Phylogenetic-signal dissection of nuclear housekeeping genes supports the paraphyly of sponges and the monophyly of Eumetazoa
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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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Some past studies have recovered support for sponge paraphyly at the base of the animal tree.
“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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BackgroundResultInfluentialError, signal, and the placement of Ctenophora sister to all other animals
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“) Taxa Genes Sites Gene occupancy, % Missing data (including gaps), % Full dataset (1) 76 251 81,008 75 40 Certain paralogs removed (2) 76 250 80,735 75 40 Taxa with high LB scores removed (3) 70 250 80,735 75 41 Genes with high LB scores removed (4) 70 231 73,323 75 41 All outgroups except Choanoflagellates removed (…”
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“Based on our previously described phylostratigraphic procedure [1,2], we generated a database of genome sequences divided into 19 phylostrata corresponding to the evolutionary relationships of the major taxa supported by phylogenomic analyses (Figure 1) [15-19].”
BackgroundMethodHigher-level metazoan relationships: recent progress and remaining questions
Edgecombe, G. D., Giribet, G., Dunn, C. W., Hejnol, A., Kristensen, R. M., Neves, R. C., Rouse, G. W., Worsaae, K., & Sørensen, M. V. (2011) · Organisms Diversity & Evolution · doi:10.1007/s13127-011-0044-4 · Cited by 291 · see citing works
“…groups is monophyletic; the only exception in recent literature has been the proposition that Porifera is paraphyletic, giving rise to all other animals (Sperling et al. 2009a, 2010), but this has been contradicted by much larger samples of genes that defend sponge monophyly (Philippe et al. 2009).”
BackgroundMethodInfluentialConstraints on the timescale of animal evolutionary history
Benton, M., Donoghue, P., Vinther, J., Asher, R., Friedman, M., & Near, T. (2015) · Palaeontologia Electronica · doi:10.26879/424 · Cited by 284 · see citing works
“There has been debate concerning the monophyly versus paraphyly of sponges and whether ctenophores are a sister clade to sponges plus Eumetazoa, or whether ctenophores are themselves eumetazoans (Sperling et al., 2009; Nosenko et al., 2013).”
BackgroundDeep metazoan phylogeny: When different genes tell different stories
Nosenko, T., Schreiber, F., Adamska, M., Adamski, M., Eitel, M., Hammel, J., Maldonado, M., Müller, W. E. G., Nickel, M., Schierwater, B., et al. (2013) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2013.01.010 · Cited by 254 · see citing works
“Although attempts to use such markers, for example microRNAs to resolve sponge relationships (Sperling et al., 2010), transposable elements (short interspersed elements, SINEs; Piskurek and Jackson, 2011) and changes in spliceosomal intron positions (NIPs; Lehmann et al., 2012), to resolve early…”
InfluentialCampbell, L. I., Rota‐Stabelli, O., Edgecombe, G. D., Marchioro, T., Longhorn, S. J., Telford, M. J., Philippe, H., Rebecchi, L., Peterson, K. J., & Pisani, D. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1105499108 · Cited by 230 · see citing works
“We next performed a signal-dissection analysis (13, 28), based on the slow-fast technique (27).”
BackgroundMethodSelf-citationThe Genomic and Cellular Foundations of Animal Origins
Richter, D. J., & King, N. (2013) · Annual Review of Genetics · doi:10.1146/annurev-genet-111212-133456 · Cited by 196 · see citing works
Sperling, E. A., & Vinther, J. (2010) · Evolution & Development · doi:10.1111/j.1525-142x.2010.00404.x · Cited by 194 · see citing works
“…the last common ancestor of animals was benthic, sessile, and fed using the WCS (Cavalier-Smith et al. 1996; Collins 1998; Kruse et al. 1998; Borchiellini et al. 2001; Medina et al. 2001; Peterson and Eernisse 2001; Wallberg et al. 2004; Peterson and Butterfield 2005; Sperling et al. 2007, 2009).”
BackgroundMethodInfluentialSelf-citationMetazoan opsin evolution reveals a simple route to animal vision
Feuda, R., Hamilton, S. C., McInerney, J. O., & Pisani, D. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1204609109 · Cited by 186 · see citing works
“Consistently with our results, some of themost thorough analyses to date (20, 21) agree that the Placozoa are the sister group of Neuralia, even though some investigators (22, 30) found different results.”
BackgroundResultSelf-citationSponge Systematics Facing New Challenges
Cárdenas, P., Pérez, T., & Boury‐Esnault, N. (2012) · Advances in marine biology · doi:10.1016/b978-0-12-387787-1.00010-6 · Cited by 193 · see citing works
“This clade has been named “Democlavia” by Sperling et al. (2009); however, this name 154 P. Cárdenas et al. is a nomen nudum because it has not been given a formal Linnaean (rank-based) definition.”
BackgroundResultInfluentialSong, F., Li, H., Jiang, P., Zhou, X. J., Liu, J., Sun, C., Vogler, A. P., & Cai, W. (2016) · Genome Biology and Evolution · doi:10.1093/gbe/evw086 · Cited by 186 · see citing works
SPERLING, E. A., ROBINSON, J. M., PISANI, D., & PETERSON, K. J. (2010) · Geobiology · doi:10.1111/j.1472-4669.2009.00225.x · Cited by 182 · see citing works
“When hexactinellids are excluded and only demosponges analyzed (whose branch lengths for this data set are similar to those of eumetazoans; Sperling et al., 2009), a spicule gap of approximately 140 Myr still remains between the node Haplosclerida + Democlavia and the first appearance of spicules…”
BackgroundMethodResultInfluentialSelf-citationEcdysozoan Mitogenomics: Evidence for a Common Origin of the Legged Invertebrates, the Panarthropoda
Rota-Stabelli, O., Kayal, E., Gleeson, D., Daub, J., Boore, J., Telford, M. J., Pisani, D., Blaxter, M., & Lavrov, D. (2010) · Genome Biology and Evolution · doi:10.1093/gbe/evq030 · Cited by 162 · see citing works
Self-citationRedmond, N. E., Morrow, C. C., THACKER, R. W., Díaz, M. C., Boury‐Esnault, N., Cárdenas, P., Hajdu, E., Lôbo‐Hajdu, G., PICTON, B. E., Pomponi, S. A., et al. (2013) · Integrative and Comparative Biology · doi:10.1093/icb/ict078 · Cited by 167 · see citing works
“2013), whereas others have suggested that Myxospongiae may be the sister group to all other demosponges (Sperling et al. 2009; Bayesian analyses of Hill et al. 2013; Thacker et al. 2013).”
BackgroundThe Evolutionary History of YAP and the Hippo/YAP Pathway
Hilman, D., & Gat, U. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msr065 · Cited by 166 · see citing works
“vectensis is considered to be the closest outgroup to the bilaterians among the known extant taxa (Finnerty et al. 2004; Dunn et al. 2008; Hejnol et al. 2009; Sperling et al. 2009; Ryan et al. 2010).”
BackgroundDeep Phylogeny and Evolution of Sponges (Phylum Porifera)
Wörheide, G., Dohrmann, M., Erpenbeck, D., Larroux, C., Maldonado, M., Voigt, O., Borchiellini, C., & Lavrov, D. V. (2012) · Advances in Marine Biology · doi:10.1016/b978-0-12-387787-1.00007-6 · Cited by 166 · see citing works
“In contrast, marine and freshwater Haplosclerida form a well-supported clade in phylogenetic reconstructions based on nuclear housekeeping genes (Sperling et al., 2009).”
BackgroundInfluentialInvertebrates and Their Roles in Coral Reef Ecosystems
Glynn, P. W., & Enochs, I. C. (2010) · Springer eBooks · doi:10.1007/978-94-007-0114-4_18 · Cited by 163 · see citing works
Redmond, A. K., & McLysaght, A. (2021) · Nature Communications · doi:10.1038/s41467-021-22074-7 · Cited by 139 · see citing works
Early metazoan life: divergence, environment and ecology
Erwin, D. H. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2015.0036 · Cited by 157 · see citing works
Higher-level phylogeny of paraneopteran insects inferred from mitochondrial genome sequences
Li, H., Shao, R., Song, N., Song, F., Jiang, P., Li, Z., & Cai, W. (2015) · Scientific Reports · doi:10.1038/srep08527 · Cited by 154 · see citing works
A basin redox transect at the dawn of animal life
Sperling, E. A., Halverson, G. P., Knoll, A. H., Macdonald, F. A., & Johnston, D. T. (2013) · Earth and Planetary Science Letters · doi:10.1016/j.epsl.2013.04.003 · Cited by 153 · see citing works
“Whether sponges are monophyletic (Philippe et al., 2009) or paraphyletic (Sperling et al., 2009), they are certainly the sister group or grade of all other animals (Philippe et al., 2011).”
BackgroundSelf-citationHill, M. S., Hill, A., Lopez, J. V., Peterson, K. J., Pomponi, S. A., Díaz, M. C., THACKER, R. W., Adamska, M., Boury‐Esnault, N., Cárdenas, P., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0050437 · Cited by 141 · see citing works
“Evolutionary relationships across the most diverse class of Porifera, Demospongiae, have mainly been addressed with three sets of phylogenetic markers: ribosomal DNA sequences [17,42], complete mitochondrial genome sequences [43], and amino acid sequences that code for seven nuclear housekeeping genes [18,44].”
BackgroundMethodResultInfluentialSelf-citationLozano-Fernández, J., Tanner, A. R., Giacomelli, M., Carton, R., Vinther, J., Edgecombe, G. D., & Pisani, D. (2019) · Nature Communications · doi:10.1038/s41467-019-10244-7 · Cited by 137 · see citing works
Self-citationMitogenomics does not resolve deep molluscan relationships (yet?)
Stöger, I., & Schrödl, M. (2012) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2012.11.017 · Cited by 130 · see citing works
“This is consistent with recent large-scaled molecular results confirming that molluscs are non-platyzoan lophotrochozoans (Dunn et al. 2008, Sperling et al. 2009, Pick et al. 2010).”
ResultLudeman, D. A., Farrar, N. R., Riesgo, A., Paps, J., & Leys, S. P. (2014) · BMC Evolutionary Biology · doi:10.1186/1471-2148-14-3 · Cited by 129 · see citing works
“[7-10], some recent phylogenomic analyses place ctenophores more basally [11,12] calling into question our understanding of the evolution of nerves and the ancestral metazoan state.”
BackgroundTalavera, G., & Vila, R. (2011) · BMC Evolutionary Biology · doi:10.1186/1471-2148-11-315 · Cited by 126 · see citing works
Riesgo, A., Andrade, S. C. S., Sharma, P. P., Novo, M., Pérez-Porro, A. R., Vahtera, V., González, V. L., Kawauchi, G. Y., & Giribet, G. (2012) · Frontiers in Zoology · doi:10.1186/1742-9994-9-33 · Cited by 126 · see citing works
“Failure to detect paralogues can lead to misinterpretations of cellular biochemistry, and often inaccuracies in reconstructions of phylogeny and molecular evolution [71,72].”
BackgroundNo longer Demospongiae: Homoscleromorpha formal nomination as a fourth class of Porifera
Gazave, E., Lapébie, P., Ereskovsky, A. V., Vacelet, J., Renard, E., Cárdenas, P., & Borchiellini, C. (2012) · Hydrobiologia · doi:10.1007/s10750-011-0842-x · Cited by 126 · see citing works
“Should the alternative hypothesis that Porifera is paraphyletic (Sperling et al., 2009) gain significant support in the future and the sponge monophyly hypothesis be convincingly refuted, Ho-moscleromorpha and Calcarea would need to change ranks and be reconsidered as potential distinct phyla.”
InfluentialMorrow, C. C., PICTON, B. E., Erpenbeck, D., Boury‐Esnault, N., Maggs, C. A., & Allcock, A. L. (2011) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2011.09.016 · Cited by 122 · see citing works
Lozano-Fernández, J., Giacomelli, M., Fleming, J. F., Chen, A., Vinther, J., Thomsen, P. F., Glenner, H., Palero, F., David, L., Iliffe, T. M., et al. (2019) · Genome Biology and Evolution · doi:10.1093/gbe/evz097 · Cited by 118 · see citing works
Self-citationVinther, J., Sperling, E. A., Briggs, D. E. G., & Peterson, K. J. (2011) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2011.1773 · Cited by 111 · see citing works
Self-citationSPERLING, E. A., PETERSON, K. J., & LAFLAMME, M. (2011) · Geobiology · doi:10.1111/j.1472-4669.2010.00259.x · Cited by 112 · see citing works
“The phylogenetic relationships of extant sponges are contentious; recent molecular phylogenetic studies consistently resolve them as sister to all other animals, but whether they are monophyletic or paraphyletic is under debate (Philippe et al., 2009; Sperling et al., 2009).”
BackgroundSelf-citationEpithelia, an Evolutionary Novelty of Metazoans
Leys, S. P., & Riesgo, A. (2011) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.21442 · Cited by 107 · see citing works
“Recent work has shown that the latter group, Homoscleromorpha, has a BM structure containing type IV collagen (Boute et al., '96), which some say is evidence of a “true epithelium” and which has prompted use of the term “Epitheliozoa” (Boury‐Esnault et al., 2003; Sperling et al., 2009).”
BackgroundEvolutionary origin of gastrulation: insights from sponge development
Nakanishi, N., Sogabe, S., & Degnan, B. M. (2014) · BMC Biology · doi:10.1186/1741-7007-12-26 · Cited by 106 · see citing works
“These approaches, along with resolving the exact order in which these early-branching metazoans diverged from the lineage leading to bilaterians (that is, whether sponges or ctenophores are the sister group to all other animals and whether sponges are monophyletic [34,38]), provide an opportunity to reconstruct the ev…”
BackgroundFernández-Valverde, S. L., Calcino, A., & Degnan, B. M. (2015) · BMC Genomics · doi:10.1186/s12864-015-1588-z · Cited by 101 · see citing works
“However, as recent molecular phylogenomic and phylogenetic analyses both support [1,15] and reject [3,4,16,17] this traditional view, it remains unclear as to whether sponges or ctenophores are the sister group to all other animals and whether poriferans are monophyletic.”
BackgroundModel Systems of Invertebrate Allorecognition
Rosengarten, R. D., & Nicotra, M. L. (2011) · Current Biology · doi:10.1016/j.cub.2010.11.061 · Cited by 101 · see citing works
Origin of animal epithelia: insights from the sponge genome
Fahey, B., & Degnan, B. M. (2010) · Evolution & Development · doi:10.1111/j.1525-142x.2010.00445.x · Cited by 109 · see citing works
“If these sponges are paraphyletic (e.g., Sperling et al. 2009), then these may represent characters that evolved in the clade containing the Calcarea, Homoscleromorpha, and Eumetazoa after it diverged from the lineage comprising the majority of demosponges.”
BackgroundInfluentialCárdenas, P., Xavier, J. R., Réveillaud, J., Schänder, C., & Rapp, H. T. (2011) · PLoS ONE · doi:10.1371/journal.pone.0018318 · Cited by 97 · see citing works
“Democlavia [1,2].”
Gazave, E., Lapébie, P., Renard, E., Vacelet, J., Rocher, C., Ereskovsky, A. V., Lavrov, D. V., & Borchiellini, C. (2010) · PLoS ONE · doi:10.1371/journal.pone.0014290 · Cited by 93 · see citing works
“Among these recent phylogenetic studies based on nuclear sequences, two alternative positions of homoscleromorphs have emerged: (i) closer to eumetazoan than to the other sponges, resulting in the paraphyly of sponges [7,9,11,23,24] or (ii) as the sister group of calcareous sponges within monophyletic Porifera [8,12].”
BackgroundInfluentialGauthier, M. E. A., Pasquier, L. D., & Degnan, B. M. (2010) · Evolution & Development · doi:10.1111/j.1525-142x.2010.00436.x · Cited by 94 · see citing works
“Porifera is considered one of the most ancient extant animal phyla (Borchiellini et al. 2001; Medina et al. 2001; Cavalier-Smith and Chao 2003; Philippe et al. 2009; Sperling et al. 2009; but see Dunn et al. 2008; Schierwater et al. 2009) and thus represents a critical comparative model to gain a general”
BackgroundMitogenomics at the base of Metazoa
Osigus, H.-J., Eitel, M., Bernt, M., Donath, A., & Schierwater, B. (2013) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2013.07.016 · Cited by 89 · see citing works
“The non-monophyly of the Porifera (as seen in all of our analyses) has been observed in several other molecular studies based on nuclear genes, where at least the Homoscleromorpha do not group with other sponges (e.g. Hejnol et al., 2009; Sperling et al., 2009; Nosenko et al., 2013).”
ResultGanot, P., Zoccola, D., Tambutté, É., Voolstra, C. R., Aranda, M., Allemand, D., & Tambutté, S. (2014) · Molecular Biology and Evolution · doi:10.1093/molbev/msu265 · Cited by 84 · see citing works
“Porifera encompass four distinct taxonomic classes (Philippe et al. 2009; Sperling et al. 2009; Erwin et al. 2011) with differences in junction depending on the class.”
BackgroundWindsor, P. J., & Leys, S. P. (2010) · Evolution & Development · doi:10.1111/j.1525-142x.2010.00434.x · Cited by 84 · see citing works
“Porifera, the sponges, are the oldest branching group of animals (Philippe et al. 2009).”
BackgroundResultInfluentialLavrov, D. V., Pett, W., Voigt, O., Wörheide, G., Forget, L., Lang, B. F., & Kayal, E. (2012) · Molecular Biology and Evolution · doi:10.1093/molbev/mss274 · Cited by 83 · see citing works
Luo, C., & Joachim Reitner, A. (2014) · Die Naturwissenschaften · doi:10.1007/s00114-014-1176-0 · Cited by 78 · see citing works
Pisani, D., Feuda, R., Peterson, K., & Smith, A. B. T. (2012) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2011.08.028 · Cited by 79 · see citing works
“site stripping) from the analyses (e.g. Brinkmann and Philippe, 1999; Rodriguez-Ezpeleta et al., 2007; Pisani, 2004; Sperling et al., 2009; Rota-Stabellli et al., 2010).”
BackgroundMethodSelf-citationImproving animal phylogenies with genomic data
Telford, M. J., & Copley, R. R. (2011) · Trends in Genetics · doi:10.1016/j.tig.2011.02.003 · Cited by 75 · see citing works
Adams, E. D. M., Goss, G. G., & Leys, S. P. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015040 · Cited by 74 · see citing works
“The most current phylogenomic analyses of animal relationships place sponges as most basal [1,5,8], but other”
BackgroundThe evolutionary root of flowering plants.
Goremykin, V., Nikiforova, S., Biggs, P., Zhong, B.-J., Delange, P., Martin, W., Woetzel, S., Atherton, R., Mclenachan, P., & Lockhart, P. (2013) · Systematic Biology · doi:10.1093/sysbio/sys070 · Cited by 76 · see citing works
“Less well appreciated is the observation that the sorting of sites based on character state variation or compatibility criteria allows the properties of sites that impact on tree building to be more easily studied (Sperling et al. 2009).”
BackgroundNovel scenarios of early animal evolution--is it time to rewrite textbooks?
Dohrmann, M., & Worheide, G. (2013) · Integrative and Comparative Biology · doi:10.1093/icb/ict008 · Cited by 71 · see citing works
“A number of multi-gene and phylogenomic analyses that did not include Ctenophora found a sistergroup relationship of Cnidaria to Bilateria (Srivastava et al. 2008, 2010; Sperling et al. 2009; Erwin et al. 2011).”
BackgroundInfluentialMolecular paleobiological insights into the origin of the Brachiopoda
Sperling, E., Pisani, D., & Peterson, K. J. (2011) · Evolution & Development · doi:10.1111/j.1525-142x.2011.00480.x · Cited by 70 · see citing works
“Because of the extreme rate variation and presence of homoplasy-prone sites, this dataset is expected to be difficult to analyze and likely to support phylogenetic artifacts even when analyzed using well-fitting, parameter-rich models (see Sperling et al. 2009a).”
BackgroundMethodInfluentialSelf-citationRiutort, M., Álvarez‐Presas, M., Lázaro, E., Solà, E., & Paps, J. (2012) · The International Journal of Developmental Biology · doi:10.1387/ijdb.113441mr · Cited by 70 · see citing works
“Finally, before systematics entered the high-throughput era, a handful of works used concatenated alignments (from 7 to 23 genes) for a significant number of phyla (Bourlat et al., 2008; Paps et al., 2009a; Sperling et al., 2009).”
Automated Removal of Noisy Data in Phylogenomic Analyses
Goremykin, V., Nikiforova, S., & Bininda-Emonds, O. (2010) · Journal of Molecular Evolution · doi:10.1007/s00239-010-9398-z · Cited by 67 · see citing works
“Such files, for instance, (*.plot) are automatically produced by the COMPASS program by Simon Harris (www.ncl.ac.uk/ microbial_eukaryotes/downloads.html) in which compatibility-based sorting approach is implemented (Pisani 2004; Sperling et al. 2009).”
MethodResultInfluentialThe Impact of Paralogy on Phylogenomic Studies – A Case Study on Annelid Relationships
Struck, T. H. (2013) · PLoS ONE · doi:10.1371/journal.pone.0062892 · Cited by 64 · see citing works
“, [1,2,3,4,5,6,7,8,9]) towards the mining of genomic and transcriptomic data using hundreds of genes (e.”
BackgroundMorrow, C. C., Redmond, N. E., PICTON, B. E., THACKER, R. W., Collins, A. G., Maggs, C. A., Sigwart, J. D., & Allcock, A. L. (2013) · Integrative and Comparative Biology · doi:10.1093/icb/ict065 · Cited by 66 · see citing works
“…and 28S rRNA (Borchiellini et al. 2004), 28S rRNA and CO1 (Nichols 2005), 28S rRNA (Holmes and Blanch 2007), complete mitochondrial genomes (Lavrov et al. 2008), and housekeeping genes (Sperling et al. 2009; Hill et al. 2013) are congruent and show Haploscleromorpha as sister to Heteroscleromorpha.”
BackgroundResultInfluentialWhat sponges can tell us about the evolution of developmental processes
Adamska, M., Degnan, B. M., Green, K., & Zwafink, C. (2011) · Zoology · doi:10.1016/j.zool.2010.10.003 · Cited by 65 · see citing works
Schöttner, S., Hoffmann, F., Cárdenas, P., Rapp, H. T., Boëtius, A., & Ramette, A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0055505 · Cited by 65 · see citing works
“The tree topology represents a synthesis of phylogenetic reconstructions from [66,74–75], showing the twelve sponge species from eight different sponge families targeted in this study.”
BackgroundRoure, B., & Philippe, H. (2011) · BMC Evolutionary Biology · doi:10.1186/1471-2148-11-17 · Cited by 64 · see citing works
“This hypothesis predicts Echinodermata Malacostraca Diptera Metatheria Primates Laurasiatheria Crocodylidae Aves Squamata Serpentes Caudata Actinopterygii Anura Porifera Cnidaria 0.1 1.0 1.0 0.96 0.97 1.0 0.83 0.62 1.0 0.76 0.94 0.94 Bi lat er ia Ve rte br ata Mammalia Sauria Amphibia Pancrustacea Figure 3 Topology in…”
BackgroundInfluentialMinxiao, W., Song, S., Li, C., & Shen, X. (2011) · BMC Genomics · doi:10.1186/1471-2164-12-73 · Cited by 64 · see citing works
“However, analyses performed with only characters carrying a moderate evolutionary rate or with the CAT + mtArt, which has been confirmed as an effective model to overcome the effects of Long Branch Attraction (LBA) [68], consistently resolved a monophyletic Branchiopoda clade.”
InfluentialRedmond, N. E., Raleigh, J., van Soest, R. W. M., Kelly, M., Travers, S. A. A., Bradshaw, B., Vartia, S., Stephens, K. M., & McCormack, G. P. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024344 · Cited by 64 · see citing works
“data is consistent with a monophyletic Haplosclerida [14].”
ResultEreskovsky, A. V., Renard, E., & Borchiellini, C. (2012) · Development Genes and Evolution · doi:10.1007/s00427-012-0399-3 · Cited by 62 · see citing works
Rivera, A. S., Hammel, J. U., Haen, K. M., Danka, E. S., Cieniewicz, B., Winters, I. P., Posfai, D., Wörheide, G., Lavrov, D. V., Knight, S. W., et al. (2011) · BMC Biotechnology · doi:10.1186/1472-6750-11-67 · Cited by 61 · see citing works
“Among the non-bilaterian animals, recent utilization of phylogenomics has increased our understanding of metazoan relationships [1-5].”
BackgroundOrigin and Evolution of Laminin Gene Family Diversity
Fahey, B., & Degnan, B. M. (2012) · Molecular Biology and Evolution · doi:10.1093/molbev/mss060 · Cited by 61 · see citing works
“…with the fact that basal lamina–like structures have not been observed in demosponges via electron microscopy (Leys et al. 2009), with the exception of homoscleromorph sponges, which are now thought to represent a lineage distinct from other demosponges (Philippe et al. 2009; Sperling et al. 2009).”
BackgroundNakov, T., Ruck, E. C., Galachyants, Y., Spaulding, S. A., & Theriot, E. C. (2014) · Phycologia · doi:10.2216/14-002.1 · Cited by 60 · see citing works
“Although accommodating ASRV is always recommended, how to best model this variation is an area of active research (Sperling et al. 2009; Cummins &McInerney 2011; Stabelli et al. 2013; Rajan 2013).”
BackgroundAshworth, M. P., Nakov, T., & Theriot, E. C. (2013) · Journal of Phycology · doi:10.1111/jpy.12131 · Cited by 57 · see citing works
Mallatt, J. M., Craig, C. W., & Yoder, M. J. (2012) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2012.05.016 · Cited by 53 · see citing works
“Hypothesis testing with rRNA data rejects the traditional, morphology-based idea that the homoscleromorph sponge, Oscarella, is a demosponge (Table 4, Hypothesis 15), and developmental evidence now upholds this rejection (Boury-Esnault et al., 2003; Kober and Nichols, 2007; Sperling et al., 2009a).”
BackgroundResultInfluentialDemosponge EST Sequencing Reveals a Complex Genetic Toolkit of the Simplest Metazoans
Harcet, M., Roller, M., Ćetković, H., Perina, D., Wiens, M., Müller, W. E. G., & Vlahoviček, K. (2010) · Molecular Biology and Evolution · doi:10.1093/molbev/msq174 · Cited by 52 · see citing works
“There is an ongoing debate on the molecular phylogeny aspects of basal metazoans (Dohrmann et al. 2008; Srivastava et al. 2008; Philippe et al. 2009; Sperling et al. 2009), and although we did not address this issue directly, we hope that the data provided in this paper will provide further evidence for understanding…”
BackgroundThe rise and fall of TRP-N, an ancient family of mechanogated ion channels, in Metazoa
Schüler, A., Schmitz, G., Reft, A., Özbek, S., Thurm, U., & Bornberg-Bauer, E. (2015) · Genome Biology and Evolution · doi:10.1093/gbe/evv091 · Cited by 51 · see citing works
“Note that this interpretation is independent of whether sponges form a monophyletic or paraphyletic group (Collins 2002; Jackson et al. 2007; Sperling et al. 2009; Erwin et al. 2011) but places Placozoa as the outmost group within all other Metazoa, and sponges as an outgroup to this common clade…”
BackgroundInferring the ancestral sexuality and reproductive condition in sponges (Porifera)
Riesgo, A., Novo, M., Sharma, P. P., Peterson, M., Maldonado, M., & Giribet, G. (2013) · Zoologica Scripta · doi:10.1111/zsc.12031 · Cited by 51 · see citing works
“Sponge paraphyly has commonly been reported when using ribosomal (e.g. Borchiellini et al. 2001, 2004), nuclear housekeeping (e.g. Sperling et al. 2009) and mitochondrial markers (e.g. Lavrov et al. 2008).”
BackgroundInfluentialHolton, T. A., & Pisani, D. (2010) · Genome Biology and Evolution · doi:10.1093/gbe/evq016 · Cited by 51 · see citing works
“Although lack of unambiguous morphological support for Ecdysozoa persists as a moot point, in the light of overwhelming molecular evidence and lack of morphological evidence conclusively discrediting Ecdysozoa, is it now finally time to shed the notion of Coelomata?”
BackgroundMethodResultInfluentialSelf-citationA review on deep molluscan phylogeny: old markers, integrative approaches, persistent problems
Schrödl, M., & Stöger, I. (2014) · Journal of Natural History · doi:10.1080/00222933.2014.963184 · Cited by 50 · see citing works
“This concept called Neotrochozoa is supported by some molecular studies, e.g. using housekeeping genes (Peterson et al. 2008, 2009; Sperling et al. 2009) or EST data (Kocot et al. 2011) with, however, still limited taxon sampling.”
BackgroundMethodAn integrated view of precambrian eumetazoan evolution
Davidson, E. H., & Erwin, D. H. (2009) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2009.74.042 · Cited by 48 · see citing works
“Differences in taxon sampling appear to have been a major reason for these divergent results (Sperling et al. 2009a).”
BackgroundResultThe Root of Flowering Plants and Total Evidence
Goremykin, V. V., Nikiforova, S. V., Cavalieri, D., Pindo, M., & Lockhart, P. J. (2015) · Systematic Biology · doi:10.1093/sysbio/syv028 · Cited by 47 · see citing works
‘Stromatolites’ built by sponges and microbes – a new type of Phanerozoic bioconstruction
Luo, C., & Joachim Reitner, A. (2015) · Lethaia · doi:10.1111/let.12166 · Cited by 47 · see citing works
A Simple and Accurate Method for Rogue Taxon Identification
Aberer, A. J., & Stamatakis, A. (2011) · IEEE International Conference on Bioinformatics and Biomedicine (BIBM) · doi:10.1109/bibm.2011.70 · Cited by 46 · see citing works
Polyphyly of the genus Axinella and of the family Axinellidae (Porifera: Demospongiaep)
Gazave, E., Carteron, S., Chenuil, A., Richelle-Maurer, E., Boury‐Esnault, N., & Borchiellini, C. (2010) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2010.05.028 · Cited by 46 · see citing works
Recent Advances and Unanswered Questions in Deep Molluscan Phylogenetics*
Kocot, K. M. (2013) · American Malacological Bulletin · doi:10.4003/006.031.0112 · Cited by 47 · see citing works
Qu, X., Jin, J., Chaw, S., Li, D.-Z., & Yi, T. (2017) · Scientific Reports · doi:10.1038/srep41005 · Cited by 44 · see citing works
Understanding Animal Evolution: The Added Value of Sponge Transcriptomics and Genomics
Renard, E., Leys, S. P., Wörheide, G., & Borchiellini, C. (2018) · BioEssays · doi:10.1002/bies.201700237 · Cited by 41 · see citing works
Belinky, F., Szitenberg, A., Goldfarb, I., Feldstein, T., Wörheide, G., Ilan, M., & Huchon, D. (2012) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2012.02.008 · Cited by 40 · see citing works
“…approaches, such as EST projects (e.g., Dunn et al., 2008; Philippe et al., 2009; Pick et al., 2010); (2) the sequencing of specific genomic DNA markers (e.g., Borchiellini et al., 1998; Erpenbeck et al., 2005b); and (3) the sequencing of specific cDNA markers (Sperling et al., 2007, 2009).”
BackgroundMethodDiversity of sponge mitochondrial introns revealed by cox 1sequences of Tetillidae
Szitenberg, A., Rot, C., Ilan, M., & Huchon, D. (2010) · BMC Evolutionary Biology · doi:10.1186/1471-2148-10-288 · Cited by 39 · see citing works
“The latter result contradicts the current view that sponges are either monophyletic [25] or that homoscleromorphs are closer to cnidarians [26].”
ResultA trophic framework for animal origins
Mills, D. B., & Canfield, D. E. (2016) · Geobiology · doi:10.1111/gbi.12216 · Cited by 38 · see citing works
Degnan, B. M., Adamska, M., Richards, G. S., Larroux, C., Leininger, S., Bergum, B., Calcino, A., Taylor, K., Nakanishi, N., & Degnan, B. M. (2015) · Springer eBooks · doi:10.1007/978-3-7091-1862-7_4 · Cited by 38 · see citing works
Oxygen and Early Animal Evolution
Xiao, S. (2014) · Treatise on Geochemistry · doi:10.1016/b978-0-08-095975-7.01310-3 · Cited by 31 · see citing works
Fortunato, S. A. V., Adamski, M., & Adamska, M. (2015) · Marine Genomics · doi:10.1016/j.margen.2015.07.008 · Cited by 31 · see citing works
DeBiasse, M. B., & Hellberg, M. E. (2015) · Ecology and Evolution · doi:10.1002/ece3.1381 · Cited by 29 · see citing works
“Nuclear protein-coding genes have been employed rarely in sponges (Sperling et al. 2009; Hill et al. 2013; DeBiasse et al. 2014), but given their fast rates (relative to COI) and the increasing ease of next generation data collection, nuclear loci hold promise for future phylogeographic and phylogenetic studies in spo…”
BackgroundGermer, J., Mann, K., Wörheide, G., & Jackson, D. J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0140100 · Cited by 29 · see citing works
“Recent studies using molecular phylogenetic analyses, transcriptomic and genomic data either confirm [14–16] or reject [17–20] the view of sponges as the sister group to all other animals.”
Carbonaceous preservation of Cambrian hexactinellid sponge spicules
Harvey, T. H. P. (2010) · Biology Letters · doi:10.1098/rsbl.2010.0377 · Cited by 29 · see citing works
Phylogenetic Signal Dissection Identifies the Root of Starfishes
Feuda, R., & Smith, A. B. T. (2015) · PLoS ONE · doi:10.1371/journal.pone.0123331 · Cited by 27 · see citing works
“The comparison of phylogenies obtained using differently fitting substitution models and different partitions has previously been used to explore the influence of non-phylogenetic signal on phylogenetic analyses [27, 29, 41–43].”
MethodFleming, J. F., Feuda, R., Roberts, N. W., & Pisani, D. (2020) · Genome Biology and Evolution · doi:10.1093/gbe/evaa015 · Cited by 25 · see citing works
“Ctenophora possesses sequences that share a common ancestor with the bilaterian ciliary opsins, and the position of the ciliary opsins in the minimal opsin tree suggests that the shared ancestor of Ctenophora, Cnidaria, and Bilateria possessed three opsins.”
BackgroundInfluentialSelf-citation
- 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
- 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
- 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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