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      Revisiting metazoan phylogeny with genomic sampling of all phyla

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          Abstract

          Proper biological interpretation of a phylogeny can sometimes hinge on the placement of key taxa—or fail when such key taxa are not sampled. In this light, we here present the first attempt to investigate (though not conclusively resolve) animal relationships using genome-scale data from all phyla. Results from the site-heterogeneous CAT + GTR model recapitulate many established major clades, and strongly confirm some recent discoveries, such as a monophyletic Lophophorata, and a sister group relationship between Gnathifera and Chaetognatha, raising continued questions on the nature of the spiralian ancestor. We also explore matrix construction with an eye towards testing specific relationships; this approach uniquely recovers support for Panarthropoda, and shows that Lophotrochozoa (a subclade of Spiralia) can be constructed in strongly conflicting ways using different taxon- and/or orthologue sets. Dayhoff-6 recoding sacrifices information, but can also reveal surprising outcomes, e.g. full support for a clade of Lophophorata and Entoprocta + Cycliophora, a clade of Placozoa + Cnidaria, and raising support for Ctenophora as sister group to the remaining Metazoa, in a manner dependent on the gene and/or taxon sampling of the matrix in question. Future work should test the hypothesis that the few remaining uncertainties in animal phylogeny might reflect violations of the various stationarity assumptions used in contemporary inference methods.

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          Assessing the root of bilaterian animals with scalable phylogenomic methods.

          A clear picture of animal relationships is a prerequisite to understand how the morphological and ecological diversity of animals evolved over time. Among others, the placement of the acoelomorph flatworms, Acoela and Nemertodermatida, has fundamental implications for the origin and evolution of various animal organ systems. Their position, however, has been inconsistent in phylogenetic studies using one or several genes. Furthermore, Acoela has been among the least stable taxa in recent animal phylogenomic analyses, which simultaneously examine many genes from many species, while Nemertodermatida has not been sampled in any phylogenomic study. New sequence data are presented here from organisms targeted for their instability or lack of representation in prior analyses, and are analysed in combination with other publicly available data. We also designed new automated explicit methods for identifying and selecting common genes across different species, and developed highly optimized supercomputing tools to reconstruct relationships from gene sequences. The results of the work corroborate several recently established findings about animal relationships and provide new support for the placement of other groups. These new data and methods strongly uphold previous suggestions that Acoelomorpha is sister clade to all other bilaterian animals, find diminishing evidence for the placement of the enigmatic Xenoturbella within Deuterostomia, and place Cycliophora with Entoprocta and Ectoprocta. The work highlights the implications that these arrangements have for metazoan evolution and permits a clearer picture of ancestral morphologies and life histories in the deep past.
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            A Large and Consistent Phylogenomic Dataset Supports Sponges as the Sister Group to All Other Animals

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              Acoelomorph flatworms are deuterostomes related to Xenoturbella.

              Xenoturbellida and Acoelomorpha are marine worms with contentious ancestry. Both were originally associated with the flatworms (Platyhelminthes), but molecular data have revised their phylogenetic positions, generally linking Xenoturbellida to the deuterostomes and positioning the Acoelomorpha as the most basally branching bilaterian group(s). Recent phylogenomic data suggested that Xenoturbellida and Acoelomorpha are sister taxa and together constitute an early branch of Bilateria. Here we assemble three independent data sets-mitochondrial genes, a phylogenomic data set of 38,330 amino-acid positions and new microRNA (miRNA) complements-and show that the position of Acoelomorpha is strongly affected by a long-branch attraction (LBA) artefact. When we minimize LBA we find consistent support for a position of both acoelomorphs and Xenoturbella within the deuterostomes. The most likely phylogeny links Xenoturbella and Acoelomorpha in a clade we call Xenacoelomorpha. The Xenacoelomorpha is the sister group of the Ambulacraria (hemichordates and echinoderms). We show that analyses of miRNA complements have been affected by character loss in the acoels and that both groups possess one miRNA and the gene Rsb66 otherwise specific to deuterostomes. In addition, Xenoturbella shares one miRNA with the ambulacrarians, and two with the acoels. This phylogeny makes sense of the shared characteristics of Xenoturbellida and Acoelomorpha, such as ciliary ultrastructure and diffuse nervous system, and implies the loss of various deuterostome characters in the Xenacoelomorpha including coelomic cavities, through gut and gill slits.
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                Author and article information

                Journal
                Proc Biol Sci
                Proc. Biol. Sci
                RSPB
                royprsb
                Proceedings of the Royal Society B: Biological Sciences
                The Royal Society
                0962-8452
                1471-2954
                10 July 2019
                10 July 2019
                10 July 2019
                : 286
                : 1906
                : 20190831
                Affiliations
                [1 ]Museum of Comparative Zoology (MCZ) and Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, USA
                [2 ]EMBL-European Bioinformatics Institute (EBI), Wellcome Genome Campus, Hinxton CB10 1SD, UK
                [3 ]Bioinformatics & Genomics Unit, Center for Genomic Regulation, Carrer del Dr. Aiguader 88, 08003 Barcelona (Spain)
                [4 ]Marine Laboratory, University of Guam, UOG Station, Mangilao, Guam 96923, USA
                [5 ]Department of Biological Sciences and Alabama Museum of Natural History, The University of Alabama, Campus Box 870344, Tuscaoosa, AL 35487, USA
                [6 ]Department of Life Sciences, Natural History Museum of London, Cromwell Road, London SW7 5BD, UK
                [7 ]Departamento de Genética e Biologia Evolutiva, IB, Universidade de São Paulo, 05508090 São Paulo, SP, Brazil
                [8 ]Bermuda Natural History Museum, PO Box FL 145, Flatts, FLBX, Bermuda
                [9 ]Natural History Museum of Denmark, Universitetsparken 15, 2100 Copenhagen, Denmark
                Author notes

                Electronic supplementary material is available online at https://dx.doi.org/10.6084/m9.figshare.c.4552313.

                Author information
                http://orcid.org/0000-0001-8097-8516
                http://orcid.org/0000-0002-4719-6640
                http://orcid.org/0000-0003-0048-7296
                http://orcid.org/0000-0001-7004-7435
                http://orcid.org/0000-0002-8673-2688
                http://orcid.org/0000-0002-7993-1523
                http://orcid.org/0000-0002-1302-5261
                http://orcid.org/0000-0002-0377-0276
                http://orcid.org/0000-0002-5467-8429
                Article
                rspb20190831
                10.1098/rspb.2019.0831
                6650721
                31288696
                945ee4f9-1c38-474a-a954-263722fa25dc
                © 2019 The Authors.

                Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

                History
                : 9 April 2019
                : 17 June 2019
                Funding
                Funded by: National Science Foundation, http://dx.doi.org/10.13039/100000001;
                Award ID: DEB-0732903
                Award ID: DEB-1457539
                Funded by: Faculty of Arts and Sciences, http://dx.doi.org/10.13039/100008036;
                Award ID: Internal core funding to GG
                Funded by: Museum of Comparative Zoology, Harvard University, http://dx.doi.org/10.13039/100010952;
                Award ID: Internal core funding to GG
                Categories
                1001
                183
                70
                198
                Evolution
                Research Article
                Custom metadata
                July 10, 2019

                Life sciences
                phylogenomics,animal phylogeny,compositional bias,taxon sampling,matrix recoding
                Life sciences
                phylogenomics, animal phylogeny, compositional bias, taxon sampling, matrix recoding

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