The DOI matches its Crossref record; 39 of the 41 references it cites were found in a registry or an index.
Origin of the metazoan phyla: Molecular clocks confirm paleontological estimates
Open accessAbstract
The time of origin of the animal phyla is controversial. Abundant fossils from the major animal phyla are found in the Cambrian, starting 544 million years ago. Many paleontologists hold that these phyla originated in the late Neoproterozoic, during the 160 million years preceding the Cambrian fossil explosion. We have analyzed 18 protein-coding gene loci and estimated that protostomes (arthropods, annelids, and mollusks) diverged from deuterostomes (echinoderms and chordates) about 670 million years ago, and chordates from echinoderms about 600 million years ago. Both estimates are consistent with paleontological estimates. A published analysis of seven gene loci that concludes that the corresponding divergence times are 1,200 and 1,000 million years ago is shown to be flawed because it extrapolates from slow-evolving vertebrate rates to faster-evolving invertebrate rates, as well as in other ways.
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“Depending on the proteins, calibration points and rate substitution models used, these estimates range from 600 to 1200 Mya (Wray et al., 1996;Ayala et al., 1998;Bromham et al., 1998;Gu, 1998;Cutler, 2000).”
From The last common bilaterian ancestor (2002) · cites this paper as Ayala et al., 1998
In the citing paper
“Our data suggest that, inconsistent with most molecular clock estimates but consistent with paleontological predictions (e.g., refs. 13 and 14), bilaterians do not have a significant precambrian evolutionary history.”
From Estimating metazoan divergence times with a molecular clock (2004) · cites this paper as [13]
In the citing paper
“The combination of a rate constancy test with high resolution of long DNA sequences (two data sets totaling over 7,000 bp), use of a wide range of taxa and fossil dates (rather than reliance on a single calibration rate), and a maximum likelihood analysis makes this method more reliable than previous molecular dating techniques (11).”
From Testing the Cambrian explosion hypothesis by using a molecular dating technique (1998) · cites this paper as [23]
In the citing paper
“Molecular phylogenies based on sequence comparisons of protein domains shared by all bilaterians suggest that the time of divergence of these proteins may extend back to 600–1,200 million years (megaannuum; Ma) ago (11–16).”
From Precambrian animal diversity: Putative phosphatized embryos from the Doushantuo Formation of China (2000) · cites this paper as [12]
In the citing paper
“Among the limitations noted are nucleotide compositional bias, among site rate variation, and heterogeneous rates of evolution across lineages (12–16).”
From Evaluating hypotheses of basal animal phylogeny using complete sequences of large and small subunit rRNA (2001) · cites this paper as [15]
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Vleugels, R., Verlinden, H., & Broeck, J. (2014) · Neurotransmitter · doi:10.14800/nt.314 · Cited by 99
“Since these events predate the estimated divergence of protostomes and deuterostomes about 600 to 650 million years ago ([66]), the invertebrate and vertebrate serotonergic systems are supposed to own roughly the same main receptor classes ([61,67]).”
BackgroundMetazoan Relationships on the Basis of 18S rRNA Sequences: A Few Years Later…
Winnepenninckx, B., de Peer, Y. V., & Backeljau, T. (1998) · American Zoologist · doi:10.1093/icb/38.6.888 · Cited by 83
Early Evolution of the Bilateria
Hausdorf, B. (2000) · Systematic Biology · doi:10.1080/10635150050207438 · Cited by 83
“, 1999) compare only the rates in two lineages at one time and have low statistical power (Ayala et al., 1998).”
BackgroundResultInfluentialOrigins, Lineage-Specific Expansions, and Multiple Losses of Tyrosine Kinases in Eukaryotes
Shiu, S., & Li, W. (2004) · Molecular Biology and Evolution · doi:10.1093/molbev/msh077 · Cited by 85
Shaul, S., & Graur, D. (2002) · Gene · doi:10.1016/s0378-1119(02)00851-x · Cited by 77
Zaugg, M., & SCHAUB, M. C. (2003) · Journal of Muscle Research and Cell Motility · doi:10.1023/a:1026021430091 · Cited by 77
“These results suggest that PC is a mechanism of tissue protection that preceded the evolution of marine and terrestrial vertebrate life 300– 400 million years ago in the mid paleozoic (Ayala et al., 1998).”
BackgroundA methane fuse for the Cambrian explosion: carbon cycles and true polar wander
Kirschvink, J. L., & Raub, T. D. (2003) · Comptes Rendus Géoscience · doi:10.1016/s1631-0713(03)00011-7 · Cited by 77
“Molecular-clock analyses have not yet converged on a consistent and robust divergence date: estimates for the main divergence of lineages range from Paleoproterozoic to Vendian time [4,7,12,13,23, 30,37,45,72,88,94,101,112,113].”
Álvaro, J. J., Ahlberg, P., Babcock, L. E., Bordonaro, O. L., Choi, D. K., Cooper, R. A., Ergaliev, G. K., Gapp, I. W., Pour, M. G., Hughes, N. C., et al. (2013) · Geological Society London Memoirs · doi:10.1144/m38.19 · Cited by 77
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“aegypti, lower Te values were obtained (Additional File 4); these values are better compatible with more recent divergence dates which, in turn, are consistent with the Cambrian explosion [61,62].”
ResultBerbee, M. L., Carmean, D., & Winka, K. (2000) · Molecular Phylogenetics and Evolution · doi:10.1006/mpev.2000.0835 · Cited by 74
“They introduced the stimulating (but controversial; see Wray et al., 1996; Morris, 1997; Ayala et al., 1998) argument that the lack of metazoan resolution reflected rapid radiation.”
BackgroundNei, M. (2002) · Journal of Heredity · doi:10.1093/jhered/93.3.157 · Cited by 73
“(Ayala et al. 1998; Feng et al. 1997; Gu 1998; Kumar and Hedges 1998; O’hUigin and Li 1992).”
Chernikova, D., Motamedi, S., Csürös, M., Koonin, E. V., & Rogozin, I. B. (2011) · Biology Direct · doi:10.1186/1745-6150-6-26 · Cited by 72
“In particular, these estimates point to a relatively late divergence of the major bilaterian lineages closely predating the Cambrian explosion and to a (relatively) young LECA, with the primary radiation of eukaryotes occurring between 1.0-1.4 Gya.”
ResultInfluentialSrinivasan, J., Dillman, A. R., Macchietto, M. G., Heikkinen, L., Lakso, M., Fracchia, K. M., Antoshechkin, I. A., Mortazavi, A., Wong, G., & Sternberg, P. W. (2013) · Genetics · doi:10.1534/genetics.112.148809 · Cited by 71
“…that origi-nated during the Precambrian or Cambrian explosion over 500 million years ago and have subsequently evolved exquisite adaptations, allowing them to inhabit nearly all ecological niches (Malakhov and Hope 1994; Ayala and Rzhetsky 1998; Blaxter et al. 1998; Rodriguez-Trelles et al. 2002).”
BackgroundMolecular Evidence for Precambrian Origin of Amelogenin, the Major Protein of Vertebrate Enamel
Delgado, S., Casañe, D., Bonnaud, L., Laurin, M., Sire, J., & Girondot, M. (2001) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a003760 · Cited by 70
“…for divergence dates and is more suitable for our study than a method that uses external divergence dates, such as the date of divergence between protostomians and deuterostomians, which is highly controversial (Ayala and Rzhetsky 1998; Bromham et al. 1998; Gu 1998; Bromham and Hendy 2000).”
MethodToll-like receptors: an overview from invertebrates to vertebrates
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Major Transitions in Animal Evolution: A Developmental Genetic Perspective
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“, 1996), but this conclusion has been challenged by Ayala et al. (1998). The consensus view at present seems to be that the Cambrian explosion was a real phenomenon, reflecting a time of rapid diversification of body plans.”
BackgroundEvolutionary and Molecular Facts Link the WWC Protein Family to Hippo Signaling
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“Observed evolutionary rates may be time-scale dependent; both morpholog ical (Gingerich, 1984) and molecular (Ayala et al., 1998) rates measured on relatively short time scales are commonly higher than those derived using longer time intervals.”
BackgroundEvolution of the CD163 family and its relationship to the bovine gamma delta T cell co-receptor WC1
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“The validity of this conclusion has already been questioned from a number of standpoints (e.g., Conway Morris, 1997; Nikoh et al., 1997; Ayala et al., 1998) with estimates revised to between ca.”
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“Cyanobacterial fossils date to 2.9 billion years ago (NoVke et al., 2003), whereas nematodes most likely arose slightly prior to or during the Cambrian explosion (Ayala and Rzhetsky, 1998; Rodriguez-Trelles et al., 2002; Wray et al., 1996).”
BackgroundInfluentialBromham, L. D., & Woolfit, M. (2004) · Systematic Biology · doi:10.1080/10635150490522278 · Cited by 66
Some Unusual Small-Subunit Ribosomal RNA Sequences of Metazoans
Giribet, G., & Wheeler, W. C. (2001) · American Museum Novitates · doi:10.1206/0003-0082(2001)337 · Cited by 63
A paleontological perspective of vertebrate origin
Shu, D. (2003) · Chinese Science Bulletin · doi:10.1007/bf03187041 · Cited by 62
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“…with mitochondrial gene sequences, the average estimated time of the deuterostome-protostome split derived from the analysis of 14 nuclear genes in Ayala et al. (1998) is 780 million years, which is roughly comparable to, although somewhat lower than, estimates derived by Feng et al. (1997) and…”
BackgroundMethodResultInfluentialComparative Immune Systems in Animals
Yuan, S., Tao, X., Huang, S., Chen, S., & Xu, A. (2013) · Annual Review of Animal Biosciences · doi:10.1146/annurev-animal-031412-103634 · Cited by 64
“Because amphioxus and sea urchin represent the oldest extant lineages for the chordate phylum and deuterostome superphylum, respectively, expansion of the innate immune–related genesmay have been a commonoccurrence in ancient deuterostomes 500–600Mya, implying that the immune systems in the ancestors of vertebrates we…”
BackgroundBaker, M. E. (2005) · Integrative and Comparative Biology · doi:10.1093/icb/45.1.172 · Cited by 59
“Multicellular animals appeared on earth about 700 to 1,000 million years ago (Ayala et al., 1998; Valentine et al., 1999; Budd and Jensen, 2000).”
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Borda, E., Oceguera-Figueroa, A. F., & Siddall, M. E. (2007) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2007.09.006 · Cited by 57
“The diversification of Annelida has been attributed to the Cambrian explosion (Ayala et al., 1998; Rousset et al., 2007) with the oldest known fossils dating back to the Silurian (>400 Mya; Eriksson et al.”
BackgroundRedox properties and evolution of human glutaredoxins
Sagemark, J., Elgán, T. H., Bürglin, T. R., Johansson, C., Holmgren, A., & Berndt, K. D. (2007) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.21416 · Cited by 58
“Dotted lines connect positions of observed (37-94) and proposed (87-110 and 87-113) disulfide bonds in some homologous members.”
BackgroundConserved genomic organisation of Group B Sox genes in insects.
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One or Three Cambrian Radiations?
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Whole genome duplications and expansion of the vertebrate GATA transcription factor gene family
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“Deuterostomes include several major groups of invertebrate and vertebrate animals (Figure 1) [9-17].”
BackgroundMolecular dates for the “cambrian explosion”: The influence of prior assumptions.
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“However, a wide range of molecular dating studies have suggested that the major lineages of animals arose long Downloaded from https://academic.oup.com/sysbio/article-abstract/54/4/672/2843005 by guest on 27 July 2018 before the Cambrian, at over 630 Mya (e.g., Wray et al., 1996; Ayala et al., 1998; Bromham et al., 19…”
BackgroundInfluentialKnigge, T., LeBlanc, G. A., & Ford, A. T. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.587608 · Cited by 55
Molecular clocks and the early evolution of metazoan nervous systems
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Verlinden, H., Vleugels, R., Zels, S., Dillen, S., Lenaerts, C., Crabbé, K., Spit, J., & Broeck, J. V. (2014) · Advances in insect physiology · doi:10.1016/b978-0-12-417010-0.00003-3 · Cited by 50
Can fast early rates reconcile molecular dates with the Cambrian explosion?
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“Molecular studies have been criticized for failing to account for variation in the rate of molecular evolution, both across sites and between lineages, or for relying too heavily on few questionable calibration dates (Conway Morris 1997; Ayala et al. 1998; Lee 1999a).”
BackgroundBody size does not predict species richness among the metazoan phyla
Orme, C. D. L., Quicke, D. L. J., Cook, J. M., & Purvis, A. (2002) · Journal of Evolutionary Biology · doi:10.1046/j.1420-9101.2002.00379.x · Cited by 50
“, 1996) to 670 mya (Ayala et al., 1998).”
Danchi, W., & López, B. (2013) · The Astrophysical Journal · doi:10.1088/0004-637x/769/1/27 · Cited by 20
Sakamaki, K., Shimizu, K., Iwata, H., Imai, K., Satou, Y., Funayama, N., Nozaki, M., Yajima, M., Nishimura, O., Higuchi, M., et al. (2014) · Molecular Biology and Evolution · doi:10.1093/molbev/msu260 · Cited by 48
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“For example , Runnegar (1982), Wray et al. (1996), and Ayala et al. (1998) suggested that divergence events we associate with the Cambrian radiation happened back between 670 to 1,200 Ma.”
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Sims, H. J., & McConway, K. (2003) · Evolution · doi:10.1111/j.0014-3820.2003.tb01538.x · Cited by 42
Regier, J. C., & Shultz, J. W. (1998) · American Zoologist · doi:10.1093/icb/38.6.918 · Cited by 42
“Indeed, a phylogenetically and morphologically diverse soft-bodied, minute, or environmentally restricted arthropod/protostome fauna may have existed long before the Cambrian and only acquired paleontological "visibility" with the evolution of armor, large body size, or extensive ecological or geographical ranges (Con…”
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Xiao, S. (2011) · Geophysical monograph · doi:10.1029/146gm16 · Cited by 41
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“(1996) and Ayala et al. (1998) testify against the ability to date such ancient events (with current data and methods).”
BackgroundCañestro, C., Hjelmqvist, L., Albalat, R., García‐Fernàndez, J., Gonzàlez‐Duarte, R., & Jörnvall, H. (2000) · European Journal of Biochemistry · doi:10.1046/j.1432-1327.2000.01711.x · Cited by 40
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Schubert, M., Holland, L. Z., Holland, N. D., & Jacobs, D. K. (2000) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a026291 · Cited by 38
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“Since these events even predate the estimated divergence of protostomes and deuterostomes about 600 to 650 million years ago [23], the invertebrate and vertebrate serotonergic systems are believed to possess roughly the same main receptor classes [21,24].”
BackgroundTherapeutic target discovery using Caenorhabditis elegans
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Evolutionary challenges of extreme environments (part 2)
Waterman, T. H. (2001) · Journal of Experimental Zoology · doi:10.1002/jez.1065 · Cited by 32
A new metazoan from the Vendian of the White Sea, Russia, with possible affinities to the ascidians
Fedonkin, M. A., Vickers-Rich, P., Swalla, B. J., Trusler, P., & Hall, M. (2012) · Paleontological Journal · doi:10.1134/s0031030112010042 · Cited by 33
Crampton, A. L. (1999) · Insect Biochemistry and Molecular Biology · doi:10.1016/s0965-1748(99)00013-2 · Cited by 33
Endosymbiotic calcifying bacteria across sponge species and oceans
Garate, L., Sureda, J., Agell, G., & Uriz, M. J. (2017) · Scientific Reports · doi:10.1038/srep43674 · Cited by 32
“The reporting of bacteria-mediated calcification mechanisms in phylogenetically apart sponges suggests the implication of bacteria in the early evolution of the skeleton in the pre-Cambrian metazoans 51 .”
Tracing the Origins of the Pituitary Adenylate-Cyclase Activating Polypeptide (PACAP)
Cardoso, J. C. R., García, M. G., & Power, D. M. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00366 · Cited by 32
Finding the tree of life: matching phylogenetic trees to the fossil record through the 20th century
Benton, M. J. (2001) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2001.1769 · Cited by 32
Ancient Origin of the New Developmental Superfamily DANGER
Nikolaidis, N., Chalkia, D., Watkins, D. N., Barrow, R. K., Snyder, S. H., van Rossum, D. B., & Patterson, R. L. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000204 · Cited by 30
“Divergence times in million years ago (MYA) were taken from references [58,59].”
A test of whether rates of speciation were unusually high during the Cambrian radiation
Lieberman, B. S. (2001) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2001.1712 · Cited by 31
“1996; Ayala et al. 1998; Bromham et al. 1998; Xiao et al. 1998), it was certainly a time of considerable diversi¢cation, including high rates of origination at higher taxonomic levels (Newell 1952; Raup 1978, 1981, 1991; Sepkoski 1979; Stanley 1979; Van Valen 1985a; Erwin et al. 1987; Gilinsky & Bambach 1987; Foote 19…”
InfluentialThe evolution and ecology of psilocybin in nature
Meyer, M. J., & Slot, J. C. (2023) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2023.103812 · Cited by 30
Neutralism and selectionism: the molecular clock
Ayala, F. J. (2000) · Gene · doi:10.1016/s0378-1119(00)00479-0 · Cited by 30
Self-citationSona, S., Suzuki, T., & Ellington, W. R. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.03.176 · Cited by 29
Devon, R. S., Schwab, C., Topp, J. D., Orban, P. C., Yang, Y.-Z., Pape, T. D., Helm, J., Davidson, T., Rogers, D. A., Gros‐Louis, F., et al. (2004) · Neurobiology of Disease · doi:10.1016/j.nbd.2004.10.002 · Cited by 28
Wenger, Y., & Galliot, B. (2013) · Genome Biology and Evolution · doi:10.1093/gbe/evt142 · Cited by 26
Phylogenetic divergence of island biotas: Molecular dates, extinction, and “relict” lineages
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Ōtsuka, J., & Sugaya, N. (2003) · Journal of Theoretical Biology · doi:10.1016/s0022-5193(03)00057-2 · Cited by 27
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The early history of the metazoa—a paleontologist’s viewpoint
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“However, the precision of the molecular clock is strongly influenced by unequal evo lutionary rates within different groups, the selected statistical methods for primary data processing, and many other assumptions of molecular biology, as well as system biases (Ayala et al., 1998; Bromham, 2003).”
BackgroundNo footprints of primordial introns in a eukaryotic genome
Wolf, Y. I., Kondrashov, F. A., & Koonin, E. V. (2000) · Trends in Genetics · doi:10.1016/s0168-9525(00)02059-x · Cited by 26
Genomic, phylogenetic, and cell biological insights into metazoan origins
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What are olfaction and gustation, and do all animals have them?
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Gomes, M. D. S., Donoghue, M. T. A., Muniyappa, M. K., Pereira, R. V., Guerra‐Sá, R., & Spillane, C. (2013) · Journal of Molecular Evolution · doi:10.1007/s00239-013-9563-2 · Cited by 24
Origin and Evolution of Dishevelled
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The Cambrian Explosion: How Do We Use the Evidence
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Early divergence dates of demosponges based on mitogenomics and evaluated fossil calibrations
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Metazoan phylogenies: falling into place or falling to pieces? A palaeontological perspective
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Role and convergent evolution of competing RNA secondary structures in mutually exclusive splicing
Yue, Y., Hou, S., Wang, X. J., Zhan, L., Cao, G., Li, G., Shi, Y., Zhang, P., Hong, W., Lin, H., et al. (2017) · RNA Biology · doi:10.1080/15476286.2017.1294308 · Cited by 18
“This suggests that exon duplication occurred before the divergence of protostomes and deuterostomes, which occurred »600 million years ago.(32) Interestingly, both the number and structure ofMRP1 duplicated exons diverged considerably during chordate evolution.”
Background
Metadata
- Authors
- Ayala, F. J., Rzhetsky, A., & Ayala, F. J.
- Affiliations
- Institute of Molecular Evolutionary Genetics, Pennsylvania State University, University Park, PA 16802; Columbia Genome Center, Columbia University, New York, NY 10032; and Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697
- Pennsylvania State University (US)
- ORCID
- Rzhetsky, Andrey
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 1998-01-20
- Volume
- 95
- Issue
- 2
- Pages
- 606-611
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC18467
- OpenAlex
- W2146480768
- Cited by
- 342
- References
- 41
- Citations by year
- 2026: 1 · 2024: 7 · 2023: 6 · 2022: 2 · 2021: 3 · 2020: 1 · 2019: 4 · 2018: 1 · 2017: 5 · 2016: 7 · 2015: 5 · 2014: 8 · 2013: 13 · 2012: 7
- FWCI
- 41.96
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- Funders
- National Institutes of Health (5p01gm042397-05)
- National Institute of General Medical Sciences (GM 42397)
- Topics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- divergence time estimation, Cambrian explosion, Neoproterozoic, protein-coding genes, molecular clock rates, invertebrate evolution, arthropods, Annelida, Mollusca, Echinodermata
- MeSH terms
- Animals, Fossils, Phylogeny, Proteins, Evolution, Molecular
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