle Scholar
  161. Raff, R. A., Field, K. G., Olsen, G. J., Giovannoni, S. J., Lane, D. J., Ghiselin, M. T., et al. (1989). Metazoan phylogeny based on analysis of 18S ribosomal RNA. In B. Fernholm, K. Bremer, & H. Jörnvall (Eds.), The hierarchy of life (pp. 247–260). Amsterdam: Elsevier Science BV.Google Scholar
  162. Raikova, O. I., Reuter, M., Jondelius, U., & Gustafsson, M. K. S. (2000). An immunocytochemical and ultrastructural study of the nervous and muscular systems of Xenoturbella westbladi (Bilateria inc. sed.). Zoomorphology, 120, 107–118.CrossRefGoogle Scholar
  163. Raikova, O. I., Reuter, M., Gustafsson, M. K. S., Maule, A. G., Halton, D. W., & Jondelius, U. (2004a). Basiepidermal nervous system in Nemertoderma westbladi (Nemertodermatida): GYIRFamide immunoreactivity. Zoology (Jena), 107, 75–86.Google Scholar
  164. Raikova, O. I., Reuter, M., Gustafsson, M. K. S., Maule, A. G., Halton, D. W., & Jondelius, U. (2004b). Evolution of the nervous system in Paraphanostoma (Acoela). Zoologica Scripta, 33, 71–88.CrossRefGoogle Scholar
  165. Rieger, R. M. (1980). A new group of interstitial worms, Lobatocerebridae nov. fam. (Annelida) and its significance for metazoan phylogeny. Zoomorphology, 95, 41–84.CrossRefGoogle Scholar
  166. Rieger, R. M. (1991). Jennaria pulchra, nov.gen. nov.spec., eine den psammobionten Anneliden nahestehende Gattung aus dem Küstengrundwasser von North Carolina. Berichte des Naturwissenschaftlich-Medizinischen Vereins in Innsbruck, 78, 203–215.Google Scholar
  167. Roeding, F., Hagner-Holler, S., Ruhberg, H., Ebersberger, I., Haeseler, A., Kube, M., et al. (2007). EST sequencing of Onychophora and phylogenomic analysis of Metazoa. Molecular Biology and Evolution, 45, 942–951.Google Scholar
  168. Roeding, F., Borner, J., Kube, M., Klages, M., Reinhardt, R., & Burmester, T. (2009). A 454 sequencing approach for large scale phylogenomic analysis of the common emperor scorpion (Pandinus imperator). Molecular Phylogenetics and Evolution, 53, 826–834.PubMedCrossRefGoogle Scholar
  169. Rogozin, I. B., Wolf, Y. I., Carmel, L., & Koonin, E. V. (2007). Ecdysozoan clade rejected by genome-wide analysis of rare amino acid replacements. Molecular Biology and Evolution, 24, 1080–1090.PubMedCrossRefGoogle Scholar
  170. Rokas, A., Krüger, D., & Carroll, S. B. (2005). Animal evolution and the molecular signature of radiations compressed in time. Science, 310, 1933–1938.PubMedCrossRefGoogle Scholar
  171. de Rosa, R., Grenier, J. K., Andreeva, T., Cook, C. E., Adoutte, A., Akam, M., et al. (1999). Hox genes in brachiopods and priapulids and protostome evolution. Nature, 399, 772–776.PubMedCrossRefGoogle Scholar
  172. Rota-Stabelli, O., Campbell, L., Brinkmann, H., Edgecombe, G. D., Longhorn, S. J., Peterson, K. J., et al. (2010a). A congruent solution to arthropod phylogeny: phylogenomics, microRNAs and morphology support monophyletic Mandibulata. Proceedings of the Royal Society B: Biological Sciences, 278, 298–306.Google Scholar
  173. Rota-Stabelli, O., Kayal, E., Gleeson, D., Daub, J., Boore, J. L., Telford, M. J., et al. (2010b). Ecdysozoan mitogenomics: evidence for a common origin of the legged invertebrates, the Panarthropoda. Genome Biology and Evolution, 2, 425–440.CrossRefGoogle Scholar
  174. Rothe, B. H., & Schmidt-Rhaesa, A. (2009). Architecture of the nervous system in two Dactylopoda species (Gastrotricha, Macrodasyida). Zoomorphology, 128, 227–246.CrossRefGoogle Scholar
  175. Roule, L. (1891). Considerations sur l’embranchement des Trochozoaires. Annales des Sciences Naturelles (Zoologie), 7me Série, 11, 121–178.Google Scholar
  176. Rouse, G. W. (1999). Trochophore concepts: ciliary bands and the evolution of larvae in spiralian Metazoa. Biological Journal of the Linnean Society, 66, 411–464.CrossRefGoogle Scholar
  177. Rouse, G. W., & Pleijel, F. (2007). Annelida. Zootaxa, 1668, 245–264.Google Scholar
  178. Ruiz-Trillo, I., Riutort, M., Littlewood, D. T. J., Herniou, E. A., & Baguñà, J. (1999). Acoel flatworms: earliest extant bilaterian metazoans, not members of Platyhelminthes. Science, 283, 1919–1923.PubMedCrossRefGoogle Scholar
  179. Ruiz-Trillo, I., Paps, J., Loukota, M., Ribera, C., Jondelius, U., Baguñà, J., et al. (2002). A phylogenetic analysis of myosin heavy chain type II sequences corroborates that Acoela and Nemertodermatida are basal bilaterians. Proceedings of the National Academy of Sciences of the USA, 99, 11246–11251.PubMedCrossRefGoogle Scholar
  180. Ruppert, E. E. (1991). Gastrotricha. In F. W. Harrison & E. E. Ruppert (Eds.), Microscopic anatomy of invertebrates, volume 4: Aschelminthes (pp. 41–109). New York: Wiley-Liss Inc.Google Scholar
  181. Ryan, J. F., Pang, K., NISC Comparative Sequencing Program, Mullikin, J. C., Martindale, M. Q., & Baxevanis, A. D. (2010). The homeodomain complement of the ctenophore Mnemiopsis leidyi suggests that Ctenophora and Porifera diverged prior to the ParaHoxozoa. EvoDevo, 1/9.Google Scholar
  182. Sanderson, M. J. (2002). Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Molecular Biology and Evolution, 19, 101–109.PubMedGoogle Scholar
  183. Sanderson, M. J. (2003). r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics, 19, 301–302.PubMedCrossRefGoogle Scholar
  184. Sanderson, M. J. (2008). Phylogenetic signal in the eukaryotic tree of life. Science, 321, 121–123.PubMedCrossRefGoogle Scholar
  185. Schierwater, B., Eitel, M., Jakob, W., Osigus, H.-J., Hadrys, H., Dellaporta, S. L., et al. (2009). Concatenated analysis sheds light on early metazoan evolution and fuels a modern “Urmetazoan” hypothesis. PLoS Biology, 7, 36–44.CrossRefGoogle Scholar
  186. Schleip, W. (1929). Die Determination der Primitiventwicklung. Leipzig: Akademische Verlagsgesellschaft.Google Scholar
  187. Schmidt-Rhaesa, A. (2004). Ecdysozoa versus Articulata. Sitzungsberichte der Gesellschaft Naturforschender Freunde zu Berlin, 43, 35–49.Google Scholar
  188. Schmidt-Rhaesa, A. (2006). Perplexities concerning the Ecdysozoa: a reply to Pilato et al. Zoologischer Anzeiger, 244, 205–208.CrossRefGoogle Scholar
  189. Schmidt-Rhaesa, A. (2007). The evolution of organ systems. Oxford: Oxford University Press.CrossRefGoogle Scholar
  190. Schmidt-Rhaesa, A., Bartolomaeus, T., Lemburg, C., Ehlers, U., & Garey, J. R. (1998). The position of the Arthropoda in the phylogenetic system. Journal of Morphology, 238, 263–285.CrossRefGoogle Scholar
  191. Scholtz, G. (2002). The Articulata hypothesis—or what is a segment? Organisms Diversity and Evolution, 2, 197–215.CrossRefGoogle Scholar
  192. Scholtz, G. (2003). Is the taxon Articulata obsolete? Arguments in favour of a close relationship between annelids and arthropods. In A. Legakis, S. Sfenthourakis, R. Polymeni, & M. Thessalou-Legaki (Eds.), The new panorama of animal evolution. Proceedings of the 18th International Congress of Zoology (pp. 489–501). Sofia: Pensoft.Google Scholar
  193. Schram, F. R. (1991). Cladistic analysis of metazoan phyla and the placement of fossil problematica. In A. M. Simonetta & S. Conway-Morris (Eds.), The early evolution of Metazoa and the significance of problematic taxa (pp. 35–46). Cambridge: Cambridge University Press.Google Scholar
  194. Schram, F. R., & Ellis, W. N. (1994). Metazoan relationships: a rebuttal. Cladistics, 10, 331–337.CrossRefGoogle Scholar
  195. Seaver, E. C. (2003). Segmentation: mono- or polyphyletic? International Journal of Developmental Biology, 47, 583–595.PubMedGoogle Scholar
  196. Sempere, L. F., Cole, C. N., McPeek, M. A., & Peterson, K. J. (2006). The phylogenetic distribution of metazoan microRNAs: insights into evolutionary complexity and constraint. Journal of Experimental Zoology, Part B: Molecular and Developmental Evolution, 306, 575–588.CrossRefGoogle Scholar
  197. Sempere, L. F., Martinez, P., Cole, C., Baguñà, J., & Peterson, K. J. (2007). Phylogenetic distribution of microRNAs supports the basal position of acoel flatworms and the polyphyly of Platyhelminthes. Evolution & Development, 9, 409–415.CrossRefGoogle Scholar
  198. Shu, D. G., Conway Morris, S., Han, J., Chen, L., Zhang, X. L., Zhang, Z. F., et al. (2001). Primitive deuterostomes from the Chengjiang Lagerstätte (Lower Cambrian, China). Nature, 414, 419–424.PubMedCrossRefGoogle Scholar
  199. Shu, D. G., Conway Morris, S., Zhang, Z. F., Liu, J. N., Han, J., Chen, L., et al. (2003). A new species of yunnanozoan with implications for deuterostome evolution. Science, 299, 1380–1384.PubMedCrossRefGoogle Scholar
  200. Shu, D.-G., Conway Morris, S., Han, J., Zhang, Z.-F., & Liu, J.-N. (2004). Ancestral echinoderms from the Chengjiang deposits of China. Nature, 430, 422–428.PubMedCrossRefGoogle Scholar
  201. Shu, D.-G., Conway Morris, S., Zhang, Z.-F., & Han, J. (2010). The earliest history of the deuterostomes: the importance of the Chengjiang Fossil-Lagerstätte. Proceedings of the Royal Society, Series B, 277, 165–174.CrossRefGoogle Scholar
  202. Siddall, M. E. (2009). Unringing the bell: metazoan phylogenomics and the partition bootstrap. Cladistics, 25, 1–9.CrossRefGoogle Scholar
  203. Slyusarev, G. S., & Kristensen, R. M. (2003). Fine structure of the ciliated cells and ciliary rootlets of Intoshia variabili (Orthonectida). Zoomorphology, 122, 33–39.Google Scholar
  204. Smith, A. B. (2005). The pre-radial history of echinoderms. Geological Journal, 40, 255–280.CrossRefGoogle Scholar
  205. Smith, A. B., & Swalla, B. J. (2009). Deciphering deuterostome phylogeny: molecular, morphological, and palaeontological perspectives. In M. J. Telford & D. T. J. Littlewood (Eds.), Animal evolution: Genomes, fossils and trees (pp. 80–92). Oxford: Oxford University Press.Google Scholar
  206. Sørensen, M. V. (2003). Further structures in the jaw apparatus of Limnognathia maerski (Micrognathozoa), with notes on the phylogeny of the Gnathifera. Journal of Morphology, 255, 131–145.PubMedCrossRefGoogle Scholar
  207. Sørensen, M. V., Funch, P., Willerslev, E., Hansen, A. J., & Olesen, J. (2000). On the phylogeny of the Metazoa in light of Cycliophora and Micrognathozoa. Zoologischer Anzeiger, 239, 297–318.Google Scholar
  208. Sørensen, M. V., Hebsgaard, M. B., Heiner, I., Glenner, H., Willerslev, E., & Kristensen, R. M. (2008). New data from an enigmatic phylum: evidence from molecular sequence data supports a sister group relationship between Loricifera and Nematomorpha. Journal of Zoological Systematics and Evolutionary Research, 46, 231–239.CrossRefGoogle Scholar
  209. Sperling, E. A., Peterson, K. J., & Pisani, D. (2009). Phylogenetic signal-dissection of nuclear housekeeping genes supports the paraphyly of sponges and the monophyly of Eumetazoa. Molecular Biology and Evolution, 26, 2261–2274.PubMedCrossRefGoogle Scholar
  210. Sperling, E. A., Vinther, J., Moy, V. N., Wheeler, B. M., Sémon, M., & Briggs, D. E. G. (2009). MicroRNAs resolve an apparent conflict between annelid systematics and their fossil record. Proceedings of the Royal Society B / Biological Sciences, 276, 4315–4322.CrossRefGoogle Scholar
  211. Sperling, E. A., Robinson, J. M., Pisani, D., & Peterson, K. J. (2010). Where’s the glass? Biomarkers, molecular clocks and microRNAs suggest a 200-Myr missing Precambrian fossil record of siliceous sponge spicules. Geobiology, 8, 24–36.PubMedCrossRefGoogle Scholar
  212. Srivastava, M., Begovic, E., Chapman, J., Putnam, N. H., Hellsten, U., Kawashima, T., et al. (2008). The Trichoplax genome and the nature of placozoans. Nature, 454, 955–960.PubMedCrossRefGoogle Scholar
  213. Srivastava, M., Simakov, O., Chapman, J., Fahey, B., Gauthier, M. E., et al. (2010). The Amphimedon queenslandica genome and the evolution of animal complexity. Nature, 466, 720–726.PubMedCrossRefGoogle Scholar
  214. Struck, T. H., & Fisse, F. (2008). Phylogenetic position of Nemertea derived from phylogenomic data. Molecular Biology and Evolution, 25, 728–736.PubMedCrossRefGoogle Scholar
  215. 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, 11.CrossRefGoogle Scholar
  216. Telford, M. J. (2006). Animal phylogeny. Current Biology, 16, R981–R985.PubMedCrossRefGoogle Scholar
  217. Telford, M. J., Bourlat, S. J., Economou, A., Papillon, D., & Rota-Stabelli, O. (2008). The evolution of the Ecdysozoa. Philosophical Transactions of the Royal Society, Series B, 363, 1529–1537.CrossRefGoogle Scholar
  218. Todaro, M. A., Telford, M. J., Lockyer, A. E., & Littlewood, D. T. (2006). Interrelationships of the Gastrotricha and their place among the Metazoa inferred from 18S rRNA genes. Zoologica Scripta, 35, 251–259.CrossRefGoogle Scholar
  219. Townsend, J. P. (2007). Profiling phylogenetic informativeness. Systematic Biology, 56, 222–231.PubMedCrossRefGoogle Scholar
  220. Valentine, J. W. (2004). On the origin of phyla. Chicago: The University of Chicago Press.Google Scholar
  221. Voigt, O., Collins, A. G., Porello, S., Pearse, V. B., & Schierwater, B. (2004). Placozoa—no longer a phylum of one. Current Biology, 14, R944–R945.PubMedCrossRefGoogle Scholar
  222. Wallace, R. L., Ricci, C., & Melone, G. (1996). A cladistic analysis of pseudocoelomate (aschelminth) morphology. Invertebrate Biology, 115, 104–112.CrossRefGoogle Scholar
  223. Wallberg, A. (2009). The dawn of a new age. Interrelationships of Acoela and Nemertodermatida and the early evolution of Bilateria. Doctoral thesis. Uppsala: Uppsala University.Google Scholar
  224. Wallberg, A., Curini-Galletti, M., Ahmadzadeh, A., & Jondelius, U. (2007). Dismissal of Acoelomorpha: Acoela and Nemertodermatida are separate early bilaterian clades. Zoologica Scripta, 36, 509–523.CrossRefGoogle Scholar
  225. Wanninger, A. (2008). Comparative lophotrochozoan neurogenesis and larval neuroanatomy: recent advances from previously neglected taxa. Acta Biologica Hungarica, 59(Supplement), 127–136.PubMedCrossRefGoogle Scholar
  226. Webster, B. L., Copley, R. R., Jenner, R. A., Mackenzie-Dodds, J. A., Bourlat, S. J., Rota-Stabelli, O., et al. (2006). Mitogenomics and phylogenomics reveal priapulid worms as extant models for the ancestral Ecdysozoan. Evolution & Development, 8, 502–510.CrossRefGoogle Scholar
  227. Webster, B. L., Mackenzie-Dodds, J. A., Telford, M. J., & Littlewood, D. T. J. (2007). The mitochondrial genome of Priapulus caudatus Lamarck (Priapulida: Priapulidae). Gene, 389, 96–105.PubMedCrossRefGoogle Scholar
  228. Westblad, E. (1949). Xenoturbella bocki n. g., n. sp., a peculiar, primitive turbellarian type. Arkiv för Zoologi, 1, 3–29.Google Scholar
  229. Wheeler, B. M., Heimberg, A. M., Moy, V. N., Sperling, E. A., Holstein, T. W., Heber, S., et al. (2009). The deep evolution of metazoan microRNAs. Evolution & Development, 11, 50–68.CrossRefGoogle Scholar
  230. Winchell, C. J., Sullivan, J., Cameron, C. B., Swalla, B. J., & Mallatt, J. (2002). Evaluating hypotheses of deuterostome phylogeny and chordate evolution with new LSU and SSU ribosomal DNA data. Molecular Biology and Evolution, 19, 762–776.PubMedGoogle Scholar
  231. Winnepenninckx, B., Backeljau, T., & De Wachter, R. (1995a). Phylogeny of protostome worms derived from 18S rRNA sequences. Molecular Biology and Evolution, 12, 641–649.Google Scholar
  232. Winnepenninckx, B., Backeljau, T., Mackey, L. Y., Brooks, J. M., De Wachter, R., Kumar, S., et al. (1995b). 18S rRNA data indicate that Aschelminthes are polyphyletic in orgin and consist of at least three distinct clades. Molecular Biology and Evolution, 12, 1132–1137.Google Scholar
  233. Witek, A., Herlyn, H., Ebersberger, I., Welch, D. B. M., & Hankeln, T. (2009). Support for the monophyletic origin of Gnathifera from phylogenomics. Molecular Phylogenetics and Evolution, 53, 1037–1041.PubMedCrossRefGoogle Scholar
  234. Wolf, Y. I., Rogozin, I. B., & Koonin, E. V. (2004). Coelomata and not Ecdysozoa: evidence from genome-wide phylogenetic analysis. Genome Research, 14, 29–36.PubMedCrossRefGoogle Scholar
  235. Worsaae, K., & Rouse, G. W. (2008). Is Diurodrilus an annelid? Journal of Morphology, 269, 1426–1455.PubMedCrossRefGoogle Scholar
  236. Xiao, S., & Laflamme, M. (2009). On the eve of animal radiation: phylogeny, ecology and evolution of the Ediacaran biota. Trends in Ecology and Evolution, 24, 31–40.PubMedCrossRefGoogle Scholar
  237. Zrzavý, J. (2001). Ecdysozoa versus Articulata: clades, artifacts, prejudices. Journal of Zoological Systematics and Evolutionary Research, 39, 159–163.CrossRefGoogle Scholar
  238. Zrzavý, J. (2003). Gastrotricha and metazoan phylogeny. Zoologica Scripta, 32, 61–81.CrossRefGoogle Scholar
  239. Zrzavý, J., Mihulka, S., Kepka, P., Bezdek, A., & Tietz, D. (1998). Phylogeny of the Metazoa based on morphological and 18S ribosomal DNA evidence. Cladistics, 14, 249–285.Google Scholar
  240. Zrzavý, J., Hypša, V., & Tietz, D. F. (2001). Myzostomida are not annelids: molecular and morphological support for a clade of animals with anterior sperm flagella. Cladistics, 17, 170–198.Google Scholar

Copyright information

© Gesellschaft für Biologische Systematik 2011

Authors and Affiliations

  • Gregory D. Edgecombe
    • 1
    Email author
  • Gonzalo Giribet
    • 2
  • Casey W. Dunn
    • 3
  • Andreas Hejnol
    • 4
  • Reinhardt M. Kristensen
    • 5
  • Ricardo C. Neves
    • 4
  • Greg W. Rouse
    • 6
  • Katrine Worsaae
    • 7
  • Martin V. Sørensen
    • 5
  1. 1.Department of PalaeontologyThe Natural History MuseumLondonUK
  2. 2.Museum of Comparative Zoology, Department of Organismic and Evolutionary BiologyHarvard UniversityCambridgeUSA
  3. 3.Department of Ecology and Evolutionary BiologyBrown UniversityProvidenceUSA
  4. 4.Sars International Centre for Marine Molecular BiologyUniversity of BergenBergenNorway
  5. 5.Natural History Museum of DenmarkUniversity of CopenhagenCopenhagenDenmark
  6. 6.Scripps Institution of OceanographyLa JollaUSA
  7. 7.Marine Biological SectionUniversity of CopenhagenHelsingørDenmark

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