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Cited by 112Marine Invertebrate Physiology and EcologyGenomics and Phylogenetic StudiesProtist diversity and phylogeny

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Support for a clade of Placozoa and Cnidaria in genes with minimal compositional bias

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Laumer, Christopher E, Gruber-Vodicka, Harald, Hadfield, Michael G, Pearse, Vicki B, Riesgo, Ana, Marioni, John C, Giribet, Gonzalo·2018·eLife
DOI 10.7554/elife.36278PMC PMC6277202

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Abstract

The phylogenetic placement of the morphologically simple placozoans is crucial to understanding the evolution of complex animal traits. Here, we examine the influence of adding new genomes from placozoans to a large dataset designed to study the deepest splits in the animal phylogeny. Using site-heterogeneous substitution models, we show that it is possible to obtain strong support, in both amino acid and reduced-alphabet matrices, for either a sister-group relationship between Cnidaria and Placozoa, or for Cnidaria and Bilateria as seen in most published work to date, depending on the orthologues selected to construct the matrix. We demonstrate that a majority of genes show evidence of compositional heterogeneity, and that support for the Cnidaria + Bilateria clade can be assigned to this source of systematic error. In interpreting these results, we caution against a peremptory reading of placozoans as secondarily reduced forms of little relevance to broader discussions of early animal evolution.

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Figures

Figure 1. Consensus phylogram showing deep metazoan interrelationships under Bayesian phylogenetic inference of the 430-orthologue amino acid matrix, using the CAT + GTR + Г4 mixture model. All nodes received full posterior probability. Numerical annotations of given nodes represent Extended Quadripartition Internode Certainty (EQP-IC) scores, describing among-gene-tree agreement for both the monophyly of the five major metazoan clades and the given relationships between them in this reference tree. A bar chart on the right depicts the proportion of the total orthologue set each terminal taxon is represented by in the concatenated matrix. ‘Placozoa H1’ in this and all other figures refers to the GRELL isolate sequenced in Srivastava et al., 2008, which has there and elsewhere been referred to as Trichoplax adhaerens, despite the absence of type material linking this name to any modern isolate. Line drawings of clade representatives are taken from the BIODIDAC database (http://biodidac.bio.uottawa.ca/).
Figure 1. Consensus phylogram showing deep metazoan interrelationships under Bayesian phylogenetic inference of the 430-orthologue amino acid matrix, using the CAT + GTR + Г4 mixture model. All nodes received full posterior probability. Numerical annotations of given nodes represent Extended Quadripartition Internode Certainty (EQP-IC) scores, describing among-gene-tree agreement for both the monophyly of the five major metazoan clades and the given relationships between them in this reference tree. A bar chart on the right depicts the proportion of the total orthologue set each terminal taxon is represented by in the concatenated matrix. ‘Placozoa H1’ in this and all other figures refers to the GRELL isolate sequenced in Srivastava et al., 2008, which has there and elsewhere been referred to as Trichoplax adhaerens, despite the absence of type material linking this name to any modern isolate. Line drawings of clade representatives are taken from the BIODIDAC database (http://biodidac.bio.uottawa.ca/).CC BY · PubMed Central
Figure 1—figure supplement 1. Maximum likelihood tree under the C60 +LG + FO + R4 profile mixture model, inferred from the 430-orthologue matrix with full taxon sampling. Nodes annotated with ultrafast bootstrap supports with NNI correction; unannotated nodes received full support.
Figure 1—figure supplement 1. Maximum likelihood tree under the C60 +LG + FO + R4 profile mixture model, inferred from the 430-orthologue matrix with full taxon sampling. Nodes annotated with ultrafast bootstrap supports with NNI correction; unannotated nodes received full support.CC BY · PubMed Central
Figure 1—figure supplement 2. Maximum likelihood tree under a profile mixture model inferred from the 430-orthologue matrix, with only Placozoa H1 used to represent this clade. Nodes annotated with ultrafast bootstrap supports with NNI correction; unannotated nodes received full support.
Figure 1—figure supplement 2. Maximum likelihood tree under a profile mixture model inferred from the 430-orthologue matrix, with only Placozoa H1 used to represent this clade. Nodes annotated with ultrafast bootstrap supports with NNI correction; unannotated nodes received full support.CC BY · PubMed Central
Figure 2. Consensus phylogram under Bayesian phylogenetic inference under the CAT + GTR + Г4 mixture model, on the 430-orthologue concatenated amino acid matrix, recoded into 6 Dayhoff groups. Nodes annotated with posterior probability; unannotated nodes received full support.
Figure 2. Consensus phylogram under Bayesian phylogenetic inference under the CAT + GTR + Г4 mixture model, on the 430-orthologue concatenated amino acid matrix, recoded into 6 Dayhoff groups. Nodes annotated with posterior probability; unannotated nodes received full support.CC BY · PubMed Central
Figure 3. Posterior consensus trees from CAT + GTR + Г4 mixture model analysis of a 94,444 amino acid supermatrix derived from the 303 single-copy conserved eukaryotic BUSCO orthologs, analysed in A. amino acid space or (B) the Dayhoff-6 reduced alphabet space. Nodal support values comprise posterior probabilities; nodes with full support not annotated. Taxon colourings as in previous Figures. (C) Plot of z-scores (summed absolute distance between taxon-specific and global empirical frequencies) from representative posterior predictive tests of amino acid compositional bias, from both the BUSCO 303-orthologue matrix (red) and the initial 430-orthologue matrix (blue). Placozoan taxon abbreviations are shown in blue font.
Figure 3. Posterior consensus trees from CAT + GTR + Г4 mixture model analysis of a 94,444 amino acid supermatrix derived from the 303 single-copy conserved eukaryotic BUSCO orthologs, analysed in A. amino acid space or (B) the Dayhoff-6 reduced alphabet space. Nodal support values comprise posterior probabilities; nodes with full support not annotated. Taxon colourings as in previous Figures. (C) Plot of z-scores (summed absolute distance between taxon-specific and global empirical frequencies) from representative posterior predictive tests of amino acid compositional bias, from both the BUSCO 303-orthologue matrix (red) and the initial 430-orthologue matrix (blue). Placozoan taxon abbreviations are shown in blue font.CC BY · PubMed Central
Figure 4. Schematic depiction of deep metazoan interrelationships in posterior consensus trees from CAT + GTR + Г4 mixture model analyses of matrices made from subsets of genes passing or failing a sensitive null-simulation test of compositional heterogeneity. Panels correspond to (A) the amino acid matrix made within the failing set; (B) the amino acid matrix derived from the passing set; (C) the Dayhoff-6 recoded matrix from the failing set; (D) the Dayhoff-6 recoded matrix from the passing set. Only nodes with posterior probability less than 1.00 are annotated numerically.
Figure 4. Schematic depiction of deep metazoan interrelationships in posterior consensus trees from CAT + GTR + Г4 mixture model analyses of matrices made from subsets of genes passing or failing a sensitive null-simulation test of compositional heterogeneity. Panels correspond to (A) the amino acid matrix made within the failing set; (B) the amino acid matrix derived from the passing set; (C) the Dayhoff-6 recoded matrix from the failing set; (D) the Dayhoff-6 recoded matrix from the passing set. Only nodes with posterior probability less than 1.00 are annotated numerically.CC BY · PubMed Central
Figure 4—figure supplement 1. Maximum likelihood tree under a profile mixture model inferred from the 349-orthologue matrix composed from the subset of genes binned as failing the null-simulation compositional bias test. Nodes annotated with ultrafast bootstrap supports with NNI correction; unannotated nodes received full support.
Figure 4—figure supplement 1. Maximum likelihood tree under a profile mixture model inferred from the 349-orthologue matrix composed from the subset of genes binned as failing the null-simulation compositional bias test. Nodes annotated with ultrafast bootstrap supports with NNI correction; unannotated nodes received full support.CC BY · PubMed Central
Figure 4—figure supplement 2. Maximum likelihood tree under a profile mixture model inferred from the 348-orthologue matrix composed from the subset of genes binned as passing the null-simulation compositional bias test. Nodes annotated with ultrafast bootstrap supports with NNI correction; unannotated nodes received full support.
Figure 4—figure supplement 2. Maximum likelihood tree under a profile mixture model inferred from the 348-orthologue matrix composed from the subset of genes binned as passing the null-simulation compositional bias test. Nodes annotated with ultrafast bootstrap supports with NNI correction; unannotated nodes received full support.CC BY · PubMed Central
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Cites

Research works printed but not linked: 3

  1. Bütschli, 1884, Bemerkungen zur Gastraea-Theorie, Morphologisches Jahrbuch, 9, 415
  2. Grell, 1971, Die Ultrastruktur Von Trichoplax adhaerens F. E. Schultze, Cytobiologie, 4, 216
  3. Grell, 1991, Placozoa. in Microscopic Anatomy of Invertebrates

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Metadata

Authors
Laumer, C. E., Gruber-Vodicka, H., Hadfield, M. G., Pearse, V. B., Riesgo, A., Marioni, J. C., & Giribet, G.
Affiliations
  • European Bioinformatics Institute (GB)
  • Max Planck Institute for Marine Microbiology, Bremen, Germany
  • University of Hawaiʻi at Mānoa (US)
  • University of California, Santa Cruz (US)
  • Natural History Museum (GB)
  • Harvard University (US)
Corresponding author
Laumer, Christopher E
ORCID
Venue
eLife
Publisher
eLife Sciences Publications, Ltd
Published
2018-10-30
Volume
7
ISSN
2050-084X (ISSN-L)
DOI
10.7554/elife.36278
PMC
PMC6277202
OpenAlex
W2898892386
Cited by
112
References
104
Citations by year
2026: 5 · 2025: 11 · 2024: 9 · 2023: 13 · 2022: 13 · 2021: 27 · 2020: 18 · 2019: 14 · 2018: 2
FWCI
11.22
Type
journal article
Language
en
Open access
Licence
Locations
  • eLife (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
  • Apollo (University of Cambridge) (submittedVersion, cc-by)
  • Apollo (cc-by)
Funders
  • Max-Planck-Institut fuer Marine Microbiologie
  • European Bioinformatics Institute
  • Harvard University (Faculty of Arts and Sciences)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Marine Invertebrate Physiology and Ecology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Protist diversity and phylogeny
Keywords
Placozoa, Cnidaria, animal phylogeny, compositional heterogeneity, early animal evolution, sister group relationships
MeSH terms
Animals, Base Composition, Bayes Theorem, Cnidaria, Models, Genetic, Phylogeny, Bias, Likelihood Functions, Metagenome, Placozoa

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