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Mitigating Anticipated Effects of Systematic Errors Supports Sister-Group Relationship between Xenacoelomorpha and Ambulacraria
Open accessAbstract
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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“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.”
From Evidence for sponges as sister to all other animals from partitioned phylogenomics with mixture models and recoding (2021) · cites this paper as [24]
In the citing paper
“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.”
From Evidence for sponges as sister to all other animals from partitioned phylogenomics with mixture models and recoding (2021) · cites this paper as [24]
In the citing paper
“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.”
From Evidence for sponges as sister to all other animals from partitioned phylogenomics with mixture models and recoding (2021) · cites this paper as [24]
In the citing paper
“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.”
From Evidence for sponges as sister to all other animals from partitioned phylogenomics with mixture models and recoding (2021) · cites this paper as [24]
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Renewed perspectives on the sedentary-pelagic last common bilaterian ancestor
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Metadata
- 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.
- ORCID
- 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
- bronze
- doi.org
- Licence
- 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
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › 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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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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