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Platyzoan paraphyly based on phylogenomic data supports a noncoelomate ancestry of spiralia

TH. Struck, AR. Wey-Fabrizius, A. Golombek, L. Hering, A. Weigert, C. Bleidorn, S. Klebow, N. Iakovenko, B. Hausdorf, M. Petersen, P. Kück, H. Herlyn, T. Hankeln,

. 2014 ; 31 (7) : 1833-49.

Language English Country United States

Document type Journal Article, Research Support, Non-U.S. Gov't

Based on molecular data three major clades have been recognized within Bilateria: Deuterostomia, Ecdysozoa, and Spiralia. Within Spiralia, small-sized and simply organized animals such as flatworms, gastrotrichs, and gnathostomulids have recently been grouped together as Platyzoa. However, the representation of putative platyzoans was low in the respective molecular phylogenetic studies, in terms of both, taxon number and sequence data. Furthermore, increased substitution rates in platyzoan taxa raised the possibility that monophyletic Platyzoa represents an artifact due to long-branch attraction. In order to overcome such problems, we employed a phylogenomic approach, thereby substantially increasing 1) the number of sampled species within Platyzoa and 2) species-specific sequence coverage in data sets of up to 82,162 amino acid positions. Using established and new measures (long-branch score), we disentangled phylogenetic signal from misleading effects such as long-branch attraction. In doing so, our phylogenomic analyses did not recover a monophyletic origin of platyzoan taxa that, instead, appeared paraphyletic with respect to the other spiralians. Platyhelminthes and Gastrotricha formed a monophylum, which we name Rouphozoa. To the exclusion of Gnathifera, Rouphozoa and all other spiralians represent a monophyletic group, which we name Platytrochozoa. Platyzoan paraphyly suggests that the last common ancestor of Spiralia was a simple-bodied organism lacking coelomic cavities, segmentation, and complex brain structures, and that more complex animals such as annelids evolved from such a simply organized ancestor. This conclusion contradicts alternative evolutionary scenarios proposing an annelid-like ancestor of Bilateria and Spiralia and several independent events of secondary reduction.

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$a Based on molecular data three major clades have been recognized within Bilateria: Deuterostomia, Ecdysozoa, and Spiralia. Within Spiralia, small-sized and simply organized animals such as flatworms, gastrotrichs, and gnathostomulids have recently been grouped together as Platyzoa. However, the representation of putative platyzoans was low in the respective molecular phylogenetic studies, in terms of both, taxon number and sequence data. Furthermore, increased substitution rates in platyzoan taxa raised the possibility that monophyletic Platyzoa represents an artifact due to long-branch attraction. In order to overcome such problems, we employed a phylogenomic approach, thereby substantially increasing 1) the number of sampled species within Platyzoa and 2) species-specific sequence coverage in data sets of up to 82,162 amino acid positions. Using established and new measures (long-branch score), we disentangled phylogenetic signal from misleading effects such as long-branch attraction. In doing so, our phylogenomic analyses did not recover a monophyletic origin of platyzoan taxa that, instead, appeared paraphyletic with respect to the other spiralians. Platyhelminthes and Gastrotricha formed a monophylum, which we name Rouphozoa. To the exclusion of Gnathifera, Rouphozoa and all other spiralians represent a monophyletic group, which we name Platytrochozoa. Platyzoan paraphyly suggests that the last common ancestor of Spiralia was a simple-bodied organism lacking coelomic cavities, segmentation, and complex brain structures, and that more complex animals such as annelids evolved from such a simply organized ancestor. This conclusion contradicts alternative evolutionary scenarios proposing an annelid-like ancestor of Bilateria and Spiralia and several independent events of secondary reduction.
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$a Golombek, Anja $u Zoological Research Museum Alexander Koenig, Bonn, Germany.
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$a Hering, Lars $u Animal Evolution and Development, Institute of Biology II, University of Leipzig, Leipzig, Germany.
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$a Weigert, Anne $u Molecular Evolution and Systematics of Animals, Institute of Biology, University of Leipzig, Leipzig, Germany.
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$a Bleidorn, Christoph $u Molecular Evolution and Systematics of Animals, Institute of Biology, University of Leipzig, Leipzig, Germany.
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$a Klebow, Sabrina $u Institute of Molecular Genetics, Biosafety Research and Consulting, Johannes Gutenberg University, Mainz, Germany.
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$a Iakovenko, Nataliia $u Department of Biology and Ecology, Ostravian University in Ostrava, Ostrava, Czech RepublicDepartment of Invertebrate Fauna and Systematics, Schmalhausen Institute of Zoology NAS of Ukraine, Kyiv, Ukraine.
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$a Hausdorf, Bernhard $u Zoological Museum, University of Hamburg, Hamburg, Germany.
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$a Petersen, Malte $u Zoological Research Museum Alexander Koenig, Bonn, Germany.
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$a Kück, Patrick $u Zoological Research Museum Alexander Koenig, Bonn, Germany.
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$a Herlyn, Holger $u Institute of Anthropology, Johannes Gutenberg University, Mainz, Germany.
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$a Hankeln, Thomas $u Institute of Molecular Genetics, Biosafety Research and Consulting, Johannes Gutenberg University, Mainz, Germany.
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