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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]
Citations
Cites
Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994) · Nucleic Acids Research · doi:10.1093/nar/22.22.4673 · Cited by 64,617
The neighbor-joining method: a new method for reconstructing phylogenetic trees.
Saitou, N., & Nei, M. (1987) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a040454 · Cited by 59,959
The Advanced Theory of Statistics.
Clarke, G. M., Kendall, M. G., & Stuart, A. (1978) · Journal of the Royal Statistical Society Series A (General) · doi:10.2307/2344782 · Cited by 6,727
Atlas of protein sequence and structure
Chang, M.-Y., Dayhoff, M. O., Eck, R. V., & Sochard, M. R. (1965) · NASA Technical Reports Server (NASA) · Cited by 4,383
Evolutionary divergence and convergence in proteins.
ZUCKERKANDL, E., & PAULING, L. (1965) · Evolving Genes and Proteins · doi:10.1016/b978-1-4832-2734-4.50017-6 · Cited by 3,020
Atlas of Protein Sequence and Structure, 1972.
Fitch, W. M., & Dayhoff, M. O. (1973) · Systematic Zoology · doi:10.2307/2412105 · Cited by 2,454
Bryson, V., & Vogel, H. J. (1965) · Science · doi:10.1126/science.147.3653.68 · Cited by 1,343
The causes of molecular evolution
Gillespie, J. H. (1992) · Choice Reviews Online · doi:10.5860/choice.30-2064 · Cited by 1,214
Yang, Z. (1993) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a040082 · Cited by 1,040
(1992) · Cambridge University Press eBooks · doi:10.1017/cbo9780511601064 · Cited by 902
Phylogenetic test of the molecular clock and linearized trees.
Takezaki, N., Rzhetsky, A., & Nei, M. (1995) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a040259 · Cited by 826
Self-citationEvolution by the birth-and-death process in multigene families of the vertebrate immune system
Nei, M., Gu, X., & Sitnikova, T. Y. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.15.7799 · Cited by 802
Biostratigraphic and Geochronologic Constraints on Early Animal Evolution
Grotzinger, J. P., Bowring, S. A., Saylor, B. Z., & Kaufman, A. J. (1995) · Science · doi:10.1126/science.270.5236.598 · Cited by 701
The Advanced Theory of Statistics.
P., E. S., & Kendall, M. G. (1944) · Journal Of The Royal Statistical Society · doi:10.2307/2981279 · Cited by 687
The Causes of Molecular Evolution
Gillespie, J. H. (1992) · doi:10.1093/oso/9780195068832.001.0001 · Cited by 634
The Proterozoic biosphere: a multidisciplinary study
Schopf, J. W. (1988) · Lethaia · doi:10.1111/j.1502-3931.1988.tb02083.x · Cited by 591
Continental breakup and the ordinal diversification of birds and mammals
Hedges, S. B., Parker, P. H., Sibley, C. G., & Kumar, S. (1996) · Nature · doi:10.1038/381226a0 · Cited by 529
Molecular Evidence for Deep Precambrian Divergences Among Metazoan Phyla
Wray, G. A., Levinton, J. S., & Shapiro, L. H. (1996) · Science · doi:10.1126/science.274.5287.568 · Cited by 511
Schopf, J. W., & Klein, C. (1992) · Cambridge University Press eBooks · doi:10.1017/cbo9780511601064.002 · Cited by 394
The fossil record and the early evolution of the Metazoa
Morris, S. C. (1993) · Nature · doi:10.1038/361219a0 · Cited by 389
Limitations of the evolutionary parsimony method of phylogenetic analysis.
Li, J., & Nei, M. (1990) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a040588 · Cited by 364
Eernisse, D. J., Albert, J. S., & Anderson, F. E. (1992) · Systematic Biology · doi:10.1093/sysbio/41.3.305 · Cited by 310
Nei, M., Stephens, J. C., & Saitou, N. (1985) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a040333 · Cited by 302
Origin and Early Evolution of the Metazoa
(1992) · Topics in geobiology · doi:10.1007/978-1-4899-2427-8 · Cited by 274
Can the Cambrian explosion be inferred through molecular phylogeny?
Philippe, H., Chenuil, A., & Adoutte, A. (1994) · Development · doi:10.1242/dev.1994.supplement.15 · Cited by 226
Ota, T., & Nei, M. (1994) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a040127 · Cited by 226
A molecular‐clock date for the origin of the animal phyla
Runnegar, B. (1982) · Lethaia · doi:10.1111/j.1502-3931.1982.tb00645.x · Cited by 151
Glaessner, M. F. (1984) · Cited by 144
Vagaries of the molecular clock.
Ayala, F. J. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.15.7776 · Cited by 140
Self-citationEstimates of DNA and protein sequence divergence: an examination of some assumptions.
Golding, G. B. (1984) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a040303 · Cited by 122
On the virtues and pitfalls of the molecular evolutionary clock
Ayala, F. J. (1986) · Journal of Heredity · doi:10.1093/oxfordjournals.jhered.a110227 · Cited by 85
Self-citationMeiofauna and the origins of the Metazoa
BOADEN, P. J. S. (1989) · Zoological Journal of the Linnean Society · doi:10.1111/j.1096-3642.1989.tb01828.x · Cited by 65
Complete genome sequences of cellular life forms: glimpses of theoretical evolutionary genomics
Koonin, E. V., & Mushegian, A. R. (1996) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(96)80032-3 · Cited by 58
Bilaterians of the Precambrian—Cambrian transition and the annelid—arthropod relationship
Valentine, J. W. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.7.2272 · Cited by 45
The amino acid sequence of cytochrome c from Helix aspersa Müller (garden snail)
Brown, R. H., Richardson, M., Boulter, D., Ramshaw, J. A. M., & Jefferies, R. P. S. (1972) · Biochemical Journal · doi:10.1042/bj1280971 · Cited by 36
Molecular clock or erratic evolution? A tale of two genes.
Ayala, F. J., Barrio, E., & Kwiatowski, J. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.21.11729 · Cited by 35
Self-citationValentine, J. W. (1973) · Systematic Zoology · doi:10.2307/2412093 · Cited by 31
Overdispersed molecular clock at the major histocompatibility complex loci
Takahata, N. (1991) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1991.0003 · Cited by 21
Molecular clocks, molecular phylogenies and the origin of phyla
Erwin, D. H. (1989) · Lethaia · doi:10.1111/j.1502-3931.1989.tb01338.x · Cited by 16
Research works printed but not linked: 16
- T Dobzhansky, F J Ayala, G L Stebbins, J W Valentine Evolution (Freeman, San Francisco, 1977).
- J W Valentine, S M Awramik, P W Signor, P M Sadler Evol Biol 25, 279–356 (1991).
- S J Gould Wonderful Life (Norton, New York, 1989).
- 10.1111/j.1096-3642.1989.tb02257.x · DOI
- H Phillipe, A Chenuil, A Adoutte Development (Cambridge, UK) Suppl 1994, 15–25 (1994).
- B Runnegar Paleontology 29, 1–24 (1986).
- M Nei, J C Stephens, N Saitou Mol Biol Evol 2, 66–85 (1985).
- G B Golding Mol Biol Evol 1, 125–142 (1983).
- L Jin, M Nei Mol Biol Evol 10, 1396–1402 (1990).
- Z Yang Mol Biol Evol 10, 1396–1402 (1993).
- N Takezaki, A Rzhetsky, M Nei Mol Biol Evol 12, 823–833 (1995).
- N Saitou, M Nei Mol Biol Evol 4, 406–425 (1987).
- W-H Li Molecular Evolution (Sinauer, Sunderland, MA, 1997).
- J W Valentine Patterns of Evolution, ed A Hallam (Elsevier, Amsterdam), pp. 27–58 (1977).
- T Ohita, M Nei Mol Biol Evol 11, 469–482 (1994).
- R R Sokal, F J Rohlf Biometry (Freeman, 2nd Ed., New York, 1981).
Cited by
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Inferring the historical patterns of biological evolution
Pagel, M. (1999) · Nature · doi:10.1038/44766 · Cited by 5,200
Sanderson, M. J. (2002) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a003974 · Cited by 1,977
“Estimates of absolute rates are often made by pairwise comparisons that necessarily average the rate differences on intervening branches (Easteal and Herbert 1997; Ayala, Rzhetsky, and Ayala 1998), thus underestimating the variability in rate.”
BackgroundMethodEarly animal evolution: emerging views from comparative biology and geology
Knoll, A. H., & Carroll, S. B. (1999) · Science · doi:10.1126/science.284.5423.2129 · Cited by 821
Reading the entrails of chickens: molecular timescales of evolution and the illusion of precision
Graur, D., & Martin, W. (2004) · Trends in Genetics · doi:10.1016/j.tig.2003.12.003 · Cited by 669
Age and rate of diversification of the Hawaiian silversword alliance (Compositae)
Baldwin, B. G., & Sanderson, M. J. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.16.9402 · Cited by 683
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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