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Phylogenetic-Signal Dissection of Nuclear Housekeeping Genes Supports the Paraphyly of Sponges and the Monophyly of Eumetazoa
Open accessAbstract
The relationships at the base of the metazoan tree have been difficult to robustly resolve, and there are several different hypotheses regarding the interrelationships among sponges, cnidarians, ctenophores, placozoans, and bilaterians, with each hypothesis having different implications for the body plan of the last common ancestor of animals and the paleoecology of the late Precambrian. We have sequenced seven nuclear housekeeping genes from 17 new sponges, bringing the total to 29 species analyzed, including multiple representatives of the Demospongiae, Calcarea, Hexactinellida, and Homoscleromorpha, and analyzed a data set also including six nonmetazoan outgroups and 36 eumetazoans using a variety of phylogenetic methods and evolutionary models. We used leaf stability to identify rogue taxa and investigate their effect on the support of the nodes in our trees, and we identified clades most likely to represent phylogenetic artifacts through the comparison of trees derived using different methods (and models) and through site-stripping analyses. Further, we investigated compositional heterogeneity and tested whether amino acid composition bias affected our results. Finally, we used Bayes factors to compare our results against previously published phylogenies. All our maximum likelihood (ML) and Bayesian analyses find sponges to be paraphyletic, with all analyses finding three extant paraphyletic sponge lineages, Demospongiae plus Hexactinellida, Calcarea, and Homoscleromorpha. All but one of our ML and Bayesian analyses support the monophyly of Eumetazoa (here Cnidaria + Bilateria) and a sister group relationship between Placozoa (here Trichoplax adhaerens) and Eumetazoa. Bayes factors invariably provide decisive support in favor of poriferan paraphyly when compared against either a sister group relationship between Porifera and Cnidaria or with a monophyletic Porifera with respect to a monophyletic Eumetazoa. Although we were able to recover sponge monophyly using our data set, this was only possible under unrealistic evolutionary models, if poorly performing phylogenetic methods were used, or in situations where the potential for the generation of tree reconstruction artifacts was artificially exacerbated. Everything considered, our data set does not provide any support for a monophyletic Diploblastica (here Placozoa + Cnidaria + Porifera) and suggests that a monophyletic Porifera may be better seen as a phylogenetic artifact.
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“Similarly, and more pertinent to the root of the animal phylogeny, some past studies have recovered support for sponge paraphyly at the base of the animal tree8,68.”
From Evidence for sponges as sister to all other animals from partitioned phylogenomics with mixture models and recoding (2021) · cites this paper as [68]
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Citations
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Items 101–171 of 171
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InfluentialPhylomitogenomics bolsters the high-level classification of Demospongiae (phylum Porifera)
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BackgroundMorrow, C. C., Cárdenas, P., Boury‐Esnault, N., PICTON, B. E., McCormack, G. P., van Soest, R. W. M., Collins, A. G., Redmond, N. E., Maggs, C. A., Sigwart, J. D., et al. (2019) · Zoological Journal of the Linnean Society · doi:10.1093/zoolinnean/zlz017 · Cited by 20
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BackgroundChasing the urmetazoon: Striking a blow for quality data?
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BackgroundPhylogenetic structure in African HIV-1 subtype C revealed by selective sequential pruning
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“Their apparently primitive cellular characteristics and organisational simplicity are confirmed by many molecular phylogenies [3, 4], with only a few recent papers, suggesting either ctenophores [5] or placozoans [6] to have branched earlier, and both results being convincingly rejected by others due to artefacts [7].”
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Macroevolution of Animal Body Plans: Is There Science after the Tree?
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“Resolving sponges as a paraphyletic grade at the base of Metazoa allows the inference that eumetazoans evolved from ancestors with a sponge-like body plan (Sperling et al. 2009).”
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Self-citationRespiration kinetics and allometric scaling in the demosponge Halichondria panicea
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Reviewing the Ediacaran fossils of the Long Mynd, Shropshire
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“However, molecular surveys claiming a close relationship between these groups periodically appear (Sperling et al., 2009; Hill et al., 2013; Schuster et al., 2017).”
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“The alternative, a route to eumetazoans through the sponge body plan (see Sperling et al. 2009, 2010 for the case based on the paraphyly of the living sponges) seems more difficult, because the sponge bodyplan (although not the genome) must then be lost.”
BackgroundMolecular and morphological congruence of three new cryptic Neopetrosia spp. in the Caribbean
Vicente, J., Ríos, J. A., Zea, S., & Toonen, R. J. (2019) · PeerJ · doi:10.7717/peerj.6371 · Cited by 10
No longer Demospongiae: Homoscleromorpha formal nomination as a fourth class of Porifera
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“Sponges have been recovered as a paraphyletic grade in some molecular phylogenetic studies (e.g. Borchiellini et al. 2001; Sperling et al. 2009; Erwin et al. 2011), which would render this feeding strategy ancestral to all metazoans.”
BackgroundSperling, E. A., Rosengarten, R. D., Moreno, M. A., & Dellaporta, S. L. (2011) · Hydrobiologia · doi:10.1007/s10750-011-0879-x · Cited by 9
“We focused on the genus Aplysina Nardo 1834 (Demospongiae, Verongida, Aplysinidae), which is a genus of aspiculate sponges within the Myxospongiae or ‘‘G2’’ clade (Borchiellini et al., 2004; Nichols, 2005; Lavrov et al., 2008; Sperling et al., 2009).”
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Chen, A., Müller, W. E. G., Hou, X., & Xiao, S. (2014) · Palaeoworld · doi:10.1016/j.palwor.2014.11.006 · Cited by 8
Invertebrate and Vertebrate Collagens
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“2009) or paraphyly (Sperling et al. 2009) of the four major sponge lineages, the first steps in type IV collagen gene evolution could follow two scenarios (Fig.”
BackgroundTesting Phylogenetic Stability with Variable Taxon Sampling
Powell, C. L. E., & Battistuzzi, F. U. (2022) · Methods in molecular biology · doi:10.1007/978-1-0716-2691-7_8 · Cited by 7
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“…chambers (Efremova & Papkovskaya, 1980; Sukhodolskaya & Papkovskaya, 1985; Paulus & Weissenfels, 1986; Paulus, 1989; Weissenfels, 1989) but whether the suborder Spongillina belongs in the order Haplosclerida has yet to be conclusively determined (Redmond et al., 2007; Sperling et al., 2009).”
BackgroundChoanoflagellates: Perspective on the Origin of Animal Multicellularity
Fairclough, S. R. (2015) · Advances in marine genomics · doi:10.1007/978-94-017-9642-2_5 · Cited by 7
“Both miRNAs and piRNAs are inferred to have been present in stem Bilateria and deep sequencing of small RNAs from early branching animals has indicated that miRNAs and piRNAs have been present since the evolution of animals (Grimson et al. 2008; Sperling et al. 2009).”
BackgroundEdiacaran sponges, animal biomineralization, and skeletal reefs
Xiao, S. (2020) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.2014393117 · Cited by 6
Records of a new spongelike group in the Riphean biota
German, T. N., & Podkovyrov, V. N. (2012) · Paleontological Journal · doi:10.1134/s0031030112030069 · Cited by 7
“However, to date, different points of view on the origin of multicellular animals and on the Ven dian–Cambrian expansion of Metazoa have been developed (Ivanov, 1968; Fedonkin, 1987, 2003; Deg nan and Degnan, 2006; Gaidos et al., 2007; Sperling et al., 2009; etc.).”
BackgroundAnderson, B. M., Pisani, D., Miller, A. I., & Peterson, K. J. (2011) · Geology · doi:10.1130/g32413.1 · Cited by 6
Self-citationPutting placozoans on the (phylogeographic) map
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The rise of genomics sheds light on the dawn of animals
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“Given the antiquity of the basal metazoan phyla, class-level representation of the Cnidaria and Porifera (assuming monophyly; cf. Sperling et al. 2009) is required to better understand the evolutionary relationships of these phyla.”
Sponges as sensitive animals: sensory systems and energetics of filtration in demosponges
Ludeman, D. A. (2015) · ERA: Education and Research Archive (University of Alberta) · doi:10.7939/r3rx93n3m · Cited by 4
Emerging Cnidarian Models for the Study of Epithelial Polarity
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“Phylogenetic analysis based on a supermatrix of inferred amino acid sequences Bayesian phylogenetic analysis based on concatenated amino-acid sequences of mitochondrial protein genes from 120 species of demosponges produced a tree of demosponge relationships consistent with the four major groups suggested by Borchiell…”
BackgroundInfluentialRobust PhylogeneticsPreprint
Liu, Q., Minh, B. Q., Lanfear, R., Charleston, M., Richards, S. A., & Holland, B. R. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.04.01.646540 · Cited by 2
Early evolution of the LIM homeobox gene family
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“Although early metazoan phylogeny remains controversial [2-5], among the living phyla sponges were likely the first animal group to diverge, followed by the subsequent branching of placozoans, and then cnidarians/bilaterians.”
Background林, 日., Botting, J. P., & 袁, 训. (2014) · Chinese Science Bulletin (Chinese Version) · doi:10.1360/csb2014-59-9-796 · Cited by 1
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Kinetid in larval cells of Spongillida (Porifera: Demospongiae): tracing the ancestral traits
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“But data in some studies imply a joining of the Spongillida and Haplosclerida branches (Sperling et al. 2009; Hill et al. 2013).”
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Insights from Sponge Transcriptomes & Physiology about the Early Evolution of Nervous Systems
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Schenkelaars, Q. (2015) · theses.fr (ABES) · doi:10.70675/678ad9b4z0094z499dzb772z9ec414b0d23e
Ruiz, C. A. (2017) · doi:10.70675/d389148dza9afz4ed0z99e9z176e9ea8b2dc
“2010) et groupe frère des Eumétazoaires (Sperling et al. 2009).”
Metadata
- Authors
- Sperling, E. A., Peterson, K. J., & Pisani, D.
- Affiliations
- Dartmouth College (US)
- National University of Ireland, Maynooth (IE)
- Venue
- Molecular Biology and Evolution
- Publisher
- Oxford University Press (OUP)
- Published
- 2009-07-13
- Volume
- 26
- Issue
- 10
- Pages
- 2261-2274
- ISSN
- 0737-4038 (ISSN-L)
- 1537-1719
- OpenAlex
- W2113314205
- Semantic Scholar
- 31400635e4a3264203bc633bd9a328f8638b1161
- Cited by
- 172
- References
- 70
- Citations by year
- 2025: 2 · 2024: 1 · 2023: 2 · 2022: 3 · 2021: 4 · 2020: 3 · 2019: 8 · 2018: 4 · 2017: 5 · 2016: 6 · 2015: 21 · 2014: 14 · 2013: 21 · 2012: 19
- FWCI
- 20.20
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Molecular Biology and Evolution (publishedVersion)
- PubMed (publishedVersion)
- Maynooth University ePrints and eTheses Archive (Maynooth University) (acceptedVersion)
- Explore Bristol Research (submittedVersion)
- Bristol Research (University of Bristol) (submittedVersion)
- Funders
- Smithsonian Tropical Research Institute
- 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 › Protist diversity and phylogeny
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Marine Sponges and Natural Products
- Keywords
- sponge phylogeny, Placozoa, Trichoplax adhaerens, Cnidaria, Demospongiae, Hexactinellida, calcareous sponges, Homoscleromorpha, phylogenetic signal, compositional heterogeneity, body plan evolution
- MeSH terms
- Animals, Bayes Theorem, Cell Nucleus, Models, Genetic, Phylogeny, Porifera, Selection, Genetic, Likelihood Functions, Genes, Essential, Placozoa
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