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Genomic, phylogenetic, and cell biological insights into metazoan origins
Abstract
Over 600 million years ago, the first multicellular metazoans evolved from their single celled ancestors. Although not recorded in the fossil record, the earliest events in metazoan evolution can be inferred by integrating findings from phylogenetics, genomics, and cell biology. Comparisons of choanoflagellate — microeukaryote relatives of metazoans, with sponges (the earliest known metazoans) — reveal genetic innovations associated with metazoan origins. Among these are the evolution of gene families required for cell adhesion and cell signaling, the presence of which catalyzed the evolution of multicellularity and whose functions have since been elaborated to regulate cell differentiation, developmental patterning, morphogenesis, and the functional integration of tissues. The most ancient tissues — differentiated epithelia — are found in sponges and evolved before the origin and diversification of modern phyla.
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“This suggests that the similarities between choanocytes and choanoflagellates were inherited from a common ancestor and that the choanocytebased feeding mode, as retained by sponges, is likely ancestral to all animals (29).”
From Oxygen requirements of the earliest animals (2014) · cites this paper as [29]
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1 retracted
RETRACTED ARTICLE: TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics
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RetractedMrBayes 3: Bayesian phylogenetic inference under mixed models
Ronquist, F., & Huelsenbeck, J. P. (2003) · Bioinformatics · doi:10.1093/bioinformatics/btg180 · Cited by 29,194
Initial sequencing and analysis of the human genome
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The genetical theory of natural selection
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Relaxed Phylogenetics and Dating with Confidence
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Murzin, A. G., Brenner, S. E., Hubbard, T., & Chothia, C. (1995) · Journal of Molecular Biology · doi:10.1016/s0022-2836(05)80134-2 · Cited by 6,435
The Wnt Signaling Pathway in Development and Disease
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Flagged first, then by citations
4 of the 1066 references couldn’t be matched to a known paper.
Research works printed but not linked: 108
- Amthor,, 2003, Geology, 10.1130/0091-7613(2003)031〈0431:EOCANA〉2.0.CO;2 · DOI
- Arduini,, 1981, Megaderaion sinemuriense, a new fossil enteropneust of the Sinemurian., Atti della Societa Italiana de Scienze Naturale e del Museo Civico di Storia Naturale de Milano
- Arenas-Mena,, 2000, Development
- Arendt,, 2004, Gastrulation
- Aruga,, 2007, BMC Evolutionary Biology
- Bateson,, 1884, Quarterly Journal of Microscopical Science
- Bateson,, 1885, Quarterly Journal of Microscopical Science
- Bengtson,, 1994, Early life on Earth. Nobel Symposium No. 84
- Bengtson,, 2000, Teasing fossils out of shales with cameras and computers., Palaeontologia Electronica
- Bengtson,, 2002, The fossil record of predation. The Paleontological Society Papers
- Bengston,, 2006, Evolving form and function: fossils and development. Proceedings of a symposium honoring Adolf Seilacher for his contributions to paleontology in celebration of his 80th birthday
- Blake,, 2005, Implications of a new Early Ordovician asteroid (Echinodermata) for the phylogeny of asterozoans., Journal of Paleontology, 10.1666/0022-3360(2005)079〈0395:IOANEO〉2.0.CO;2 · DOI
- Boveri,, 1899, Festschrift für C. v. Kupffer
- Bowring,, 2003, Geochronological constraints on terminal Neoproterozoic events and the rise of metazoans., Geophysical Research Abstracts
- Brakefield,, 2009, Emerging model organisms: a laboratory manual
- Briggs,, 1995, Fossils of the Burgess Shale
- Brusca,, 1990, Invertebrates
- Brusca,, 2003, Invertebrates
- Butterfield,, 1990, Paleobiology
- Carroll,, 2005, From DNA to diversity: molecular genetics and the evolution of animal design
- Casali,, 2001, Development
- Cerfontaine,, 1906, Archives de Biologie
- Conway, 1998, The crucible of creation
- Coyne,, 2004, Speciation
- Darwin,, 1859, On the origin of species
- Dautert,, 1929, Zoologische Jahrbücher, Abteilung für Anatomie und Ontogenie der Tiere
- Derelle, R. (2007) L'apport des Cténaires à la compréhension de l'évolution des Métazoaires: positionnement par la phylogénomique et recherche de gènes de développement chez Pleurobrachia pileus. Doctoral thesis. Université de Pierre et Marie Curie, Paris (unpublished).
- Dohle,, 1997, Are the insects more closely related to the crustaceans than to the myriapods?, Entomologica Scandinavica
- Dohle,, 2001, Are the insects terrestrial crustaceans? A discussion of some new facts and arguments and the proposal of a proper name ‘Tetraconata’ for the monophyletic unit Crustacea + Hexapoda., Annales de la Societé Entomologique de France
- Economou, A.D. (2008) Phylogenetic and developmental studies of the evolution of an insect novelty. PhD thesis, University College London.
- Eernisse,, 2004, Assembling the tree of life
- Evans,, 2008, BMC Evolutionary Biology
- Fioroni,, 1979, Phylogenetische Abänderungen der Gastrula bei Mollusken., Zeitschrift fur Zoologische Systematik und Evolutionsforschung
- Funch,, 1996, Journal of Morphology, 10.1002/(SICI)1097-4687(199612)230:3〈231::AID-JMOR1〉3.0.CO;2-H · DOI
- Gehling,, 2005, Evolving form and function: fossils and development: proceedings of a symposium honoring Adolf Seilacher for his contributions to paleontology, in celebration of his 80th birthday
- Gerhart,, 1998, Warkany lecture: signaling pathways in development., Teratology
- Gerhart,, 1997, Cells, embryos, and evolution: toward a cellular and developmental understanding of phenotypic variation and evolutionary adaptability
- Gerould,, 1906, Zoologische Jahrbücher, Abteilung für Anatomie und Ontogenie der Tiere
- Ghiselin,, 1988, The origin of molluscs in the light of molecular evidence., Oxford Surveys in Evolutionary Biology.
- Giribet,, 2007, Zootaxa
- Gosling,, 2008, Experimental taphonomy of lophotrochozoan and deuterostome embryos., Evolution & Development
- Haag,, 2001, From mutants to mechanisms? Assessing the candidate gene paradigm in evolutionary biology., Evolution
- Haeckel,, 1874, Die Gastraea-theorie, die phylogenetische Klassifikation des Tierreichs und die Homologie der Keimblätter., Jenaische Zeitschrift für Naturwissenschaften
- Heider,, 1909, Zoologischer Anzeiger
- Helfenbein,, 2004, Molecular Biology and Evolution, 10.1093/molbev/msh011 · DOI
- Hertwig,, 1880, Über die Entwicklungsgeschichte der Sagitten., Jenaische Zeitschrift für Medizin und Naturwissenschaft
- Hibberd,, 1975, Journal of Cell Science
- Hughes,, 2000, Development
- Hyman,, 1940, The invertebrates
- Hyman,, 1951, The invertebrates. Vol. 2. Platyhelminthes and Rhynchocoela
- Hyman,, 1959, The invertebrates. Vol. 5. Smaller coelomate groups
- Inoue,, 1958, The development and structure of the larva., Japanese Journal of Zoology
- Irish,, 1989, EMBO Journal
- Jackson,, 2006, BMC Genomics
- Jägersten,, 1940, Zur Kenntnis der Morphologie, Entwicklung und Taxonomie der Myzostomida., Nova Acta Regiase Societatis Scientiarum Upsaliensis Ser. 4
- Jägersten,, 1955, On the early phylogeny of the Metazoa: the bilatero-gastrea theory., Zoologiska Bidrag från Uppsala
- Karpov,, 1998, Acta Protozoologica
- Kennedy,, 1998, Two or four Neoproterozoic glaciations?, Geology, 10.1130/0091-7613(1998)026〈1059:TOFNG〉2.3.CO;2 · DOI
- Kennel,, 1885, Arbeiten aus dem Zoologisch-Zootomischen Institut in Würzburg
- Koch,, 2002, European Journal of Entomology
- Kühn,, 1933, Uber die Determination des symmetrie Systems auf dem vorderflugel von Phylogeny., Evolution
- Leuckart,, 1827, Versuch einer naturgemässen Eintheilung der Helminthen
- Lin,, 2006, Historical Biology
- Lüter,, 2000, Ultrastructure of larval and adult setae of Brachiopoda., Zoologischer Anzeiger
- Mattei,, 1987, Les spermatozoïdes des Acanthocéphales et des Myzostomides: Ressemblance et conséquences phylétiques., Comptes Rendus De L'Academie Des Sciences de Paris, Sciences de la Vie
- Mayr,, 1960, The evolution of life
- Norden-Krichmaer,, 2007, BMC Genomics
- Ogasawara,, 1999, Development
- Okai,, 2000, Developmental Dynamics, 10.1002/(SICI)1097-0177(200003)217:3〈309::AID-DVDY9〉3.0.CO;2-2 · DOI
- Peterson,, 1999, Development
- Prum,, 1999, Development and evolutionary origin of feathers., Journal of Experimental Zoology, 10.1002/(SICI)1097-010X(19991215)285:4〈291::AID-JEZ1〉3.0.CO;2-9 · DOI
- Remane,, 1950, Die Entstehung der Metamerie der Wirbellosen., Zoologischer Anzeiger
- Roule,, 1891, Considerations sur l'embranchement des Trochozoaires., Annales des Sciences Naturelle (Zoologie) 7e série
- Rouse,, 2001, Polychaetes
- Rowe,, 2004, Assembling the tree of life
- Runnegar,, 1996, Origin and evolutionary radiation of the Mollusca
- Ruppert,, 1991, Microscopic anatomy of invertebrates, Vol. 4. Aschelminthes
- Ruppert,, 1991, Microscopic anatomy of invertebrates, Vol. 4. Aschelminthes
- Rusten,, 2002, Development
- Salvini-Plawen,, 1980, Phylogenetischer Status und Bedeutung der mesenchymaten Bilateria., Zoologische Jahrbücher, Abteilung für Anatomie und Ontogenie der Tiere
- Salvini-Plawen,, 1996, Origin and evolutionary radiation of the Mollusca
- Saville-Kent,, 1880, A manual of the Infusoria
- Schleip,, 1929, Die Determination der Primitiventwicklung
- Schmitz,, 2001, Genetics
- Scholz,, 1998, International Journal of Developmental Biology
- Sedgwick,, 1885, Quarterly Journal of the Microscopical Society
- Selenka,, 1876, Entwicklung der Holothurien., Zeitschrift für Wissenschaftliche Zoologie
- Slyusarev,, 2003, Zoomorphology
- Smith,, 2004, Assembling the tree of life
- Sørensen, M.V. (2001) On the phylogeny and jaw evolution in Gnathifera. PhD Thesis, University of Copenhagen, Copenhagen.
- Surface,, 1907, Proceedings of the Academy of Natural Sciences Philadelphia
- Tagawa,, 2000, T-Brain expression in the apical organ of hemichordate tornaria larvae suggests its evolutionary link to the vertebrate forebrain., Journal of Experimental Zoology (Molecular Development and Evolution), 10.1002/(SICI)1097-010X(20000415)288:1〈23::AID-JEZ3〉3.0.CO;2-H · DOI
- Telford,, 2003, International Journal of Developmental Biology
- Ulrich,, 1951, Vorschläge zu einer Revision der Großeinteilung des Tierreichs., Verhandlungen der Deutschen Zoologische Gesellschaft, Marburg (1950)
- Valentine,, 2004, On the origin of phyla
- Voronov,, 1998, Development
- Wagner,, 2001, Gastropod phylogenetics: progress, problems, and implications., Journal of Paleontology, 10.1666/0022-3360(2001)075〈1128:GPPPAI〉2.0.CO;2 · DOI
- Westblad,, 1949, Arkiv för Zoologi
- Weygoldt,, 1960, Zoologische Jahrbücher, Abteilung für Anatomie und Ontogenie der Tiere
- Wheeler,, 2004, Assembling the tree of life
- Wiens,, 2006, Evolution
- Wolff,, 1995, Development
- Wolff,, 1998, Development
- Woolley,, 2000, Conserved mechanisms of repair: from damaged single cells to wounds in multicellular tissues., BioEssays, 10.1002/1521-1878(200010)22:10〈911::AID-BIES6〉3.0.CO;2-V · DOI
- Xiao,, 2000, Phosphatized animal embryos from the Neoproterozoic Doushantuo Formation at Weng'An, Guizhou, South China., Journal of Paleontology, 10.1666/0022-3360(2000)074〈0767:PAEFTN〉2.0.CO;2 · DOI
- Yin,, 2004, Acta Palaeontologica Polonica
- Zelinka,, 1891, Zur Entwicklungsgeschichte der Räderthiere nebst Bemerkungen über ihre Anatomie und Biologie., Zeitschrift für Wissenschaftliche Zoologie
- Zigler,, 2003, Evolution
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Metadata
- Authors
- Nichols, S. A., Dayel, M. J., & King, N.
- Venue
- Animal Evolution
- Publisher
- Oxford University PressOxford
- Published
- 2009-08-01
- Pages
- 24-32
- OpenAlex
- W2502404727
- Cited by
- 24
- References
- 1,066
- Citations by year
- 2025: 1 · 2024: 1 · 2022: 1 · 2020: 1 · 2019: 3 · 2018: 1 · 2016: 3 · 2015: 3 · 2014: 3 · 2013: 4 · 2012: 1
- FWCI
- 13.67
- Type
- book chapter
- Language
- en
- Open access
- closed
- Topics
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Protist diversity and phylogeny
- Keywords
- metazoan origin, evolution of multicellularity, choanoflagellates, sponges, cell adhesion genes, gene family evolution, metazoan phylogeny, cell differentiation, morphogenesis
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