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Higher-level metazoan relationships: recent progress and remaining questions

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Abstract

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.

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References

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Ahlrichs, W. H. (1995). Seison annulatus und Seison nebaliae—Ultrastruktur und Phylogenie. Verhandlungen der Deutschen Zoologischen Gesellschaft, 88, 155.

    Google Scholar 

  • 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.

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Ax, P. (1996). Multicellular animals. A new approach to the phylogenetic order in nature. Volume I. Berlin: Springer.

    Google Scholar 

  • Ax, P. (2001). Das System der Metazoa III. Ein Lehrbuch der phylogenetischen Systematik. Stuttgart: Spektrum Akademischer Verlag.

    Google Scholar 

  • Backeljau, T., Winnepenninckx, B., & De Bruyn, L. (1993). Cladistic analysis of metazoan relationships: a reappraisal. Cladistics, 9, 167–181.

    Article  Google Scholar 

  • 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 

  • Balavoine, G., de Rosa, R., & Adoutte, A. (2002). Hox clusters and bilaterian phylogeny. Molecular Phylogenetics and Evolution, 24, 266–373.

    Article  CAS  Google Scholar 

  • de Beauchamp, P. (1965). Classe des Rotifères. In P. P. Grassé (Ed.), Traité de Zoologie IV, 3 (pp. 1225–1379). Paris: Masson.

    Google Scholar 

  • 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 

  • 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 

  • Blair, J. E., Ikeo, K., Gojobori, T., & Hedges, S. B. (2002). The evolutionary position of nematodes. BMC Evolutionary Biology, 2, 1–7.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Brown, F. D., Prendergast, A., & Swalla, B. J. (2008). Man is but a worm: chordate origins. Genesis, 46, 605–613.

    Article  PubMed  Google Scholar 

  • Budd, G. E. (2001). Tardigrades as ‘stem-group arthropods’: the evidence from the Cambrian fauna. Zoologischer Anzeiger, 240, 265–279.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Cavalier Smith, T. (1998). A revised six-kingdom system of life. Biological Reviews, 73, 203–266.

    Article  PubMed  CAS  Google Scholar 

  • Conway Morris, S. (2000). The Cambrian “explosion”: slow-fuse or megatonnage? Proceedings of the National Academy of Sciences of the USA, 97, 4426–4429.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Delsuc, F., Brinkmann, H., & Philippe, H. (2005). Phylogenomics and the reconstruction of the tree of life. Nature Reviews / Genetics, 6, 361–375.

    Article  CAS  Google Scholar 

  • Delsuc, F., Brinkmann, H., Chourrout, D., & Philippe, H. (2006). Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature, 439, 965–668.

    Article  PubMed  CAS  Google Scholar 

  • Delsuc, F., Tsagkogeorga, G., Lartillot, N., & Philippe, H. (2008). Additional molecular support for the new chordate phylogeny. Genesis, 46, 592–604.

    Article  PubMed  Google Scholar 

  • 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 

  • Dong, X. (2007). Developmental sequence of Cambrian embryo Markuelia. Chinese Science Bulletin, 52, 929–935.

    Article  Google Scholar 

  • Dopazo, H., & Dopazo, J. (2005). Genome-scale evidence of the nematode-arthropod clade. Genome Biology, 6, R41.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Farris, J. S. (1970). Methods for computing Wagner trees. Systematic Zoology, 19, 83–92.

    Article  Google Scholar 

  • Farris, J. S., Kluge, A. G., & Eckhardt, M. J. (1970). A numerical approach to phylogenetic systematics. Systematic Zoology, 19, 172–189.

    Article  Google Scholar 

  • Felsenstein, J. (1973). Maximum-likelihood estimation of evolutionary trees from continuous characters. American Journal of Human Genetics, 25, 471–492.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Franzén, Å., & Afzelius, B. A. (1987). The ciliated epidermis of Xenoturbella bocki (Platyhelminthes, Xenoturbellida) with some phylogenetic considerations. Zoologica Scripta, 16, 9–17.

    Article  Google Scholar 

  • Funch, P. (1996). The chordoid larva of Symbion pandora (Cycliophora) is a modified trochophore. Journal of Morphology, 230, 231–263.

    Article  Google Scholar 

  • Funch, P., & Kristensen, R. M. (1995). Cycliophora is a new phylum with affinities to Entoprocta and Ectoprocta. Nature, 378, 711–714.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Ghiselin, M. T. (1988). The origin of molluscs in the light of molecular evidence. Oxford Surveys in Evolutionary Biology, 5, 66–95.

    Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Giribet, G. (2003). Molecules, development and fossils in the study of metazoan evolution; Articulata versus Ecdysozoa revisited. Zoology, 106, 303–326.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Giribet, G. (2008). Assembling the lophotrochozoan (=spiralian) tree of life. Philosophical Transactions of the Royal Society, Series B, 363, 1513–1522.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Haase, A., Stern, M., Wächtler, K., & Bicker, G. (2001). A tissue-specific marker of Ecdysozoa. Development Genes and Evolution, 211, 428–433.

    Article  PubMed  CAS  Google Scholar 

  • Haeckel, E. (1866). Generelle Morphologie der Organismen. Berlin: Georg Reimer.

    Google Scholar 

  • Halanych, K. M. (2004). The new view of animal phylogeny. Annual Reviews of Ecology, Evolution and Systematics, 35, 229–256.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Harvey, T. H. P., Dong, X., & Donoghue, P. C. J. (2010). Are palaeoscolecids ancestral ecdysozoans? Evolution & Development, 12, 177–200.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • Haszprunar, G. (2000). Is the Aplacophora monophyletic? A cladistic point of view. American Malacological Bulletin, 15, 115–130.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Helmkampf, M., Bruchhaus, I., & Hausdorf, B. (2008a). Multigene analysis of lophophorate and chaetognath phylogenetic relationships. Molecular Phylogenetics and Evolution, 46, 206–214.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Hennig, W. (1950). Grundzüge einer Theorie der phylogenetischen Systematik. Berlin: Deutscher Zentralverlag.

    Google Scholar 

  • Hennig, W. (1965). Phylogenetic systematics. Annual Review of Entomology, 10, 97–166.

    Article  Google Scholar 

  • Hennig, W. (1966). Phylogenetic systematics. Urbana: University of Illinois Press.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Jenner, R. A. (2001). Bilaterian phylogeny and uncritical recycling of morphological data sets. Systematic Biology, 50, 730–742.

    Article  PubMed  CAS  Google Scholar 

  • Jenner, R. A. (2004a). The scientific status of metazoan cladistics: why current research practice must change. Zoologica Scripta, 33, 293–310.

    Article  Google Scholar 

  • 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 

  • 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.

  • Jensen, S., Droser, M. L., & Gehling, J. G. (2005). Trace fossil preservation and the early evolution of animals. Palaeogeography, Palaeoclimatology, Palaeoecology, 220, 19–29.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Kapp, H. (2000). The unique embryology of Chaetognatha. Zoologischer Anzeiger, 239, 263–266.

    Google Scholar 

  • Kaul, S., & Stach, T. (2010). Ontogeny of the collar cord: neurulation in the hemichordate Saccoglossus kowalevskii. Journal of Morphology, 271, 1240–1259.

    Article  PubMed  Google Scholar 

  • Kluge, A. G., & Farris, J. S. (1969). Quantitative phyletics and the evolution of anurans. Systematic Zoology, 18, 1–32.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Lake, J. A. (1990). Origin of the metazoa. Proceedings of the National Academy of Sciences of the USA, 87, 763–766.

    Article  PubMed  CAS  Google Scholar 

  • Lartillot, N., & Philippe, H. (2008). Improvement of molecular phylogenetic inference and phylogeny of Bilateria. Proceedings of the Royal Society, Series B, 363, 1463–1472.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Lundin, K. (2001). Degenerating epidermal cells in Xenoturbella bocki (phylum uncertain), Nemertodermatida and Acoela (Platyhelminthes). Belgian Journal of Zoology, 131, 153–157.

    Google Scholar 

  • Lüter, C. (2000). Ultrastructure of larval and adult setae of Brachiopoda. Zoologischer Anzeiger, 239, 75–90.

    Google Scholar 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • Mallatt, J., & Chen, J.-Y. (2003). Fossil sister group of craniates: predicted and found. Journal of Morphology, 258, 1–31.

    Article  PubMed  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Neuhaus, B., & Higgins, R. P. (2002). Ultrastructure, biology, and phylogenetic relationships of Kinorhyncha. Integrative and Comparative Biology, 42, 619–632.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Nickel, M. (2010). Evolutionary emergence of synaptic nervous systems: what can we learn from the non-synaptic, nerveless Porifera? Invertebrate Biology, 129, 1–16.

    Article  Google Scholar 

  • Nielsen, C. (1995). Animal evolution. Interrelationships of the living phyla (1st ed.). Oxford: Oxford University Press.

    Google Scholar 

  • Nielsen, C. (2001). Animal evolution. Interrelationships of the living phyla (2nd ed.). Oxford: Oxford University Press.

    Google Scholar 

  • Nielsen, C. (2010). After all: Xenoturbella is an acoelomorph! Evolution & Development, 12, 241–243.

    Article  Google Scholar 

  • Nielsen, C., Scharff, N., & Eibye-Jacobsen, D. (1995). Cladistic analysis of the animal kingdom. Biological Journal of the Linnean Society, 57, 385–410.

    Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Pardos, F. (1988). Fine structure and function of pharynx cilia in Glossobalanus minutus Kowalewsky (Enteropneusta). Acta Zoologica, 69, 1–12.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Philippe, H., Brinkmann, H., Martinez, P., Riutort, M., & Baguñà, J. (2007). Acoel flatworms are not Platyhelminthes: evidence from phylogenomics. PloS ONE, 8, e717.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Prendini, L. (2001). Species or supraspecific taxa as terminals in cladistic analysis? Groundplans versus exemplars revisited. Systematic Biology, 50, 290–300.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Rokas, A., Krüger, D., & Carroll, S. B. (2005). Animal evolution and the molecular signature of radiations compressed in time. Science, 310, 1933–1938.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

  • 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.

    Article  Google Scholar 

  • Rothe, B. H., & Schmidt-Rhaesa, A. (2009). Architecture of the nervous system in two Dactylopoda species (Gastrotricha, Macrodasyida). Zoomorphology, 128, 227–246.

    Article  Google Scholar 

  • Roule, L. (1891). Considerations sur l’embranchement des Trochozoaires. Annales des Sciences Naturelles (Zoologie), 7me Série, 11, 121–178.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Rouse, G. W., & Pleijel, F. (2007). Annelida. Zootaxa, 1668, 245–264.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

  • Sanderson, M. J. (2002). Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Molecular Biology and Evolution, 19, 101–109.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Sanderson, M. J. (2008). Phylogenetic signal in the eukaryotic tree of life. Science, 321, 121–123.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Schleip, W. (1929). Die Determination der Primitiventwicklung. Leipzig: Akademische Verlagsgesellschaft.

    Google Scholar 

  • Schmidt-Rhaesa, A. (2004). Ecdysozoa versus Articulata. Sitzungsberichte der Gesellschaft Naturforschender Freunde zu Berlin, 43, 35–49.

    Google Scholar 

  • Schmidt-Rhaesa, A. (2006). Perplexities concerning the Ecdysozoa: a reply to Pilato et al. Zoologischer Anzeiger, 244, 205–208.

    Article  Google Scholar 

  • Schmidt-Rhaesa, A. (2007). The evolution of organ systems. Oxford: Oxford University Press.

    Book  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Scholtz, G. (2002). The Articulata hypothesis—or what is a segment? Organisms Diversity and Evolution, 2, 197–215.

    Article  Google Scholar 

  • 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 

  • 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 

  • Schram, F. R., & Ellis, W. N. (1994). Metazoan relationships: a rebuttal. Cladistics, 10, 331–337.

    Article  Google Scholar 

  • Seaver, E. C. (2003). Segmentation: mono- or polyphyletic? International Journal of Developmental Biology, 47, 583–595.

    PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Siddall, M. E. (2009). Unringing the bell: metazoan phylogenomics and the partition bootstrap. Cladistics, 25, 1–9.

    Article  Google Scholar 

  • 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 

  • Smith, A. B. (2005). The pre-radial history of echinoderms. Geological Journal, 40, 255–280.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Struck, T. H., & Fisse, F. (2008). Phylogenetic position of Nemertea derived from phylogenomic data. Molecular Biology and Evolution, 25, 728–736.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Telford, M. J. (2006). Animal phylogeny. Current Biology, 16, R981–R985.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Townsend, J. P. (2007). Profiling phylogenetic informativeness. Systematic Biology, 56, 222–231.

    Article  PubMed  CAS  Google Scholar 

  • Valentine, J. W. (2004). On the origin of phyla. Chicago: The University of Chicago Press.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Wallace, R. L., Ricci, C., & Melone, G. (1996). A cladistic analysis of pseudocoelomate (aschelminth) morphology. Invertebrate Biology, 115, 104–112.

    Article  Google Scholar 

  • 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.

  • 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.

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Westblad, E. (1949). Xenoturbella bocki n. g., n. sp., a peculiar, primitive turbellarian type. Arkiv för Zoologi, 1, 3–29.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Winnepenninckx, B., Backeljau, T., & De Wachter, R. (1995a). Phylogeny of protostome worms derived from 18S rRNA sequences. Molecular Biology and Evolution, 12, 641–649.

    CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Worsaae, K., & Rouse, G. W. (2008). Is Diurodrilus an annelid? Journal of Morphology, 269, 1426–1455.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Zrzavý, J. (2001). Ecdysozoa versus Articulata: clades, artifacts, prejudices. Journal of Zoological Systematics and Evolutionary Research, 39, 159–163.

    Article  Google Scholar 

  • Zrzavý, J. (2003). Gastrotricha and metazoan phylogeny. Zoologica Scripta, 32, 61–81.

    Article  Google Scholar 

  • 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 

  • 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 

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Acknowledgements

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).

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Edgecombe, G.D., Giribet, G., Dunn, C.W. et al. Higher-level metazoan relationships: recent progress and remaining questions. Org Divers Evol 11, 151–172 (2011). https://doi.org/10.1007/s13127-011-0044-4

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