Cited by 154Marine Invertebrate Physiology and EcologyInvertebrate Taxonomy and EcologyGenomics and Phylogenetic Studies

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

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Philippe, Hervé, Poustka, Albert J., Chiodin, Marta, Hoff, Katharina J., Dessimoz, Christophe, Tomiczek, Bartlomiej, Schiffer, Philipp H., Müller, Steven +17 more·2019·Current Biology

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.

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Crossref · 10.1016/j.cub.2019.04.009

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  • The RL2 findings support recent efforts pairing recoding and site-heterogeneous models to resolve difficult, ancient nodes in animal phylogeny, despite the erosion of data relevant to more shallow nodes.

    “The RL2 findings also support recent efforts pairing recoding and site-heterogeneous models to resolve difficult, ancient nodes in animal phylogeny5,9,24,33, despite the erosion of data relevant to more shallow nodes.”
  • CAT/CATGTR offers improved resilience to long-branch attraction artefacts and is almost always better fitting than standard site-homogeneous amino acid substitution models.

    “CAT/CATGTR offers improved resilience to long-branch attraction artefacts (LBA)22 and is almost always better fitting than standard site-homogeneous amino acid substitution models (e.g. WAG)8–10,23–29.”
  • The reduction in support for Xenacoelomorpha as sister to all other bilaterians is consistent with this placement being a systematic error.

    “Interestingly, our re-analyses of the REA dataset (WEA15 and WEA17 do not include Xenacoelomorpha) show reducing support for Xenacoelomorpha as sister to all other bilaterian animals as better-fitting models are applied (REA dataset UFBOOT: L1 = 98%; L4 = 49%) (Supplementary Fig. 17), consistent with this placement being a systematic error24.”
  • Despite supporting Ctenophora sister under CATGTR, WEA17 was later shown to support Porifera sister when amino acid recoding strategies and CATGTR are combined.

    “Despite supporting Ctenophora sister under CATGTR, WEA17 was later shown to support Porifera sister when amino acid recoding strategies and CATGTR are combined, an approach reported to allow better accommodation of systematic error9,24.”

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Authors
Philippe, H., Poustka, A. J., Chiodin, M., Hoff, K. J., Dessimoz, C., Tomiczek, B., Schiffer, P. H., Müller, S., Domman, D., Horn, M., Kuhl, H., Timmermann, B., Satoh, N., Hikosaka-Katayama, T., Nakano, H., Rowe, M. L., Elphick, M. R., Thomas-Chollier, M., Hankeln, T., Mertes, F., Wallberg, A., Rast, J. P., Copley, R. R., Martinez, P., & Telford, M. J.
Affiliations
  • Centre National de la Recherche Scientifique (FR)
  • Max Planck Institute for Molecular Genetics (DE)
  • New York University (US)
  • Universität Greifswald (DE)
  • SIB Swiss Institute of Bioinformatics (CH)
  • University College London (GB)
  • University of Vienna (AT)
  • Leibniz Institute of Freshwater Ecology and Inland Fisheries (DE)
  • Okinawa Institute of Science and Technology Graduate University (JP)
  • Hiroshima University (JP)
  • Shimoda Marine Research Center, University of Tsukuba (JP)
  • Queen Mary University of London (GB)
  • Johannes Gutenberg University Mainz (DE)
  • Helmholtz Munich (DE)
  • Emory University (US)
Corresponding author
Telford, Maximilian J.
Venue
Current Biology
Publisher
Elsevier BV
Published
2019-06
Volume
29
Issue
11
Pages
1818-1826.e6
ISSN
0960-9822 (ISSN-L)
OpenAlex
W2944996147
Cited by
152
References
45
Citations by year
2026: 9 · 2025: 19 · 2024: 16 · 2023: 20 · 2022: 28 · 2021: 25 · 2020: 24 · 2019: 11
FWCI
16.77
Type
journal article
Language
en
Open access
Locations
  • Current Biology (publishedVersion)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, other-oa)
  • UCL Discovery (University College London) (submittedVersion)
  • IRIS (submittedVersion)
  • Site cant be reached (submittedVersion, other-oa)
  • MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
  • PuSH - Publication Server of Helmholtz Zentrum München (submittedVersion)
  • Queen Mary Research Online (Queen Mary University of London) (submittedVersion)
  • SERVAL (Université de Lausanne) (submittedVersion)
Funders
  • European Research Council (ERC-2012-AdG 322790)
  • Labex TULIP (ANR-10-LABX-41)
  • Deutsche Forschungsgemeinschaft (DFG Ha2103/4)
  • Johannes Gutenberg University Center of Computational Sciences Mainz
  • Swiss National Science Foundation (150654)
  • OIST
  • JSPS (JP26711022)
  • Canada Foundation for Innovation
  • Ministère de l’Économie, de la Science et de l’Innovation du Québec
  • Fonds de Recherche du Québec — Nature et Technologies
Topics
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Invertebrate Taxonomy and Ecology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
Keywords
Xenacoelomorpha, Acoelomorpha, Xenoturbella, Ambulacraria, long-branch attraction, systematic errors, molecular evolution rate, phylogenetic signal
MeSH terms
Animals, Echinodermata, Biological Evolution, Invertebrates, Phylogeny, Chordata

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