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Curr Biol. 2019 Jun 3;29(11):1818-1826.e6. doi: 10.1016/j.cub.2019.04.009. Epub 2019 May 16.

Mitigating Anticipated Effects of Systematic Errors Supports Sister-Group Relationship between Xenacoelomorpha and Ambulacraria.

Author information

1
Centre de Théorisation et de Modélisation de la Biodiversité, Station d'Ecologie Théorique et Expérimentale, UMR CNRS 5321, 09200 Moulis, France; Département de Biochimie, Centre Robert-Cedergren, Université de Montréal, Montréal, QC H3C 3J7, Canada.
2
Evolution and Development Group, Max-Planck Institute for Molecular Genetics, Ihnestrasse 73, 14195 Berlin, Germany; Dahlem Centre for Genome Research and Medical Systems Biology Envirnomental and Phylogenomics Group, Max-Planck-Straße 3, 12489 Berlin, Germany.
3
Departament de Genètica, Microbiologia i Estadística, Universitat de Barcelona, Av. Diagonal, 643, 08028 Barcelona, Spain; School of Medicine, New York University, 435 E 30th Street, New York, NY 10016, USA.
4
Bioinformatics Group, Institute for Mathematics and Computer Science, University of Greifswald, Walther-Rathenau-Str. 47, 17487 Greifswald, Germany.
5
Centre for Life's Origins and Evolution, Department of Genetics, Evolution and Environment, University College London, Darwin Building, Gower Street, London WC1E 6BT, UK; Department of Computer Science, University College London, Darwin Building, Gower Street, London WC1E 6BT, UK; Department of Computational Biology, University of Lausanne, 1015 Lausanne, Switzerland; Center for Integrative Genomics, University of Lausanne, 1015 Lausanne, Switzerland; Swiss Institute of Bioinformatics, Génopode, 1015 Lausanne, Switzerland.
6
Centre for Life's Origins and Evolution, Department of Genetics, Evolution and Environment, University College London, Darwin Building, Gower Street, London WC1E 6BT, UK; Department of Computer Science, University College London, Darwin Building, Gower Street, London WC1E 6BT, UK; Laboratory of Evolutionary Biochemistry, Intercollegiate Faculty of Biotechnology, University of Gdansk and Medical University of Gdansk, 80-307 Gdansk, Poland.
7
Centre for Life's Origins and Evolution, Department of Genetics, Evolution and Environment, University College London, Darwin Building, Gower Street, London WC1E 6BT, UK; Department of Computer Science, University College London, Darwin Building, Gower Street, London WC1E 6BT, UK.
8
Centre for Microbiology and Environmental Systems Science, University of Vienna, 1090 Vienna, Austria.
9
Sequencing Core Facility, Max Planck Institute for Molecular Genetics, Ihnestraße 63-73, 14195 Berlin, Germany; Department of Ecophysiology and Aquaculture, Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Müggelseedamm 301, 12587 Berlin, Germany.
10
Sequencing Core Facility, Max Planck Institute for Molecular Genetics, Ihnestraße 63-73, 14195 Berlin, Germany.
11
Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa 904-0495, Japan.
12
Natural Science Center for Basic Research and Development, Gene Science Division, Hiroshima University, Higashi-Hiroshima 739-8527, Japan.
13
Shimoda Marine Research Center, University of Tsukuba, Shimoda, Shizuoka 415-0025, Japan.
14
School of Biological & Chemical Sciences, Queen Mary University of London, Mile End Road, London E1 4NS, UK.
15
Institut de Biologie de l'Ecole Normale Supérieure (IBENS), Ecole Normale Supérieure, CNRS, INSERM, PSL Université Paris, 75005 Paris, France.
16
Institute of Organismic and Molecular Evolution, Molecular Genetics and Genome Analysis, Johannes Gutenberg University Mainz, J.J. Becher-Weg 30a, 55128 Mainz, Germany.
17
Helmholtz Zentrum München, Deutsches Forschungszentrum für Gesundheit und Umwelt (GmbH), Ingolstädter Landstraße 1, 85764 Neuherberg, Gemany.
18
Department of Medical Biochemistry and Microbiology, Science for Life Laboratory, Uppsala University, 751 23 Uppsala, Sweden.
19
Department of Pathology and Laboratory Medicine, Emory University School of Medicine, Atlanta, GA, USA.
20
Laboratoire de Biologie du Développement de Villefranche-sur-mer (LBDV), Sorbonne Université, CNRS, 06230 Villefranche-sur-mer, France.
21
Departament de Genètica, Microbiologia i Estadística, Universitat de Barcelona, Av. Diagonal, 643, 08028 Barcelona, Spain; ICREA (Institut Català de Recerca i Estudis Avancats), Passeig Lluís Companys 23, 08010 Barcelona, Spain.
22
Centre for Life's Origins and Evolution, Department of Genetics, Evolution and Environment, University College London, Darwin Building, Gower Street, London WC1E 6BT, UK; Department of Computer Science, University College London, Darwin Building, Gower Street, London WC1E 6BT, UK. Electronic address: m.telford@ucl.ac.uk.

Abstract

Xenoturbella and the acoelomorph worms (Xenacoelomorpha) are simple marine animals with controversial affinities. They have been placed as the sister group of all other bilaterian animals (Nephrozoa hypothesis), implying their simplicity is an ancient characteristic [1, 2]; alternatively, they have been linked to the complex Ambulacraria (echinoderms and hemichordates) in a clade called the Xenambulacraria [3-5], suggesting their simplicity evolved by reduction from a complex ancestor. The difficulty resolving this problem implies the phylogenetic signal supporting the correct solution is weak and affected by inadequate modeling, creating a misleading non-phylogenetic signal. The idea that the Nephrozoa hypothesis might be an artifact is prompted by the faster molecular evolutionary rate observed within the Acoelomorpha. Unequal rates of evolution are known to result in the systematic artifact of long branch attraction, which would be predicted to result in an attraction between long-branch acoelomorphs and the outgroup, pulling them toward the root [6]. Other biases inadequately accommodated by the models used can also have strong effects, exacerbated in the context of short internal branches and long terminal branches [7]. We have assembled a large and informative dataset to address this problem. Analyses designed to reduce or to emphasize misleading signals show the Nephrozoa hypothesis is supported under conditions expected to exacerbate errors, and the Xenambulacraria hypothesis is preferred in conditions designed to reduce errors. Our reanalyses of two other recently published datasets [1, 2] produce the same result. We conclude that the Xenacoelomorpha are simplified relatives of the Ambulacraria.

KEYWORDS:

Acoelomorpha; Ambulacraria; Metazoa; Nephrozoa; Xenoturbella; phylogenomics; phylogeny; systematic error

PMID:
31104936
DOI:
10.1016/j.cub.2019.04.009

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