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Cited by 365Genomics and Phylogenetic StudiesMarine Invertebrate Physiology and EcologyProtist diversity and phylogeny

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Revisiting metazoan phylogeny with genomic sampling of all phyla

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Laumer, Christopher E., Fernández, Rosa, Lemer, Sarah, Combosch, David, Kocot, Kevin M., Riesgo, Ana, Andrade, Sónia C. S., Sterrer, Wolfgang, Sørensen, Martin V., Giribet, Gonzalo·2019·Proceedings of the Royal Society B: Biological Sciences
DOI 10.1098/rspb.2019.0831PMC PMC6650721
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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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Figure 1. Schematic description of gene tree construction, orthologue assignment and matrix construction. Gene selection criteria for clade-specific matrix construction and other methodological details are discussed in the text.
Figure 1. Schematic description of gene tree construction, orthologue assignment and matrix construction. Gene selection criteria for clade-specific matrix construction and other methodological details are discussed in the text.CC BY · PubMed Central
Figure 2. (a) Posterior consensus summary of CAT + GTR + Γ4 analysis of reduced, BMGE-trimmed pan-Metazoa matrix in amino acid space, trimmed of four rogue taxa prior to summary. (b) Cladogram depiction of relationships and support within Spiralia recovered in the previous analysis, shown to improve readability. (c) Posterior consensus summary of CAT + GTR + Γ4 analysis of the same matrix, recoded into Dayhoff-6 groups and trimmed of six rogue taxa prior to summary. (d) Cladogram depiction of relationships and support within Spiralia recovered in the previous analysis. Nodal support values are posterior probability; unlabelled nodes received full support. Relationships within labelled clades (phyla) are not annotated with support values to improve visualization, except in the case that the monophyly of the clade in question received less than full posterior probability. (Online version in colour.)
Figure 2. (a) Posterior consensus summary of CAT + GTR + Γ4 analysis of reduced, BMGE-trimmed pan-Metazoa matrix in amino acid space, trimmed of four rogue taxa prior to summary. (b) Cladogram depiction of relationships and support within Spiralia recovered in the previous analysis, shown to improve readability. (c) Posterior consensus summary of CAT + GTR + Γ4 analysis of the same matrix, recoded into Dayhoff-6 groups and trimmed of six rogue taxa prior to summary. (d) Cladogram depiction of relationships and support within Spiralia recovered in the previous analysis. Nodal support values are posterior probability; unlabelled nodes received full support. Relationships within labelled clades (phyla) are not annotated with support values to improve visualization, except in the case that the monophyly of the clade in question received less than full posterior probability. (Online version in colour.)CC BY · PubMed Central
Figure 3. (a) Posterior consensus summary of CAT + GTR + Γ4 analysis of BMGE-trimmed Spiralia-specific matrix in amino acid space, trimmed of 2 rogue taxa prior to summary; the phylogram is drawn with the position of the root taken from the pan-Metazoa results shown in figure 2b. Cladogram depiction of the same, given to improve readability. Criteria for nodal annotation are as in figure 2; in this case, no internodes outside the labelled phyla received less than full support.
Figure 3. (a) Posterior consensus summary of CAT + GTR + Γ4 analysis of BMGE-trimmed Spiralia-specific matrix in amino acid space, trimmed of 2 rogue taxa prior to summary; the phylogram is drawn with the position of the root taken from the pan-Metazoa results shown in figure 2b. Cladogram depiction of the same, given to improve readability. Criteria for nodal annotation are as in figure 2; in this case, no internodes outside the labelled phyla received less than full support.CC BY · PubMed Central
Figure 4. (a) Posterior consensus summary of CAT + GTR + Γ4 analysis of BMGE-trimmed Ecdysozoa-specific matrix in amino acid space, trimmed of Nectonema sp. (Nematomorpha) due to its behaviour as a rogue taxon prior to summary. (b) Cladogram depiction of ingroup ecdysozoan relationships within this phylogram, given to improve readability. Criteria for nodal annotation are as in figure 2. (Online version in colour.)
Figure 4. (a) Posterior consensus summary of CAT + GTR + Γ4 analysis of BMGE-trimmed Ecdysozoa-specific matrix in amino acid space, trimmed of Nectonema sp. (Nematomorpha) due to its behaviour as a rogue taxon prior to summary. (b) Cladogram depiction of ingroup ecdysozoan relationships within this phylogram, given to improve readability. Criteria for nodal annotation are as in figure 2. (Online version in colour.)CC BY · PubMed Central
Figure 5. Cladograms depicting metazoan relationships outside Bilateria, summarizing relationships from CAT + GTR + Γ4 analysis of the non-Bilateria specific matrix, varied as follows: (a) amino acid matrix with all sampled opisthokont outgroups; (b) the same, recoded into Dayhoff-6 groups; (c) amino acid matrix including only Choanoflagellata as outgroups; (d) the same, recoded into Dayhoff-6 groups. On the matrix pruned of non-choanoflagellate outgroups, BMGE-trimming was performed after pruning, yielding a matrix of 68 337 sites, in contrast to the 61 096 sites retained when all outgroups are included prior to trimming. Trees have been arbitrarily drawn with the root between Apusomonadida and Opisthokonta. (Online version in colour.)
Figure 5. Cladograms depicting metazoan relationships outside Bilateria, summarizing relationships from CAT + GTR + Γ4 analysis of the non-Bilateria specific matrix, varied as follows: (a) amino acid matrix with all sampled opisthokont outgroups; (b) the same, recoded into Dayhoff-6 groups; (c) amino acid matrix including only Choanoflagellata as outgroups; (d) the same, recoded into Dayhoff-6 groups. On the matrix pruned of non-choanoflagellate outgroups, BMGE-trimming was performed after pruning, yielding a matrix of 68 337 sites, in contrast to the 61 096 sites retained when all outgroups are included prior to trimming. Trees have been arbitrarily drawn with the root between Apusomonadida and Opisthokonta. (Online version in colour.)CC BY · PubMed Central

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  1. Ax P, 1999, Das System der Metazoa II. Ein Lehrbuch der phylogenetischen Systematik

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Metadata

Authors
Laumer, C. E., Fernández, R., Lemer, S., Combosch, D., Kocot, K. M., Riesgo, A., Andrade, S. C. S., Sterrer, W., Sørensen, M. V., & Giribet, G.
Affiliations
  • European Bioinformatics Institute (GB)
  • Harvard University (US)
  • University of Alabama (US)
  • Natural History Museum (GB)
  • Universidade de São Paulo (BR)
  • Bermuda Natural History Museum, PO Box FL 145, Flatts, FLBX, Bermuda
  • Natural History Museum of Denmark (DK)
Corresponding author
Laumer, Christopher E.
ORCID
Venue
Proceedings of the Royal Society B: Biological Sciences
Publisher
The Royal Society
Published
2019-07-10
Volume
286
Issue
1906
Pages
20190831
ISSN
  • 0080-4649 (ISSN-L)
  • 0962-8452
  • 1471-2954
DOI
10.1098/rspb.2019.0831
PMC
PMC6650721
OpenAlex
W2957892651
Semantic Scholar
19950757d5ee0e9f1ec51627ad75dc7ffaa31ab8
Cited by
360
References
77
Citations by year
2026: 24 · 2025: 41 · 2024: 65 · 2023: 61 · 2022: 55 · 2021: 59 · 2020: 43 · 2019: 10
FWCI
14.23
Type
journal article
Language
en
Update notices
correction (2019-11-06)
Open access
Licence
Locations
  • Proceedings of the Royal Society B Biological Sciences (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Research at the University of Copenhagen (University of Copenhagen) (publishedVersion, cc-by)
  • Repositori digital de la UPF (Universitat Pompeu Fabra) (publishedVersion, cc-by)
Funders
  • National Science Foundation (DEB-0732903, DEB-1457539)
  • Faculty of Arts and Sciences (Internal core funding to GG)
  • Museum of Comparative Zoology, Harvard University (Internal core funding to GG)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
  • 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 › Protist diversity and phylogeny
Keywords
animal phylogeny, Lophophorata, Gnathifera, chaetognaths, Spiralia, Panarthropoda, Lophotrochozoa, Ctenophora, Entoprocta, Cycliophora, Placozoa, Cnidaria, matrix construction, stationarity assumption, phylogenetic incongruence
MeSH terms
Animals, Classification, Phylogeny, Genomics

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