Novel scenarios of early animal evolution--is it time to rewrite textbooks?
Abstract
Understanding how important phenotypic, developmental, and genomic features of animals originated and evolved is essential for many fields of biological research, but such understanding depends on robust hypotheses about the phylogenetic interrelationships of the higher taxa to which the studied species belong. Molecular approaches to phylogenetics have proven able to revolutionize our knowledge of organismal evolution. However, with respect to the deepest splits in the metazoan Tree of Life-the relationships between Bilateria and the four non-bilaterian phyla (Porifera, Placozoa, Ctenophora, and Cnidaria)-no consensus has been reached yet, since a number of different, often contradictory, hypotheses with sometimes spectacular implications have been proposed in recent years. Here, we review the recent literature on the topic and contrast it with more classical perceptions based on analyses of morphological characters. We conclude that the time is not yet ripe to rewrite zoological textbooks and advocate a conservative approach when it comes to developing scenarios of the early evolution of animals.
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Traditionally, sponges (Porifera) have been interpreted as the sister group to the remaining animals (Porifera-sister hypothesis).
“Traditionally, sponges have been recognized as the sister group to the remaining animals (the ' Porifera-sister ' hypothesis)”
From Genomic data do not support comb jellies as the sister group to all other animals (2015) · cites this paper as [1]
Cites
Broad phylogenomic sampling improves resolution of the animal tree of life
Dunn, C. W., Hejnol, A., Matus, D. Q., Pang, K., Browne, W. E., Smith, S. A., Seaver, E., Rouse, G. W., Obst, M., Edgecombe, G. D., et al. (2008) · Nature · doi:10.1038/nature06614 · Cited by 1,921 · cited 4× · see citing works
“However, it was demonstrated shortly after its original publication (Dunn et al. 2008) that the ‘‘Ctenophora-first’’ topology resulted from methodological artifacts caused by insufficient sampling of non-bilaterian taxa and inadequate outgroup choice (Pick et al. 2010; see also Philippe et al.…”
BackgroundInfluentialErwin, D. H., Laflamme, M., Tweedt, S. M., Sperling, E. A., Pisani, D., & Peterson, K. J. (2011) · Science · doi:10.1126/science.1206375 · Cited by 1,336 · cited 3× · 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).”
BackgroundPhylogenomics and the reconstruction of the tree of life
Delsuc, F., Brinkmann, H., & Philippe, H. (2005) · Nature Reviews Genetics · doi:10.1038/nrg1603 · Cited by 1,228 · see citing works
The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans
King, N., Westbrook, M. J., Young, S. L., Kuo, A., Abedin, M., Chapman, J., Fairclough, S., Hellsten, U., Isogai, Y., Letunic, I., et al. (2008) · Nature · doi:10.1038/nature06617 · Cited by 1,139 · see citing works
Resolving difficult phylogenetic questions: Why more sequences are not enough
Philippe, H., Brinkmann, H., Lavrov, D. V., Littlewood, D. T. J., Manuel, M., Wörheide, G., & Baurain, D. (2011) · PLoS Biology · doi:10.1371/journal.pbio.1000602 · Cited by 1,129 · see citing works
Self-citationThe Amphimedon queenslandica genome and the evolution of animal complexity
Srivastava, M., Simakov, O., Chapman, J., Fahey, B., Gauthier, M. E. A., Mitros, T., Richards, G. S., Conaco, C., Dacre, M., Hellsten, U., et al. (2010) · Nature · doi:10.1038/nature09201 · Cited by 1,049 · see citing works
Animal evolution: interrelationships of the living phyla
(2012) · Choice Reviews Online · doi:10.5860/choice.50-1469 · Cited by 1,041 · see citing works
The Trichoplax genome and the nature of placozoans
Srivastava, M., Begovic, E., Chapman, J., Putnam, N. H., Hellsten, U., Kawashima, T., Kuo, A., Mitros, T., Salamov, A., Carpenter, M. L., et al. (2008) · Nature · doi:10.1038/nature07191 · Cited by 889 · see citing works
Assessing the root of bilaterian animals with scalable phylogenomic methods
Hejnol, A., Obst, M., Stamatakis, A., Ott, M., Rouse, G. W., Edgecombe, G. D., Martinez, P., Baguñà, J., Bailly, X., Jondelius, U., et al. (2009) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2009.0896 · Cited by 747 · cited 2× · see citing works
“Then, in a landmark phylogenomic study aimed at resolving deep bilaterian relationships, Dunn et al. (2008; see also Hejnol et al. 2009) surprisingly recovered Ctenophora as the sister-group to all remaining Metazoa.”
BackgroundPhylogenomics: The beginning of incongruence?
JEFFROY, O., BRINKMANN, H., DELSUC, F., & PHILIPPE, H. (2006) · Trends in Genetics · doi:10.1016/j.tig.2006.02.003 · Cited by 698 · see citing works
Phylogenomics Revives Traditional Views on Deep Animal Relationships
Philippe, H., Derelle, R., Lopez, P., Pick, K., Borchiellini, C., Boury-Esnault, N., Vacelet, J., Renard, E., Houliston, E., Quéinnec, E., et al. (2009) · Current Biology · doi:10.1016/j.cub.2009.02.052 · Cited by 695 · see citing works
Rare genomic changes as a tool for phylogenetics
Rokas, A., & Holland, P. W. H. (2000) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(00)01967-4 · Cited by 688 · see citing works
The new animal phylogeny: Reliability and implications
Adoutte, A., Balavoine, G., Lartillot, N., Lespinet, O., Prud'homme, B., & de Rosa, R. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.9.4453 · Cited by 512 · see citing works
The New View of Animal Phylogeny
Halanych, K. M. (2004) · Annual Review of Ecology, Evolution, and Systematics · doi:10.1146/annurev.ecolsys.35.112202.130124 · Cited by 489 · see citing works
Estimating metazoan divergence times with a molecular clock
Peterson, K. J., Lyons, J. B., Nowak, K. S., Takacs, C. M., Wargo, M. J., & McPeek, M. A. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0401670101 · Cited by 461 · see citing works
Collins, A. G., Schuchert, P., Marques, A. C., Jankowski, T., Medina, M., & Schierwater, B. (2006) · Systematic Biology · doi:10.1080/10635150500433615 · Cited by 382 · see citing works
Six major steps in animal evolution: Are we derived sponge larvae?
Nielsen, C. (2008) · Evolution & Development · doi:10.1111/j.1525-142x.2008.00231.x · Cited by 343 · cited 1× · see citing works
“…Sperling et al. (2007) attracted quite some attention, and inspired some authors to develop elaborate novel scenarios of the early evolution of animals; for example, Nielsen (2008) hypothesized that the ancestor of Eumetazoa evolved from a progenetic homoscleromorph larva (see also Nielsen 2011).”
BackgroundImproved phylogenomic taxon sampling noticeably affects nonbilaterian relationships
Pick, K. S., Philippe, H., Schreiber, F., Erpenbeck, D., Jackson, D. J., Wrede, P., Wiens, M., Alie, A., Morgenstern, B., Manuel, M., et al. (2010) · Molecular Biology and Evolution · doi:10.1093/molbev/msq089 · Cited by 334 · see citing works
Philippe, H., Delsuc, F., Brinkmann, H., & Lartillot, N. (2005) · Annual Review of Ecology, Evolution, and Systematics · doi:10.1146/annurev.ecolsys.35.112202.130205 · Cited by 306 · see citing works
Higher-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
Schierwater, B., Eitel, M., Jakob, W., Osigus, H.-J., Hadrys, H., Dellaporta, S. L., Kolokotronis, S.-O., & DeSalle, R. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000020 · Cited by 260 · see citing works
Park, E., Hwang, D., Lee, J., Song, J., Seo, T., & Won, Y. (2011) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2011.10.008 · Cited by 256 · see citing works
Deep 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
Self-citationDellaporta, S. L., Xu, A., Sagasser, S., Jakob, W., Moreno, M. A., Buss, L. W., & Schierwater, B. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0602076103 · Cited by 252 · see citing works
Independent evolution of striated muscles in cnidarians and bilaterians
Steinmetz, P. R. H., Kraus, J. E. M., Larroux, C., Hammel, J. U., Amon-Hassenzahl, A., Houliston, E., Wörheide, G., Nickel, M., Degnan, B. M., & Technau, U. (2012) · Nature · doi:10.1038/nature11180 · Cited by 252 · see citing works
Self-citationCollins, A. G. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.26.15458 · Cited by 252 · see citing works
Animal biodiversity: An introduction to higher-level classification and taxonomic richness
Zhang, Z. (2011) · Zootaxa · doi:10.11646/zootaxa.3148.1.3 · Cited by 244 · see citing works
Cnidarian phylogenetic relationships as revealed by mitogenomics
Kayal, E., Roure, B., Philippe, H., Collins, A. G., & Lavrov, D. V. (2013) · BMC Evolutionary Biology · doi:10.1186/1471-2148-13-5 · Cited by 240 · see citing works
Poriferan paraphyly and its implications for Precambrian palaeobiology
Sperling, E. A., Pisani, D., & Peterson, K. J. (2007) · Geological Society, London, Special Publications · doi:10.1144/sp286.25 · Cited by 206 · cited 3× · see citing works
“The first NHP7 analysis including multiple sponge lineages and using character-based, probabilistic reconstruction methods showed strong support for sponge paraphyly, with Homoscleromorpha (represented by a single species) being the sister-group of Eumetazoa (CnidariaþBilateria; Placozoa and Ctenophora were not sample…”
BackgroundMethodInfluentialMolecular phylogeny of choanoflagellates, the sister group to Metazoa
Carr, M., Leadbeater, B. S. C., Hassan, R., Nelson, M., & Baldauf, S. L. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0801667105 · Cited by 205 · see citing works
Sperling, E. A., Peterson, K. J., & Pisani, D. (2009) · Molecular Biology and Evolution · doi:10.1093/molbev/msp148 · Cited by 172 · cited 8× · 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).”
BackgroundInfluentialDeep 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
Self-citationMy favorite animal, <i>Trichoplax adhaerens</i>
Schierwater, B. (2005) · BioEssays · doi:10.1002/bies.20320 · Cited by 161 · see citing works
Ryan, J. F., Pang, K., Program, N. C. S., Mullikin, J. C., Martindale, M. Q., & Baxevanis, A. D. (2010) · EvoDevo · doi:10.1186/2041-9139-1-9 · Cited by 160 · cited 3× · see citing works
“…of Ctenophora can be considered: (1) as the sister-group to the remaining Epitheliozoa (Pick et al. 2010), consistent with the ‘‘ParaHoxozoa’’ hypothesis (Ryan et al. 2010) and (2) as sister-group to Cnidaria (Philippe et al. 2009), consistent with the Eumetazoa and Coelenterata hypotheses.”
BackgroundResultPhylogeny and evolution of glass sponges (Porifera, Hexactinellida)
Dohrmann, M., Janussen, D., Reitner, J., Collins, A. G., & Wörheide, G. (2008) · Systematic Biology · doi:10.1080/10635150802161088 · Cited by 143 · cited 2× · see citing works
“non-bilaterian species in an independent phylogenomic dataset (150 proteins) originally established by Dunn et al. (2008). Most recently, Nosenko et al.”
BackgroundSelf-citationThe phylogenetic position of the comb jellies (Ctenophora) and the importance of taxonomic sampling
Wållberg, A., Thollesson, M., Farris, J. S., & Jondelius, U. (2004) · Cladistics · doi:10.1111/j.1096-0031.2004.00041.x · Cited by 141 · see citing works
No 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
Comparative Genomics of Large Mitochondria in Placozoans
Signorovitch, A. Y., Buss, L. W., & Dellaporta, S. L. (2007) · PLoS Genetics · doi:10.1371/journal.pgen.0030013 · Cited by 115 · see citing works
Placozoa – no longer a phylum of one
Voigt, O., Collins, A. G., Pearse, V. B., Pearse, J. S., Ender, A., Hadrys, H., & Schierwater, B. (2004) · Current Biology · doi:10.1016/j.cub.2004.10.036 · Cited by 113 · cited 1× · see citing works
“These comprise the Porifera (sponges), Cnidaria (corals, jellyfish, and their kin), Ctenophora (comb jellies), and the enigmatic, monospecific (but see Voigt et al. 2004; Guidi et al. 2011) Placozoa (Trichoplax adhaerens).”
BackgroundPlacozoa Are Not Derived Cnidarians: Evidence from Molecular Morphology
Ender, A., & Schierwater, B. (2003) · Molecular Biology and Evolution · doi:10.1093/molbev/msg018 · Cited by 111 · see citing works
Epithelia, 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
On the molecular phylogeny of sponges (Porifera)*
Erpenbeck, D., & Wörheide, G. (2007) · Zootaxa · doi:10.11646/zootaxa.1668.1.10 · Cited by 100 · see citing works
Pett, W., Ryan, J. F., Pang, K., Mullikin, J. C., Martindale, M. Q., Baxevanis, A. D., & Lavrov, D. V. (2011) · Mitochondrial DNA · doi:10.3109/19401736.2011.624611 · Cited by 91 · see citing works
Perspectives in Animal Phylogeny and Evolution
Minelli, A. (2008) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198566205.001.0001 · Cited by 89 · see citing works
Wang, X., & Lavrov, D. V. (2006) · Molecular Biology and Evolution · doi:10.1093/molbev/msl167 · Cited by 83 · see citing works
Group I-intron trans-splicing and mRNA editing in the mitochondria of placozoan animals
Burger, G., Yan, Y., Javadi, P., & Lang, B. F. (2009) · Trends in Genetics · doi:10.1016/j.tig.2009.07.003 · Cited by 77 · see citing works
Improving 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
Maxwell, E. K., Ryan, J. F., Schnitzler, C. E., Browne, W. E., & Baxevanis, A. D. (2012) · BMC Genomics · doi:10.1186/1471-2164-13-714 · Cited by 58 · see citing works
Kohn, A. B., Citarella, M. R., Kocot, K. M., Bobkova, Y. V., Halanych, K. M., & Moroz, L. L. (2012) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2011.12.009 · Cited by 53 · see citing works
Dayraud, C., Alié, A., Jager, M., Chang, P., Le Guyader, H., Manuel, M., & Quéinnec, E. (2012) · BMC Evolutionary Biology · doi:10.1186/1471-2148-12-107 · Cited by 49 · see citing works
Animal evolution: genomes, fossils, and trees
Telford, M. J. (2010) · Choice Reviews Online · doi:10.5860/choice.47-5016 · Cited by 48 · see citing works
Ultrastructural analyses support different morphological lineages in the phylum placozoa Grell, 1971
Guidi, L., Eitel, M., Cesarini, E., Schierwater, B., & Balsamo, M. (2011) · Journal of Morphology · doi:10.1002/jmor.10922 · Cited by 45 · see citing works
MicroRNAs and metazoan phylogeny: big trees from little genes
Sperling, E. A., & Peterson, K. J. (2009) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199549429.003.0015 · Cited by 44 · see citing works
石柠 (2006) · 写作：中学版 · Cited by 42 · see citing works
Phylogenetic position of Placozoa based on large subunit (LSU) and small subunit (SSU) rRNA genes
da Silva, F. B., Muschner, V. C., & Bonatto, S. L. (2007) · Genetics and Molecular Biology · doi:10.1590/s1415-47572007000100022 · Cited by 42 · see citing works
Large-Scale Parsimony Analysis of Metazoan Indels in Protein-Coding Genes
Belinky, F., Cohen, O., & Huchon, D. (2009) · Molecular Biology and Evolution · doi:10.1093/molbev/msp263 · Cited by 37 · see citing works
Cnidarian milestones in metazoan evolution
Boero, F., Schierwater, B., & Piraino, S. (2007) · Integrative and Comparative Biology · doi:10.1093/icb/icm041 · Cited by 35 · see citing works
Robinson, J. M., Sperling, E. A., Bergum, B., Adamski, M., Nichols, S., Adamska, M., & Peterson, K. J. (2013) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.22485 · Cited by 27 · see citing works
The Diploblast-Bilateria sister hypothesis
Schierwater, B., Kolokotronis, S., Eitel, M., & DeSalle, R. (2009) · Communicative & Integrative Biology · doi:10.4161/cib.2.5.8763 · Cited by 26 · see citing works
Riesgo, A., & Maldonado, M. (2009) · Biological Journal of the Linnean Society · doi:10.1111/j.1095-8312.2009.01214.x · Cited by 22 · see citing works
An even “newer” animal phylogeny
DeSalle, R., & Schierwater, B. (2008) · BioEssays · doi:10.1002/bies.20842 · Cited by 19 · see citing works
Chasing the urmetazoon: Striking a blow for quality data?
Osigus, H., Eitel, M., & Schierwater, B. (2012) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2012.05.028 · Cited by 18 · see citing works
Pennisi, E. (2003) · Science · doi:10.1126/science.300.5626.1694 · Cited by 18 · see citing works
A New Look at Some Old Animals
Blackstone, N. W. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000007 · Cited by 17 · see citing works
The Early Evolution of Hox Genes: A Battle of Belief?
Schierwater, B., & Kamm, K. (2010) · Advances in experimental medicine and biology · doi:10.1007/978-1-4419-6673-5_5 · Cited by 12 · see citing works
Nervous System May Have Evolved Twice
Pennisi, E. (2013) · Science · doi:10.1126/science.339.6118.391-a · Cited by 11 · see citing works
Near intron pairs and the metazoan tree
Lehmann, J., Stadler, P. F., & Krauss, V. (2013) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2012.11.012 · Cited by 11 · see citing works
Genome reveals comb jellies' ancient origin
Maxmen, A. (2013) · Nature · doi:10.1038/nature.2013.12176 · Cited by 3 · see citing works
Byrum, C. A. (2012) · EvoDevo · doi:10.1186/2041-9139-3-5 · Cited by 1 · see citing works
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Error, signal, and the placement of Ctenophora sister to all other animals
Whelan, N. V., Kocot, K. M., Moroz, L. L., & Halanych, K. M. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1503453112 · Cited by 331 · see citing works
Genomic data do not support comb jellies as the sister group to all other animals
Pisani, D., Pett, W., Dohrmann, M., Feuda, R., Rota-Stabelli, O., Philippe, H., Lartillot, N., & Wörheide, G. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1518127112 · Cited by 319 · see citing works
Self-citationImproved Modeling of Compositional Heterogeneity Supports Sponges as Sister to All Other Animals
Feuda, R., Dohrmann, M., Pett, W., Philippe, H., Rota-Stabelli, O., Lartillot, N., Wörheide, G., & Pisani, D. (2017) · Current Biology · doi:10.1016/j.cub.2017.11.008 · Cited by 291 · see citing works
Self-citationDating early animal evolution using phylogenomic data
Dohrmann, M., & Wörheide, G. (2017) · Scientific Reports · doi:10.1038/s41598-017-03791-w · Cited by 217 · see citing works
Self-citationThe hidden biology of sponges and ctenophores
Dunn, C. W., Leys, S. P., & Haddock, S. H. D. (2015) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2015.03.003 · Cited by 212 · see citing works
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King, N., & Rokas, A. (2017) · Current Biology · doi:10.1016/j.cub.2017.08.054 · Cited by 144 · see citing works
Leininger, S., Adamski, M., Bergum, B., Guder, C., Liu, J., Laplante, M., Bråte, J., Hoffmann, F., Fortunato, S., Jordal, S., et al. (2014) · Nature Communications · doi:10.1038/ncomms4905 · Cited by 136 · see citing works
Oxygen and animal evolution: Did a rise of atmospheric oxygen "trigger" the origin of animals?
Mills, D. B., & Canfield, D. E. (2014) · BioEssays · doi:10.1002/bies.201400101 · Cited by 138 · see citing works
Scientists, G. C. O. (2013) · Journal of Heredity · doi:10.1093/jhered/est084 · Cited by 115 · see citing works
Iten, H. V., Marques, A. C., Leme, J. D. M., Pacheco, M. L. A. F., & Simões, M. G. (2014) · Palaeontology · doi:10.1111/pala.12116 · Cited by 114 · see citing works
Ehrlich, H., Kaluzhnaya, O. V., Brunner, E., Tsurkan, M. V., Ereskovsky, A. V., Ilan, M., Tabachnick, K. R., Bazhenov, V. V., Paasch, S., Kammer, M., et al. (2013) · Journal of Structural Biology · doi:10.1016/j.jsb.2013.06.015 · Cited by 98 · see citing works
Ganot, 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
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Feuda, R., Rota-Stabelli, O., Oakley, T. H., & Pisani, D. (2014) · Genome Biology and Evolution · doi:10.1093/gbe/evu154 · Cited by 70 · see citing works
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Green, D. R., & Fitzgerald, P. (2016) · Current Biology · doi:10.1016/j.cub.2016.05.023 · Cited by 81 · 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
Simion, P., Bekkouche, N., Jager, M., Quéinnec, E., & Manuel, M. (2015) · Zoology · doi:10.1016/j.zool.2014.06.004 · Cited by 46 · see citing works
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Deppisch, P., Helfrich‐Förster, C., & Senthilan, P. R. (2022) · Genes · doi:10.3390/genes13091613 · Cited by 42 · see citing works
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Juravel, K., Porras, L., Höhna, S., Pisani, D., & Wörheide, G. (2023) · PLoS ONE · doi:10.1371/journal.pone.0282444 · Cited by 38 · see citing works
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Americus, B., Lotan, T., Bartholomew, J. L., & Atkinson, S. D. (2020) · International Journal for Parasitology · doi:10.1016/j.ijpara.2020.04.012 · Cited by 34 · see citing works
Parry, L. A., Lerosey‐Aubril, R., Weaver, J. C., & Ortega‐Hernández, J. (2021) · iScience · doi:10.1016/j.isci.2021.102943 · Cited by 34 · see citing works
Sponges as models to study emergence of complex animals
Adamska, M. (2016) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2016.05.026 · Cited by 33 · see citing works
The 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
Histories of molecules: Reconciling the past
O’Malley, M. A. (2015) · Studies in History and Philosophy of Science Part A · doi:10.1016/j.shpsa.2015.09.002 · Cited by 33 · see citing works
Of early animals, anaerobic mitochondria, and a modern sponge
Mentel, M., Roettger, M., Leys, S. P., Tielens, A. G. M., & Martin, W. F. (2014) · BioEssays · doi:10.1002/bies.201400060 · Cited by 32 · see citing works
Mussini, G., & Dunn, F. S. (2023) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.13014 · 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
Insights into the evolution of digestive systems from studies of Trichoplax adhaerens
Smith, C. L., & Mayorova, T. D. (2019) · Cell and Tissue Research · doi:10.1007/s00441-019-03057-z · Cited by 28 · see citing works
Ferrier, D. E. K. (2016) · Briefings in Functional Genomics · doi:10.1093/bfgp/elv056 · Cited by 28 · see citing works
Germer, J., Mann, K., Wörheide, G., & Jackson, D. J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0140100 · Cited by 29 · 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
Schenkelaars, Q., Quintero, O. A., Hall, C. P., Fierro‐Constaín, L., Renard, E., Borchiellini, C., & Hill, A. (2016) · Developmental Biology · doi:10.1016/j.ydbio.2016.02.026 · Cited by 28 · see citing works
Just, J., Kristensen, R. M., & Olesen, J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0102976 · Cited by 25 · see citing works
Koutsouveli, 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
Rho Family of Ras-Like GTPases in Early-Branching Animals
Beljan, S., Bosnar, M. H., & Ćetković, H. (2020) · Cells · doi:10.3390/cells9102279 · Cited by 23 · see citing works
Ahrens, J. B., Santos, H. G. D., & Siltberg-Liberles, J. (2016) · Molecular Biology and Evolution · doi:10.1093/molbev/msw092 · Cited by 23 · see citing works
Differentiation and Transdifferentiation of Sponge Cells
Adamska, M. (2018) · Results and problems in cell differentiation · doi:10.1007/978-3-319-92486-1_12 · Cited by 23 · see citing works
Myxozoan Affinities and Route to Endoparasitism
Okamura, B., & Gruhl, A. (2015) · Springer eBooks · doi:10.1007/978-3-319-14753-6_2 · Cited by 20 · see citing works
Sponge cell cultivation: Optimization of the model Petrosia ficiformis (Poiret 1789)
Pozzolini, M., Mussino, F., Cerrano, C., Scarfı̀, S., & Giovine, M. (2014) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/j.jembe.2014.02.004 · Cited by 16 · see citing works
My Oldest Sister Is a Sea Walnut?
Rokas, A. (2013) · Science · doi:10.1126/science.1248424 · Cited by 14 · see citing works
Evolution, Origins and Diversification of Parasitic Cnidarians
Okamura, B., & Gruhl, A. (2021) · Topics in geobiology · doi:10.1007/978-3-030-42484-8_4 · Cited by 14 · see citing works
Cohen, B. L., Kaulfuss, A., & Lüter, C. (2014) · Zoological Journal of the Linnean Society · doi:10.1111/zoj.12121 · Cited by 12 · see citing works
Setiawan, E., CHODIANTORO, M. R., INSANY, G. F., Subagio, I. B., Dewi, N. K., & Muzaki, F. K. (2021) · Biodiversitas Journal of Biological Diversity · doi:10.13057/biodiv/d220803 · Cited by 9 · see citing works
Lopez, J. V. (2019) · Springer eBooks · doi:10.1007/978-94-024-1612-1_8 · Cited by 7 · see citing works
Davies, N. J., Krusche, P., Tauber, E., & Ott, S. (2015) · BMC Evolutionary Biology · doi:10.1186/s12862-015-0499-6 · Cited by 7 · see citing works
Analysis of the interaction between human RITA and Drosophila Suppressor of Hairless
Brockmann, B., Mastel, H., Oswald, F., & Maier, D. (2014) · Hereditas · doi:10.1111/hrd2.00074 · Cited by 7 · see citing works
Hejnol, A. (2014) · Nature · doi:10.1038/nature13340 · Cited by 6 · see citing works
Symbiogeny and the Evolution of Tissues: The Hypothesis
Shostak, S. (2015) · Biological Systems Open Access · doi:10.4172/2329-6577.1000127 · Cited by 6 · see citing works
Yun, H., Janussen, D., Zhang, X., & Joachim Reitner, A. (2023) · Lethaia · doi:10.18261/let.56.3.5 · Cited by 5 · see citing works
Identification and Characterization of Novel Conserved Domains in Metazoan Zic Proteins
Tohmonda, T., Kamiya, A., Ishiguro, A., Iwaki, T., Fujimi, T. J., Hatayama, M., & Aruga, J. (2018) · Molecular Biology and Evolution · doi:10.1093/molbev/msy122 · Cited by 5 · see citing works
Setiawan, E., Muzaki, F. K., & Ashuri, N. M. (2018) · NICHE Journal of Tropical Biology · doi:10.14710/niche.1.2.19-29 · Cited by 4 · see citing works
Schlosser, G. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.24136-9 · Cited by 3 · see citing works
Shostak, S. (2015) · Cell & Developmental Biology · doi:10.4172/2168-9296.1000155 · Cited by 3 · see citing works
Emerging Cnidarian Models for the Study of Epithelial Polarity
Rathbun, L. I., Everett, C. A., & Bergstralh, D. T. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.854373 · Cited by 3 · see citing works
Origin of Metazoan Patterning Systems and the Role of ANTP ‐Class Homeobox Genes
Thomas‐Chollier, M., & Martı́nez, P. (2016) · Encyclopedia of Life Sciences · doi:10.1002/9780470015902.a0022852.pub2 · Cited by 3 · see citing works
Yun, H., Zhang, X., Brock, G. A., Han, J., Li, L., Pan, B., Li, G., & Joachim Reitner, A. (2025) · Communications Biology · doi:10.1038/s42003-025-08655-y · Cited by 3 · see citing works
Science Behind, Around, and After Trees
Stach, T. (2015) · BioScience · doi:10.1093/biosci/biu205 · Cited by 2 · see citing works
Evolutionary Origins of Stemness
Ivanović, Z., & Vlaski‐Lafarge, M. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-800540-8.00010-7 · Cited by 1 · see citing works
Leitz, T. (2015) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199682201.003.0005 · Cited by 1 · see citing works
Insights from Sponge Transcriptomes & Physiology about the Early Evolution of Nervous Systems
Farrar, N. R. (2014) · ERA: Education and Research Archive (University of Alberta) · doi:10.7939/r3183485q
Um panorama atual sobre a filogenia de Metazoa: conflitos e concordâncias
Andrade, M. P., Ferreira, F. D. S., de França, T. C., Sampronha, S., Santos, D., Silva, P. K. R., Carrijo, T. F., Nunes, F. R. C., & de Oliveira, O. M. P. (2021) · Revista da Biologia · doi:10.11606/revbio.21.07.10.2021
Hou, X.-G., Siveter, D. J., Siveter, D. J., Aldridge, R. J., Cong, P.-Y., Gabbott, S. E., Ma, X., Purnell, M. A., & Williams, M. (2017) · Wiley eBooks · doi:10.1002/9781118896372.refs
Um panorama atual sobre a filogenia de Metazoa: conflitos e concordâncias
Andrade, M. P., Ferreira, F. D. S., de França, T. C., Sampronha, S., Santos, D., Silva, P. K. R., Carrijo, T. F., Nunes, F. R. C., & de Oliveira, O. M. P. (2021) · Revista da Biologia · doi:10.11606/issn.1984-5154.v21p1-13
Nervous system evolution : insights from the sea urchin
Formery, L. (2019) · theses.fr (ABES) · doi:10.70675/146c0b8aza71az47ecza2c7zc12baf0f5794
Kuncoro, P. N., Aunurohim, Aunurohim, Ashuri, N. M., Priyono, D. S., & Setiawan, E. (2026) · Acta Limnologica Brasiliensia · doi:10.1590/s2179-975x1626
- Authors
- Dohrmann, M., & Worheide, G.
- Affiliations
- Bayerische Staatssammlung für Paläontologie und Geologie (DE)
- Venue
- Integrative and Comparative Biology
- Publisher
- Oxford University Press (OUP)
- Published
- 2013-03-28
- Volume
- 53
- Issue
- 3
- Pages
- 503-511
- ISSN
- 1540-7063 (ISSN-L)
- 1557-7023
- OpenAlex
- W2124743553
- Cited by
- 71
- References
- 69
- Citations by year
- 2026: 1 · 2025: 1 · 2023: 3 · 2022: 3 · 2021: 7 · 2020: 5 · 2019: 3 · 2018: 4 · 2017: 6 · 2016: 6 · 2015: 16 · 2014: 13 · 2013: 3
- FWCI
- 1.47
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Integrative and Comparative Biology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- American Microscopical Society
- Topics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protist diversity and phylogeny
- Keywords
- early animal evolution, metazoan phylogeny, sponges, Placozoa, Ctenophora, Cnidaria, Bilateria, molecular phylogeny, morphological characters, evolutionary scenarios, textbook revision
- MeSH terms
- Animals, Biological Evolution, Invertebrates, Phylogeny, Species Specificity
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