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Revisiting metazoan phylogeny with genomic sampling of all phyla
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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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“Interestingly, some recent studies have reported Placozoa as sister to Cnidaria (sometimes paired with Ctenophora second) when minimizing compositional heterogeneity5,33, and we have also recovered some support for this (RL2 analysis of WEA15 dataset) (Fig. 3c).”
From Evidence for sponges as sister to all other animals from partitioned phylogenomics with mixture models and recoding (2021) · cites this paper as [5]
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“Furthermore, we previously showed that cnidarians and placozoans are united as sister lineages to the exclusion of bilaterians and sponges based on the mixing of genes from ALG_Ea and ALG_F found on cnidarian chromosomes and placozoan scaffolds57, consistent with recent gene trees55.”
From Ancient gene linkages support ctenophores as sister to other animals (2023) · cites this paper as [55]
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“If sponges are monophyletic (as supported by recent phylogenomic studies8,10,55), then the four fusions-with-mixing that are found in demosponges and parahoxozoans must be shared by all sponges.”
From Ancient gene linkages support ctenophores as sister to other animals (2023) · cites this paper as [55]
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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 [5]
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A taxon-rich and genome-scale phylogeny of Opisthokonta
Liu, H., Steenwyk, J. L., Zhou, X., Schultz, D. T., Kocot, K. M., Shen, X., Rokas, A., & Li, Y. (2024) · PLoS Biology · doi:10.1371/journal.pbio.3002794 · Cited by 41
Self-citationHox gene expression during development of the phoronid Phoronopsis harmeri
Gąsiorowski, L., & Hejnol, A. (2020) · EvoDevo · doi:10.1186/s13227-020-0148-z · Cited by 31
“Laumer CE, Bekkouche N, Kerbl A, Goetz F, Neves RC, Sørensen MV, et al. Spiralian phylogeny informs the evolution of microscopic lineages.”
BackgroundInfluentialTranscriptome‐based target‐enrichment baits for stony corals (Cnidaria: Anthozoa: Scleractinia)
Quek, Z. B. R., Jain, S. S., Neo, M. L., Rouse, G. W., & Huang, D. (2020) · Molecular Ecology Resources · doi:10.1111/1755-0998.13150 · Cited by 30
“Since the advent of DNA sequencing, molecular data have been imperative for phylogenetic reconstructions across the tree of life (Laumer et al., 2019; Pizarro et al., 2018; Wickett et al., 2014), and scleractinian corals are no exception.”
BackgroundEvolutionary History of Major Chemosensory Gene Families across Panarthropoda
Vizueta, J., Escuer, P., Frías-López, C., Guirao‐Rico, S., Hering, L., Mayer, G., Rozas, J., & Sánchez‐Gracia, A. (2020) · Molecular Biology and Evolution · doi:10.1093/molbev/msaa197 · Cited by 31
DNA Sequences Are as Useful as Protein Sequences for Inferring Deep Phylogenies
Kapli, P., Kotari, I., Telford, M. J., Goldman, N., & Yang, Z. (2023) · Systematic Biology · doi:10.1093/sysbio/syad036 · Cited by 36
“…exclusively relied on protein sequences (Philippe et al. 2011; Laumer et al. 2015; Telford et al. 2015; Kocot et al. 2017; Cannon et al. 2016; Laumer et al. 2019; Marlétaz et al. 2019; Philippe et al. 2019; Kapli and Telford 2020; Kapli et al. 2021), and no cor‑ responding DNA alignments for…”
BackgroundMethodPandey, A., & Braun, E. L. (2020) · Biology · doi:10.3390/biology9040064 · Cited by 30
“Placozoa+cnidaria also emerged in a subsequent study with more extensive taxon sampling [117], but only after sites that appeared to exhibit compositional bias and/or saturation were excluded.”
BackgroundResultLyons, D. C., Perry, K. J., Batzel, G. O., & Henry, J. J. (2020) · Developmental Biology · doi:10.1016/j.ydbio.2020.04.008 · Cited by 29
“It includes familiar taxa such as molluscs, annelids, and platyhelminthes, as well as several lesser-known groups, such as entoprocts and gnathostomulids (Giribet, 2008; Laumer et al., 2019).”
BackgroundPolyzoa is back: The effect of complete gene sets on the placement of Ectoprocta and Entoprocta
Khalturin, K., Shunatova, N., Shchenkov, S. V., Sasakura, Y., Kawamitsu, M., & Satoh, N. (2022) · Science Advances · doi:10.1126/sciadv.abo4400 · Cited by 30
“Thus, Giribet and Edgecombe ( 56 ) mentioned that the inclusion of Cycliophora in the analyses changes the topology: Some phylogenomic analyses recover a group of Bryozoa + Entoprocta ( 12 , 42 , 43 ), but this clade often disappears when Cycliophora is added ( 9 , 14 , 16 , 32 ).”
InfluentialA comprehensive study of arthropod and onychophoran Fox gene expression patterns
Janßen, R., Schomburg, C., Prpíc, N.-M., & Budd, G. E. (2022) · PLoS ONE · doi:10.1371/journal.pone.0270790 · Cited by 27
Hahn, N., Büschgens, L., Schwedhelm‐Domeyer, N., Bank-Aubin, S., Geurten, B. R. H., Neugebauer, P., Massih, B., Göpfert, M. C., & Heinrich, R. (2019) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2019.00251 · Cited by 26
Andrikou, C., Passamaneck, Y. J., Lowe, C. J., Martindale, M. Q., & Hejnol, A. (2019) · EvoDevo · doi:10.1186/s13227-019-0146-1 · Cited by 28
Ctenophores are direct developers that reproduce continuously beginning very early after hatching
Edgar, A., Ponciano, J. M., & Martindale, M. Q. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2122052119 · Cited by 28
Jakovlić, I., Zou, H., Ye, T., Zhang, H., Liu, X., Xiang, C., Wang, G., & Zhang, D. (2023) · Nature Communications · doi:10.1038/s41467-023-42095-8 · Cited by 28
“The phylum-level tree topology was constrained according to Laumer et al. 54 .”
Bar-Yaacov, D. (2022) · PLoS Pathogens · doi:10.1371/journal.ppat.1010250 · Cited by 27
Ancestral morphology of Ecdysozoa constrained by an early Cambrian stem group ecdysozoan
Howard, R. J., Edgecombe, G. D., Shi, X., Hou, X., & Ma, X. (2020) · BMC Evolutionary Biology · doi:10.1186/s12862-020-01720-6 · Cited by 26
“Hypotheses concerning the origins and early evolution of multiple ecdysozoan subgroups have been proposed from their spectacular Cambrian fossil record [13–18], but all taxa fall within the Cycloneuralia (Scalidophora + Nematoida) or Panarthropoda, with little known about the ancestral characteristics of Ecdysozoa bey…”
BackgroundInfluentialBrenzinger, B., Schrödl, M., & Kano, Y. (2021) · Scientific Reports · doi:10.1038/s41598-021-99172-5 · Cited by 27
The lower Cambrian lobopodianCardiodictyonresolves the origin of euarthropod brains
Strausfeld, N. J., Hou, X., Sayre, M. E., & Hirth, F. (2022) · Science · doi:10.1126/science.abn6264 · Cited by 28
Phylogenomics and the first higher taxonomy of Placozoa, an ancient and enigmatic animal phylum
Tessler, M., Neumann, J. S., Kamm, K., Osigus, H., Eshel, G., Narechania, A., Burns, J. A., DeSalle, R., & Schierwater, B. (2022) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2022.1016357 · Cited by 28
“Trees were based on the amino acid sequence matrix in Supplementary Data 1, and rooted using Capsaspora owczarzaki based on current understanding of our outgroup and ingroup relationships (Ruiz-Trillo et al., 2004; Sebé-Pedrós et al., 2013; Suga et al., 2013; Laumer et al., 2019; Fernández and Gabaldón, 2020; Pandey a…”
MethodThe compact genome of the sponge Oopsacas minuta (Hexactinellida) is lacking key metazoan core genes
Santini, S., Schenkelaars, Q., Jourda, C., Duschene, M., Belahbib, H., Rocher, C., Selva, M., Riesgo, A., Vervoort, M., Leys, S. P., et al. (2023) · BMC Biology · doi:10.1186/s12915-023-01619-w · Cited by 28
Self-citationStructural and evolutionary insights into astacin metallopeptidases
Gomis‐Rüth, F. X., & Stöcker, W. (2023) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2022.1080836 · Cited by 26
“Also setting phylum Porifera at the root of Metazoa contradicts recent models, which choose Ctenophora for this place (Giribet et al., 2019; Laumer et al., 2019).”
BackgroundMethodResultInfluentialCunha, T. J., de Medeiros, B. A. S., Lord, A., Sørensen, M. V., & Giribet, G. (2023) · Current Biology · doi:10.1016/j.cub.2023.07.003 · Cited by 25
Self-citationMartynov, A. V., Lundin, K., PICTON, B. E., Fletcher, K. C., Malmberg, K., & Korshunova, T. (2020) · PLoS ONE · doi:10.1371/journal.pone.0227173 · Cited by 27
Wernström, J. V., Gąsiorowski, L., & Hejnol, A. (2022) · bioRxiv · doi:10.1186/s13227-022-00202-8 · Cited by 17
“The similar pattern of loss in bryozoans and phoronids agrees well with recent studies that indicate a sister-group relationship between the two [31, 43, 44, 92, 93].”
BackgroundResultKoutsouveli, V., Cárdenas, P., Conejero, M., Rapp, H. T., & Riesgo, A. (2020) · Frontiers in Marine Science · doi:10.3389/fmars.2020.595267 · Cited by 25
Self-citationNitric oxide signaling in ctenophores
Moroz, L. L., Mukherjee, K., & Romanova, D. Y. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1125433 · Cited by 24
“The recently proposed most basal position of ctenophores (as the sister group to all other animals) is still highly debated (Whelan et al., 2015, 2017; Halanych et al., 2016; Telford et al., 2016; Laumer et al., 2019; Fernandez and Gabaldon, 2020; Kapli and Telford, 2020; Li et al., 2021; Redmond and McLysaght, 2021;…”
BackgroundFusion, fission, and scrambling of the bilaterian genome in BryozoaPreprint
Lewin, T. D., Liao, I. J.-Y., Chen, M.-E., Bishop, J., Holland, P. W. H., & Luo, Y. (2025) · Genome Research · doi:10.1101/gr.279636.124 · Cited by 23
“…(1) the Lophophorata hypothesis, which proposes a close relationship to phoronids and brachiopods (Nesnidal et al. 2013; Luo et al. 2018; Laumer et al. 2019; Marlétaz et al. 2019), and (2) the Polyzoa hypothesis, which proposes closer affiliation to Entoprocta and Cycliophora (Supple-mentalFig.”
InfluentialApplication of phylogenomic tools to unravel anthozoan evolution
Quek, Z. B. R., & Huang, D. (2021) · Coral Reefs · doi:10.1007/s00338-021-02072-3 · Cited by 24
The early animal radiation: insights from interpreting the Cambrian problematic fossils
Cong, P. (2023) · Frontiers in Earth Science · doi:10.3389/feart.2023.1120118 · Cited by 24
“In protostome, we are now more confident about the phylogenetic position not only of the common animals such as arthropods, molluscs, annelids, brachiopods, and bryozoans but of some small cryptic groups such as chaetognaths, gnathifers, tardigrades, xenoturbellids, aceolomorphs (Laumer et al., 2019), albeit final agr…”
BackgroundDrábková, M., Kocot, K. M., Halanych, K. M., Oakley, T. H., Moroz, L. L., Cannon, J. T., Kuris, A. M., Garcia‐Vedrenne, A. E., Pankey, M. S., Ellis, E. A., et al. (2022) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2022.0683 · Cited by 26
“B 2890220683 2 The early radiation of Lophotrochozoa (549–535 Ma; [13]), a major clade of protostome metazoans including annelids, molluscs, brachiopods, bryozoans, flatworms and rotifers among others, has been especially challenging to uncover [5,8,9,14,15].”
BackgroundSelf-citationA Cambrian tommotiid preserving soft tissues reveals the metameric ancestry of lophophorates
Guo, J. C., Parry, L. A., Vinther, J., Edgecombe, G. D., Wei, F., Zhao, J., Zhao, Y., Béthoux, O., Lei, X., Chen, A., et al. (2022) · Current Biology · doi:10.1016/j.cub.2022.09.011 · Cited by 28
Mitochondrial Genome Evolution of Placozoans: Gene Rearrangements and Repeat Expansions
Miyazawa, H., Osigus, H., Rolfes, S., Kamm, K., Schierwater, B., & Nakano, H. (2020) · Genome Biology and Evolution · doi:10.1093/gbe/evaa213 · Cited by 22
“In sponge mitogenomes, differences in the number and locations of these repeats and their proliferation in both the IGRs and protein-coding genes have been reported even between closely related species (Lavrov 2010).”
BackgroundFossil Constraints on the Timescale of Parasitic Helminth Evolution
Baets, K. D., Dentzien‐Dias, P., Harrison, G. W. M., Littlewood, D. T. J., & Parry, L. A. (2021) · Topics in geobiology · doi:10.1007/978-3-030-42484-8_7 · Cited by 23
Gąsiorowski, L., Børve, A., Cherneva, I. A., Orús-Alcalde, A., & Hejnol, A. (2021) · BMC Biology · doi:10.1186/s12915-021-01113-1 · Cited by 21
Moreland, R. T., Nguyen, A., Ryan, J. F., & Baxevanis, A. D. (2020) · Database · doi:10.1093/database/baaa029 · Cited by 20
Roberts, N. G., Gilmore, M. J., Struck, T. H., & Kocot, K. M. (2024) · Genome Biology and Evolution · doi:10.1093/gbe/evae254 · Cited by 22
Self-citationOntano, A. Z., Steiner, H. G., & Sharma, P. P. (2021) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2021.107378 · Cited by 22
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
- 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
- hybrid
- doi.org
- 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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