Revisiting metazoan phylogeny with genomic sampling of all phyla
Open accessAbstract
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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Some recent studies have reported Placozoa as sister to Cnidaria (sometimes paired with Ctenophora second) when minimizing compositional heterogeneity.
“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]
The Results and discussion (Non-bilaterian matrices, N and N′) report strong support for Placozoa as sister to Cnidaria after Dayhoff-6 recoding and removal of distant outgroups. The paper does not establish the parenthetical claim that Ctenophora was placed second in that analysis; it says the placement of the deepest-splitting animal phylum varied by matrix. (LLM, conf=0.83)
Experimental — accuracy not yet measuredCnidarians 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 scaffolds, consistent with recent gene trees.
“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]
If sponges are monophyletic, then the four fusions-with-mixing that are found in demosponges and parahoxozoans must be shared by all sponges.
“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]
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.”
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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Self-citationData from: Revisiting metazoan phylogeny with genomic sampling of all phyla
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BackgroundAncient gene linkages support ctenophores as sister to other animals
Schultz, D. T., Haddock, S. H. D., Bredeson, J. V., Green, R. E., Simakov, O., & Rokhsar, D. S. (2023) · Nature · doi:10.1038/s41586-023-05936-6 · Cited by 362 · see citing works
Deeply conserved synteny and the evolution of metazoan chromosomes
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PhyKIT: a broadly applicable UNIX shell toolkit for processing and analyzing phylogenomic data
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Evolution of DNA Methylome Diversity in Eukaryotes
de Mendoza, A., Lister, R., & Bogdanović, O. (2019) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.11.003 · Cited by 165 · see citing works
Diversity and evolution of the animal virome
Harvey, E., & Holmes, E. C. (2022) · Nature Reviews Microbiology · doi:10.1038/s41579-021-00665-x · Cited by 165 · see citing works
Toward a genome sequence for every animal: Where are we now?
Hotaling, S., Kelley, J. L., & Frandsen, P. B. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2109019118 · Cited by 167 · see citing works
Gene gain and loss across the metazoan tree of life
Fernández, R., & Gabaldón, T. (2020) · Nature Ecology & Evolution · doi:10.1038/s41559-019-1069-x · Cited by 165 · see citing works
Self-citationThe origin of animals: an ancestral reconstruction of the unicellular-to-multicellular transition
Ros-Rocher, N., Pérez-Posada, A., Leger, M. M., & Ruiz‐Trillo, I. (2021) · Open Biology · doi:10.1098/rsob.200359 · Cited by 160 · see citing works
“Mikhailov KV et al. 2009 The origin of Metazoa: a transition from temporal to spatial cell differentiation.”
BackgroundInfluentialRooting the Animal Tree of Life
Li, Y., Shen, X.-X., Evans, B., Dunn, C. W., & Rokas, A. (2021) · Molecular Biology and Evolution · doi:10.1093/molbev/msab170 · Cited by 146 · see citing works
Redmond, A. K., & McLysaght, A. (2021) · Nature Communications · doi:10.1038/s41467-021-22074-7 · Cited by 139 · see citing works
The origin of animal body plans: a view from fossil evidence and the regulatory genome
Erwin, D. H. (2020) · Development · doi:10.1242/dev.182899 · Cited by 133 · see citing works
“However, their placement is sensitive to the position of ctenophores (Laumer et al., 2019) and they are shown in a polytomy with cnidarians in Fig.”
BackgroundNeural versus alternative integrative systems: molecular insights into origins of neurotransmitters
Moroz, L. L., Romanova, D. Y., & Kohn, A. B. (2021) · Philosophical Transactions of the Royal Society B · doi:10.1098/rstb.2019.0762 · Cited by 130 · see citing works
Lack of support for Deuterostomia prompts reinterpretation of the first Bilateria
Kapli, P., Natsidis, P., Leite, D. J., Fursman, M., Jeffrie, N., Rahman, I. A., Philippe, H., Copley, R. R., & Telford, M. J. (2021) · Science Advances · doi:10.1126/sciadv.abe2741 · Cited by 100 · see citing works
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“The problem is particularly acute when dealing with fast evolving sequences, such as viral or immune-related ones, or when attempting to resolve distant relationships, such as at the origins of animals 4–6 or beyond.”
Kallal, R. J., Kulkarni, S., Dimitrov, D., Benavides, L. R., Arnedo, M. A., Giribet, G., & Hormiga, G. (2020) · Cladistics · doi:10.1111/cla.12439 · Cited by 100 · see citing works
Self-citationCurrent understanding on the Cambrian Explosion: questions and answers
Zhang, X., & Shu, D. (2021) · PalZ · doi:10.1007/s12542-021-00568-5 · Cited by 96 · see citing works
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On the origin and evolution of RNA editing in metazoans
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Diversity of cilia-based mechanosensory systems and their functions in marine animal behaviour
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Major Revisions in Pancrustacean Phylogeny and Evidence of Sensitivity to Taxon Sampling
Bernot, J. P., Owen, C. L., Wolfe, J. M., Meland, K., Olesen, J., & Crandall, K. A. (2023) · Molecular Biology and Evolution · doi:10.1093/molbev/msad175 · Cited by 82 · see citing works
Evolution of glutamatergic signaling and synapses
Moroz, L. L., Nikitin, M. A., Poličar, P. G., Kohn, A. B., & Romanova, D. Y. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108740 · Cited by 80 · see citing works
Microbiomes of microscopic marine invertebrates do not reveal signatures of phylosymbiosis
Boscaro, V., Holt, C. C., Steenkiste, N. W. L. V., Herranz, M., Irwin, N. A. T., Àlvarez-Campos, P., Grzelak, K., Holovachov, O. V., Kerbl, A., Mathur, V., et al. (2022) · Nature Microbiology · doi:10.1038/s41564-022-01125-9 · Cited by 76 · see citing works
Examples of Extreme Survival: Tardigrade Genomics and Molecular Anhydrobiology
Arakawa, K. (2022) · Annual Review of Animal Biosciences · doi:10.1146/annurev-animal-021419-083711 · Cited by 72 · see citing works
The Ediacaran origin of Ecdysozoa: integrating fossil and phylogenomic data
Howard, R. J., Giacomelli, M., Lozano-Fernández, J., Edgecombe, G. D., Fleming, J. F., Kristensen, R. M., Ma, X., Olesen, J., Sørensen, M. V., Thomsen, P. F., et al. (2022) · Journal of the Geological Society · doi:10.1144/jgs2021-107 · Cited by 70 · see citing works
“Only one other phylogenetic study has sampled all eight ecdysozoan phyla (Laumer et al. 2019), which was largely consistent with our topology.”
BackgroundResultInfluentialSelf-citationWang, J., Zhang, L., Lian, S., Qin, Z., Zhu, X., Dai, X., Huang, Z., Ke, C., Zhou, Z., Wei, J., et al. (2020) · Nature Ecology & Evolution · doi:10.1038/s41559-020-1138-1 · Cited by 68 · see citing works
A Practical Guide to Design and Assess a Phylogenomic Study
Lozano-Fernández, J. (2022) · Genome Biology and Evolution · doi:10.1093/gbe/evac129 · Cited by 68 · see citing works
“…and filter those outlier sequences have been used to curate phylogenomic matrices of protists (Strassert et al. 2021; Irisarri et al. 2022), plants (Laurin-Lemay et al. 2012), fungi (Varga et al. 2019), metazoans (Simion et al. 2017) or mammals (Scornavacca et al. 2019), and there are softwares to…”
BackgroundMethodArthropod Origins: Integrating Paleontological and Molecular Evidence
Edgecombe, G. D. (2020) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev-ecolsys-011720-124437 · Cited by 65 · see citing works
Barrera‐Redondo, J., Lotharukpong, J. S., Drost, H., & Coelho, S. M. (2023) · Genome biology · doi:10.1186/s13059-023-02895-z · Cited by 61 · see citing works
Animal regeneration in the era of transcriptomics
Bideau, L., Kerner, P., Hui, J. H. L., Vervoort, M., & Gazave, E. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03760-7 · Cited by 64 · see citing works
“Phylogenetic tree topology is derived from recent metazoans’ phylogenies [175, 176], with still-controversial lineage positioning depicted with dotted lines.”
BackgroundFunctional Insights From the Evolutionary Diversification of Big Defensins
Gerdol, M., Schmitt, P., Venier, P., Rocha, G., Rosa, R. D., & Destoumieux‐Garzón, D. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00758 · Cited by 59 · see citing works
“The topology of the tree follows the branching pattern resulting from a recent phylogenomic study (100).”
BackgroundMolecular evidence for a single origin of ultrafiltration-based excretory organs
Gąsiorowski, L., Andrikou, C., Janßen, R., Bump, P. A., Budd, G. E., Lowe, C. J., & Hejnol, A. (2021) · Current Biology · doi:10.1016/j.cub.2021.05.057 · Cited by 55 · see citing works
Form and Function of the Vertebrate and Invertebrate Blood-Brain Barriers
Dunton, A. D., Göpel, T., Ho, D. H., & Burggren, W. W. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222212111 · Cited by 55 · see citing works
Skimming genomes for systematics and DNA barcodes of corals
Quattrini, A. M., McCartin, L. J., Easton, E. E., Horowitz, J., Wirshing, H. H., Bowers, H., Mitchell, K., González‐García, M. D. P., Sei, M., McFadden, C. S., et al. (2024) · Ecology and Evolution · doi:10.1002/ece3.11254 · Cited by 53 · see citing works
“Numerous genomic methods [e.g., whole-genome se - quencing (e.g., Laumer et al., 2019), transcriptomics (e.g., Whelan et al., 2017) restriction-site associated sequencing (e.g., Herrera & Shank, 2016), target-capture (e.g., McFadden et al., 2021 )] de - veloped over the past two decades have…”
MethodHernandez, A. M., & Ryan, J. F. (2019) · doi:10.1101/729103 · Cited by 52 · see citing works
Koutsouveli, V., Cárdenas, P., Santodomingo, N., Marina, A., Morato, E., Rapp, H. T., & Riesgo, A. (2020) · Molecular Biology and Evolution · doi:10.1093/molbev/msaa183 · Cited by 49 · see citing works
Self-citationOrigins and diversification of animal innate immune responses against viral infections
Iwama, R. E., & Moran, Y. (2023) · Nature Ecology & Evolution · doi:10.1038/s41559-022-01951-4 · Cited by 51 · see citing works
Moroz, L. L., Romanova, D. Y., Nikitin, M. A., Sohn, D., Kohn, A. B., Neveu, É., Varoqueaux, F., & Fasshauer, D. (2020) · Scientific Reports · doi:10.1038/s41598-020-69851-w · Cited by 51 · see citing works
Martín-Durán, J. M., & Marlétaz, F. (2020) · Development · doi:10.1242/dev.181081 · Cited by 48 · see citing works
“Science 239, 748-753. doi:10.1126/science.3277277 Giribet, G. (2008).”
InfluentialRecent progress in reconstructing lophotrochozoan (spiralian) phylogeny
Bleidorn, C. (2019) · Organisms Diversity & Evolution · doi:10.1007/s13127-019-00412-4 · Cited by 51 · see citing works
Evolutionary dynamics of transposable elements in bdelloid rotifers
Nowell, R. W., Wilson, C. G., Almeida, P., Schiffer, P. H., Fontaneto, D., Becks, L., Rodríguez, F., Arkhipova, I. R., & Barraclough, T. G. (2021) · eLife · doi:10.7554/elife.63194 · Cited by 46 · see citing works
Vasilikopoulos, A., Balke, M., Kukowka, S., Pflug, J. M., Martín, S., Meusemann, K., Hendrich, L., Mayer, C., Maddison, D. R., Niehuis, O., et al. (2021) · Systematic Entomology · doi:10.1111/syen.12508 · Cited by 46 · see citing works
“Therefore, we chose to filter supermatrix A by applying strategies designed to select conserved alignment sites, reduce the degree of missing data and the potential effects of model violations in phylogenetic reconstructions (Misof et al., 2001; Sharma et al., 2014; Laumer et al., 2019).”
MethodMartínez, A., Bonaglia, S., Domênico, M. D., Fonseca, G., Ingels, J., Jörger, K. M., Laumer, C., Leasi, F., Zeppilli, D., Baldrighi, E., et al. (2025) · Communications Biology · doi:10.1038/s42003-025-07888-1 · Cited by 54 · see citing works
Self-citationA chromosome-scale genome assembly and karyotype of the ctenophore <i>Hormiphora californensis</i>
Schultz, D. T., Francis, W. R., McBroome, J. D., Christianson, L. M., Haddock, S. H. D., & Green, R. E. (2021) · G3 Genes|Genomes|Genetics · doi:10.1093/g3journal/jkab302 · Cited by 35 · see citing works
Orr, R. J. S., Martino, E. D., Ramsfjell, M. H., Gordon, D. P. ., Berning, B., Chowdhury, I. A., Craig, S. F., Cumming, R. L., Figuerola, B., Florence, W. K., et al. (2022) · Science Advances · doi:10.1126/sciadv.abm7452 · Cited by 43 · see citing works
“The continued exploration of the fossil record of bryozoans may yet reveal surprises, as even originations of groups as well studied as land plants continue to astonish (40), and the relationships among metazoan groups remain elusive (41).”
BackgroundMultiple Horizontal Acquisitions of Plant Genes in the Whitefly Bemisia tabaci
Gilbert, C., & Maumus, F. (2022) · Genome Biology and Evolution · doi:10.1093/gbe/evac141 · Cited by 41 · see citing works
Nanglu, K., Cole, S. R., Wright, D. F., & Souto, C. (2022) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12908 · Cited by 37 · see citing works
“Although some data support Xenacoelomorpha as monophyletic and sister to Nephrozoa (Hejnol et al., 2009; Cannon et al., 2016; Rouse et al., 2016; Laumer et al., 2019), there is also evidence that at least the Xenoturbellida may be sister to the Ambulacraria (Paps, Baguñ & Riutort, 2009; Philippe et al.”
BackgroundInfluentialAlternative neural systems: What is a neuron? (Ctenophores, sponges and placozoans)
Moroz, L. L., & Romanova, D. Y. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.1071961 · Cited by 39 · see citing works
“The position of comb jellies as the sister lineage to all Metazoa (Figure 2B) has been supported by independent large-scale phylogenomic studies: this is the Ctenophora-first hypothesis (Whelan et al., 2015; Halanych et al., 2016; Whelan et al., 2017; Laumer et al., 2019; Fernandez and Gabaldon, 2020; Li et al., 2021).”
BackgroundSystematic errors in orthology inference and their effects on evolutionary analyses
Natsidis, P., Kapli, P., Schiffer, P. H., & Telford, M. J. (2021) · iScience · doi:10.1016/j.isci.2021.102110 · Cited by 41 · see citing works
Cool your jets: biological jet propulsion in marine invertebrates
Gemmell, B. J., Dabiri, J. O., Colin, S. P., Costello, J. H., Townsend, J. P., & Sutherland, K. R. (2021) · Journal of Experimental Biology · doi:10.1242/jeb.222083 · Cited by 38 · see citing works
Evolution of DNA Methylation Across Ecdysozoa
Engelhardt, J., Scheer, O., Stadler, P. F., & Prohaska, S. J. (2022) · Journal of Molecular Evolution · doi:10.1007/s00239-021-10042-0 · Cited by 38 · see citing works
“Data for seven species each were retrieved from ENSEMBL Yates et al. (2020) and Laumer et al. Laumer et al. (2019).”
BackgroundMethodInfluentialResolving tricky nodes in the tree of life through amino acid recoding
Giacomelli, M., Rossi, M. E., Lozano-Fernández, J., Feuda, R., & Pisani, D. (2022) · iScience · doi:10.1016/j.isci.2022.105594 · Cited by 40 · see citing works
Romanova, D. Y., Heyland, A., Sohn, D., Kohn, A. B., Fasshauer, D., Varoqueaux, F., & Moroz, L. L. (2020) · Neuroreport · doi:10.1097/wnr.0000000000001436 · Cited by 33 · see citing works
Phylogenomic analyses of mud dragons (Kinorhyncha)
Herranz, M., Stiller, J., Worsaae, K., & Sørensen, M. V. (2021) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2021.107375 · Cited by 37 · see citing works
Self-citationGeographical sampling bias on the assessment of endemism areas for marine meiobenthic fauna
Garraffoni, A. R. S., Sørensen, M. V., Worsaae, K., Domênico, M. D., Sales, L. P., dos Santos, J. P., & Lourenço, A. P. (2021) · Cladistics · doi:10.1111/cla.12453 · Cited by 38 · see citing works
Self-citationMulti‐response phylogenetic mixed models: concepts and application
Halliwell, B., Holland, B. R., & Yates, L. A. (2025) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.70001 · Cited by 34 · see citing works
Mapalo, M., Arakawa, K., Baker, C. M., Persson, D. K., Mirano‐Bascos, D., & Giribet, G. (2020) · G3 Genes Genomes Genetics · doi:10.1534/g3.119.400734 · Cited by 34 · see citing works
Self-citationMoroz, L. L., Sohn, D., Romanova, D. Y., et al. (2020) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2020.04.135 · Cited by 34 · see citing works
Function and Distribution of the Wamide Neuropeptide Superfamily in Metazoans
Williams, E. A. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.00344 · Cited by 34 · see citing works
Nuclear Receptors and Development of Marine Invertebrates
Miglioli, A., Canesi, L., Gomes, I. D. L., Schubert, M., & Dumollard, R. (2021) · Genes · doi:10.3390/genes12010083 · Cited by 34 · see citing works
Neurotransmitters of sleep and wakefulness in flatworms
Omond, S. E. T., Hale, M. W., & Lesku, J. A. (2022) · SLEEP · doi:10.1093/sleep/zsac053 · Cited by 33 · see citing works
“However, more recent studies have challenged this view and place the platyhelminths as the sister to annelids and mollusks in the superphylum Lophotrochozoa [42,43].”
BackgroundThe enigmatic Placozoa part 1: Exploring evolutionary controversies and poor ecological knowledge
Schierwater, B., Osigus, H., Bergmann, T., Blackstone, N. W., Hadrys, H., Hauslage, J., Humbert, P. O., Kamm, K., Kvansakul, M., Wysocki, K., et al. (2021) · BioEssays · doi:10.1002/bies.202100080 · Cited by 32 · see citing works
“The situationwould becomemore complicated— or even highly unlikely—if ctenophores were regarded sister to the other four groups.[65] While modern ctenophores are likely a relict of”
BackgroundSharma, P. P., Ballesteros, J. A., & Santibáñez‐López, C. E. (2021) · Diversity · doi:10.3390/d13110568 · Cited by 33 · see citing works
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 39 · see citing works
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 · see citing works
“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 · see citing works
“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 · see citing works
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 · see citing works
“…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 · see citing works
“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 · see citing works
“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 · see citing works
“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 29 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
“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 · see citing works
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 · see citing works
“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 · see citing works
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 · see citing works
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 · see citing works
“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 26 · see citing works
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 · see citing works
“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 26 · see citing works
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 · see citing works
Wernström, J. V., Gąsiorowski, L., & Hejnol, A. (2022) · EvoDevo · doi:10.1186/s13227-022-00202-8 · Cited by 25 · see citing works
“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 · see citing works
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 25 · see citing works
“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 · see citing works
“…(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 · see citing works
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 23 · see citing works
“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 · see citing works
“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 · see citing works
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 · see citing works
“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 · see citing works
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 · see citing works
Moreland, R. T., Nguyen, A., Ryan, J. F., & Baxevanis, A. D. (2020) · Database · doi:10.1093/database/baaa029 · Cited by 22 · see citing works
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 · see citing works
Self-citationOntano, A. Z., Steiner, H. G., & Sharma, P. P. (2021) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2021.107378 · Cited by 21 · see citing works
- 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 · 2018: 1
- 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
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › 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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