Can fast early rates reconcile molecular dates with the Cambrian explosion?
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Molecular dates consistently place the divergence of major metazoan lineages in the Precambrian, leading to the suggestion that the 'Cambrian explosion' is an artefact of preservation which left earlier forms unrecorded in the fossil record. While criticisms of molecular analyses for failing to deal with variation in the rate of molecular evolution adequately have been countered by analyses which allow both site-to-site and lineage-specific rate variation, no analysis to date has allowed the rates to vary temporally. If the rates of molecular evolution were much higher early in the metazoan radiation, molecular dates could consistently overestimate the divergence times of lineages. Here, we use a new method which uses multiple calibration dates and an empirically determined range of possible substitution rates to place bounds on the basal date of divergence of lineages in order to ask whether faster rates of molecular evolution early in the metazoan radiation could possibly account for the discrepancy between molecular and palaeontological date estimates. We find that allowing basal (interphylum) lineages the fastest observed substitution rate brings the minimum possible divergence date (586 million years ago) to the Vendian period, just before the first multicellular animal fossils, but excludes divergence of the major metazoan lineages in a Cambrian explosion.
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Estimating maximum and minimum possible rates for a given data set requires several calibration dates, which are not always available, and gives conservative assessments of molecular dates suitable only for rejecting particular hypotheses as inconsistent with the data.
“Estimating maximum and minimum possible rates for a given data set requires several calibration dates, which are not always available, and gives conservative assessments of molecular dates that are suitable only for rejecting particular hypotheses as being inconsistent with the data 55 .”
From The modern molecular clock (2003) · cites this paper as [55]
Cites
The Neutral Theory of Molecular Evolution
Kimura, M. (1979) · Scientific American · doi:10.1038/scientificamerican1179-98 · Cited by 7,698 · see citing works
The Neutral Theory of Molecular Evolution
Kimura, M. (1983) · Cambridge University Press eBooks · doi:10.1017/cbo9780511623486 · Cited by 6,300 · see citing works
A molecular timescale for vertebrate evolution
Kumar, S., & Hedges, S. B. (1998) · Nature · doi:10.1038/31927 · Cited by 1,936 · see citing works
Noble, B. (1969) · UCLA - Biblioteca de Ciencias y Tecnologia Felix Morales Bueno · Cited by 1,328 · see citing works
Body size, metabolic rate, generation time, and the molecular clock.
Martin, A. P., & Palumbi, S. R. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.9.4087 · Cited by 1,239 · see citing works
Early 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 · see citing works
Calibrating Rates of Early Cambrian Evolution
Bowring, S. A., Grotzinger, J. P., Isachsen, C. E., Knoll, A. H., Pelechaty, S. M., & Kolosov, P. (1993) · Science · doi:10.1126/science.11539488 · Cited by 526 · see citing works
Precambrian Sponges with Cellular Structures
Li, C.-W., Chen, J.-Y., & Hua, T.-E. (1998) · Science · doi:10.1126/science.279.5352.879 · Cited by 489 · see citing works
Mass survival of birds across the Cretaceous–Tertiary boundary: Molecular evidence.
Cooper, A., & Penny, D. (1997) · Science · doi:10.1126/science.275.5303.1109 · Cited by 472 · see citing works
The fossil record and the early evolution of the Metazoa
Morris, S. C. (1993) · Nature · doi:10.1038/361219a0 · Cited by 389 · see citing works
The Late Precambrian fossil Kimberella is a mollusc-like bilaterian organism
Fedonkin, M. A., & Waggoner, B. M. (1997) · Nature · doi:10.1038/42242 · Cited by 373 · see citing works
Origin of the metazoan phyla: Molecular clocks confirm paleontological estimates
Ayala, F. J., Rzhetsky, A., & Ayala, F. J. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.2.606 · Cited by 342 · see citing works
The Probability of Fixation in Populations of Changing Size
Otto, S. P., & Whitlock, M. C. (1997) · Genetics · doi:10.1093/genetics/146.2.723 · Cited by 341 · see citing works
Foote, M., Hunter, J. P., Janis, C. M., & Sepkoski, J. J. (1999) · Science · doi:10.1126/science.283.5406.1310 · Cited by 303 · see citing works
Fossils, molecules and embryos: new perspectives on the Cambrian explosion
Valentine, J. W., Jablonski, D., & Erwin, D. H. (1999) · Development · doi:10.1242/dev.126.5.851 · Cited by 300 · see citing works
Explosive Evolution in Tertiary Birds and Mammals
Feduccia, A. (1995) · Science · doi:10.1126/science.267.5198.637 · Cited by 299 · see citing works
Estimating divergence dates from molecular sequences.
Rambaut, A., & Bromham, L. (1998) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a025940 · Cited by 298 · see citing works
Self-citationDeterminants of rate variation in mammalian DNA sequence evolution.
Bromham, L., Rambaut, A., & Harvey, P. H. (1996) · Journal of Molecular Evolution · doi:10.1007/bf02202109 · Cited by 291 · see citing works
Self-citationLong expected sponges from the Neoproterozoic Ediacara fauna of South Australia
Gehling, J. G., & Rigby, J. K. (1996) · Journal of Paleontology · doi:10.1017/s0022336000023283 · Cited by 256 · see citing works
Genomic evolution during a 10,000-generation experiment with bacteria
Papadopoulos, D., Schneider, D., Meier-Eiss, J., Arber, W., Lenski, R. E., & Blot, M. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.7.3807 · Cited by 234 · see citing works
(1993) · Biodiversity Heritage Library (Smithsonian Institution) · Cited by 197 · see citing works
Evolutionary explosions and the phylogenetic fuse
Cooper, A., & Fortey, R. A. (1998) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(97)01277-9 · Cited by 196 · see citing works
Ediacara-type fossils in Cambrian sediments
Jensen, S., Gehling, J. G., & Droser, M. L. (1998) · Nature · doi:10.1038/31215 · Cited by 185 · see citing works
An examination of the generation-time effect on molecular evolution.
Ohta, T. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.22.10676 · Cited by 176 · see citing works
The Power of Relative Rates Tests Depends on the Data
Bromham, L., Penny, D., Rambaut, A., & Hendy, M. D. (2000) · Journal of Molecular Evolution · doi:10.1007/s002399910034 · Cited by 168 · see citing works
Self-citationTesting the Cambrian explosion hypothesis by using a molecular dating technique
Bromham, L., Rambaut, A., Fortey, R., Cooper, A., & Penny, D. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.21.12386 · Cited by 148 · see citing works
Self-citationMolecular Clock Calibrations and Metazoan Divergence Dates
Lee, M. S. Y. (1999) · Journal of Molecular Evolution · doi:10.1007/pl00006562 · Cited by 142 · cited 2× · see citing works
“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).”
BackgroundMetabolic Rate, Generation Time, and the Rate of Molecular Evolution in Birds
Mooers, A. Ø., & Harvey, P. H. (1994) · Molecular Phylogenetics and Evolution · doi:10.1006/mpev.1994.1040 · Cited by 141 · cited 1× · see citing works
“The body size trend in molecular evolution rate in tetrapod vertebrates (Martin & Palumbi 1993; Mooers & Harvey 1994; Bromham et al. 1996) has prompted the suggestion that the presumed small size of the earliest metazoans generated faster rates early in the metazoan radiation (Conway Morris 1998).”
BackgroundCORRELATED RATES OF MOLECULAR AND MORPHOLOGICAL EVOLUTION
Omland, K. E. (1997) · Evolution · doi:10.1111/j.1558-5646.1997.tb01461.x · Cited by 141 · see citing works
Growing up with dinosaurs: molecular dates and the mammalian radiation
Bromham, L., Phillips, M. J., & Penny, D. (1999) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(98)01507-9 · Cited by 127 · see citing works
Self-citationRate of rbc L gene sequence evolution and species diversification in flowering plants (angiosperms)
Barraclough, T. G., Harvey, P., & Nee, S. (1996) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1996.0088 · Cited by 104 · see citing works
The cambrian evolutionary ‘explosion’ recalibrated
Fortey, R. A., Briggs, D. E. G., & Wills, M. A. (1997) · BioEssays · doi:10.1002/bies.950190510 · Cited by 95 · see citing works
Early Metazoan Evolution: Reconciling Paleontology and Molecular Biology
MORRIS, S. C. (1998) · American Zoologist · doi:10.1093/icb/38.6.867 · Cited by 64 · cited 9× · see citing works
“…rates during the metazoan radiation, particularly given Omland’s (1997) observation of an association between the rates of molecular change and rates of morphological change for a number of phylogenies (Vermeij 1996; Conway Morris 1998; Knoll & Carroll 1999; Lee 1999b; Valentine et al. 1999).”
BackgroundInfluentialTHE AGE AND RELATIONSHIPS OF THE MAJOR ANIMAL PHYLA
Lynch, M. (1999) · Evolution · doi:10.1111/j.1558-5646.1999.tb03768.x · Cited by 64 · see citing works
The Future of the Fossil Record
Jablonski, D. (1999) · Science · doi:10.1126/science.284.5423.2114 · Cited by 59 · see citing works
Temporal scaling of molecular evolution in primates and other mammals.
Gingerich, P. D. (1986) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a040391 · Cited by 55 · see citing works
Molecular clocks: Defusing the Cambrian ‘explosion’?
Morris, S. C. (1997) · Current Biology · doi:10.1016/s0960-9822(06)00039-x · Cited by 52 · see citing works
Rate of gene sequence evolution and species diversification in flowering plants: a re–evaluation
Savolainen, V., & Goudet, J. (1998) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1998.0337 · Cited by 28 · see citing works
Vermeij, G. J. (1996) · Science · doi:10.1126/science.274.5287.525 · Cited by 23 · see citing works
Molecular dates and the mammalian radiation
Archibald, J. D. (1999) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(99)01652-3 · Cited by 12 · see citing works
Shortening the phylogenetic fuse
Lee, M. S. Y. (1998) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(98)01377-9 · Cited by 10 · see citing works
Reply from L. Bromham, D. Penny and M.J. Phillips
Bromham, L. D., Penny, D., & Phillips, M. J. (1999) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(99)01651-1 · Cited by 5 · see citing works
Self-citation
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Sanderson, M. J. (2002) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a003974 · Cited by 1,977 · see citing works
The timing of eukaryotic evolution: Does a relaxed molecular clock reconcile proteins and fossils?
Douzery, E. J. P., Snell, E. A., Bapteste, E., Delsuc, F., & Philippe, H. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0403984101 · Cited by 638 · see citing works
Bromham, L., & Penny, D. (2003) · Nature Reviews Genetics · doi:10.1038/nrg1020 · Cited by 615 · see citing works
Self-citationMolecular evidence on plant divergence times
Sanderson, M. J., Thorne, J. L., Wikström, N., & Bremer, K. (2004) · American Journal of Botany · doi:10.3732/ajb.91.10.1656 · Cited by 301 · see citing works
Benton, M. J., & Ayala, F. J. (2003) · Science · doi:10.1126/science.1077795 · Cited by 252 · see citing works
Aris-Brosou, S., & Yang, Z. (2002) · Systematic Biology · doi:10.1080/10635150290102375 · Cited by 230 · see citing works
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Slack, K. E., Jones, C. M., Ando, T., Harrison, G. L. (., Fordyce, R. E., Arnason, U., & Penny, D. (2006) · Molecular Biology and Evolution · doi:10.1093/molbev/msj124 · Cited by 283 · see citing works
Dating the Time of Origin of Major Clades: Molecular Clocks and the Fossil Record
Smith, A. B., & Peterson, K. J. (2002) · Annual Review of Earth and Planetary Sciences · doi:10.1146/annurev.earth.30.091201.140057 · Cited by 193 · see citing works
Ho, S. Y. W. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msi125 · Cited by 190 · see citing works
Time Flies, a New Molecular Time-Scale for Brachyceran Fly Evolution Without a Clock
Wiegmann, B. M., Yeates, D. K., Thorne, J. L., & Kishino, H. (2003) · Systematic Biology · doi:10.1080/10635150390250965 · Cited by 182 · see citing works
Rates of phenotypic and genomic evolution during the Cambrian explosion
Lee, M. S. Y., Soubrier, J., & Edgecombe, G. D. (2013) · Current Biology · doi:10.1016/j.cub.2013.07.055 · Cited by 162 · see citing works
Aris-Brosou, S. (2003) · Molecular Biology and Evolution · doi:10.1093/molbev/msg226 · Cited by 164 · see citing works
Bayesian molecular dating: opening up the black box
Bromham, L. D., Duchêne, S., Hua, X., Ritchie, A. M., Duchêne, D. A., & Ho, S. Y. W. (2017) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12390 · Cited by 152 · see citing works
Self-citationTESTING THE RELATIONSHIP BETWEEN MORPHOLOGICAL AND MOLECULAR RATES OF CHANGE ALONG PHYLOGENIES
Bromham, L., Woolfit, M., Lee, M. S. Y., & Rambaut, A. (2002) · Evolution · doi:10.1111/j.0014-3820.2002.tb00118.x · Cited by 139 · see citing works
Self-citationLartillot, N., & Delsuc, F. (2011) · Evolution · doi:10.1111/j.1558-5646.2011.01558.x · Cited by 92 · see citing works
On nitric oxide signaling, metamorphosis, and the evolution of biphasic life cycles
Bishop, C. D., & Brandhorst, B. P. (2003) · Evolution & Development · doi:10.1046/j.1525-142x.2003.03059.x · Cited by 84 · see citing works
What is the age of flowering plants?
Sauquet, H., Ramírez‐Barahona, S., & Magallón, S. (2022) · Journal of Experimental Botany · doi:10.1093/jxb/erac130 · Cited by 79 · see citing works
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Bromham, L. D., & Leys, R. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msi133 · Cited by 77 · see citing works
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Kirschvink, J. L., & Raub, T. D. (2003) · Comptes Rendus Géoscience · doi:10.1016/s1631-0713(03)00011-7 · Cited by 77 · see citing works
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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 71 · see citing works
Padovan, A. C. B., Sanson, G. F. O., Brunstein, A., & Briones, M. R. S. (2005) · Journal of Molecular Evolution · doi:10.1007/s00239-004-0164-y · Cited by 69 · see citing works
Bromham, L. D., & Woolfit, M. (2004) · Systematic Biology · doi:10.1080/10635150490522278 · Cited by 63 · see citing works
Self-citationFontanillas, E., Welch, J. J., Thomas, J. A., & Bromham, L. D. (2007) · BMC Evolutionary Biology · doi:10.1186/1471-2148-7-95 · Cited by 59 · see citing works
Self-citationTinn, O., & Oakley, T. H. (2008) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2008.03.001 · Cited by 54 · see citing works
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Welch, J. J., Fontanillas, E., & Bromham, L. (2005) · Systematic Biology · doi:10.1080/10635150590947212 · Cited by 53 · see citing works
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Bromham, L. (2003) · Journal of Molecular Evolution · doi:10.1007/s00239-003-0002-7 · Cited by 40 · see citing works
Self-citationWhat can DNA Tell us About the Cambrian Explosion?
Bromham, L. D. (2003) · Integrative and Comparative Biology · doi:10.1093/icb/43.1.148 · Cited by 42 · see citing works
Self-citationThe Precambrian emergence of animal life: a geobiological perspective
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Levinton, J. S. (2008) · BioScience · doi:10.1641/b580912 · Cited by 23 · see citing works
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Takezaki, N. (2018) · Genome Biology and Evolution · doi:10.1093/gbe/evy125 · Cited by 21 · see citing works
Phylochronology of early metazoans: combined evidence from molecular and fossil data
Qun, Y., Ma, J., Xiaoyan, S., & Peiyun, C. (2007) · Geological Journal · doi:10.1002/gj.1074 · Cited by 20 · see citing works
Attwood, S. W., Lokman, H. S., & Ong, K.-S. (2005) · Journal of Molluscan Studies · doi:10.1093/mollus/eyi040 · Cited by 18 · see citing works
Hull, J. M., Savage, W. K., Bollmer, J. L., Kimball, R. T., Parker, P. G., Whiteman, N. K., & Ernest, H. B. (2008) · Biological Journal of the Linnean Society · doi:10.1111/j.1095-8312.2008.01082.x · Cited by 18 · see citing works
Babenko, V. N. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh833 · Cited by 18 · see citing works
Zou, H., Lei, H., Chen, R., Chen, F.-L., Li, W. X., Li, M., Zhang, D., Jakovlić, I., & Wang, G. (2022) · Water Biology and Security · doi:10.1016/j.watbs.2022.100033 · Cited by 15 · see citing works
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Budd, G. E., & Mann, R. P. (2025) · Systematic Biology · doi:10.1093/sysbio/syaf020 · Cited by 7 · see citing works
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Barthélémy, R.-M., PETENIAN, F., Vannier, J., Casanova, J.-P., & Faure, É. (2006) · International Journal of Zoological Research · doi:10.3923/ijzr.2006.284.300 · Cited by 7 · see citing works
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Benton, M. J. (2011) · Harvard University Press eBooks · doi:10.2307/j.ctv1pncpmx.7 · Cited by 6 · see citing works
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Ma, C., Luo, Y., Zhang, C., Cheng, C., Hua, N., Liu, X., Wu, J., Qin, L., Yu, P., Luo, J., et al. (2024) · 中国科学通报:英文版 · doi:10.1016/j.scib.2024.04.052 · Cited by 4 · see citing works
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Syvanen, M. (2002) · Elsevier eBooks · doi:10.1016/b978-012680126-2/50038-4 · Cited by 2 · see citing works
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Budd, G. E. (2013) · Current Biology · doi:10.1016/j.cub.2013.07.019 · Cited by 2 · see citing works
EXCURSIONS IN MACROEVOLUTION1,2
Wagner, P. J. (2002) · Evolution · doi:10.1554/0014-3820(2002)056[1876:eim]2.0.co;2 · Cited by 1 · see citing works
Part H, Brachiopoda (Revised), vol. 6, References and Index
Williams, A. (2007) · Treatise on Invertebrate Paleontology · doi:10.17161/dt.v0i0.5525 · Cited by 1 · see citing works
Budd, G. E., & Mann, R. P. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.02.01.578373 · Cited by 1 · see citing works
Wagner, P. J. (2002) · Evolution · doi:10.1111/j.0014-3820.2002.tb00205.x
- Self-citation
Laflamme (2004) · doi:10.1666/0022-3360(2004)078
- Authors
- Bromham, L. D., & Hendy, M. D.
- Affiliations
- The University of Queensland (AU)
- Massey University (NZ)
- Corresponding author
- Bromham, L. D.
- Venue
- Proceedings of the Royal Society of London. Series B: Biological Sciences
- Publisher
- The Royal Society
- Published
- 2000-05-22
- Volume
- 267
- Issue
- 1447
- Pages
- 1041-1047
- ISSN
- 0080-4649 (ISSN-L)
- 0962-8452
- 1471-2954
- PMC
- PMC1690629
- OpenAlex
- W2018170589
- Cited by
- 50
- References
- 42
- Citations by year
- 2025: 1 · 2024: 2 · 2022: 2 · 2018: 1 · 2017: 1 · 2016: 1 · 2013: 2
- FWCI
- 7.02
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the Royal Society B Biological Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Figshare (submittedVersion, cc-by)
- Topics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Keywords
- Cambrian explosion, divergence time estimation, molecular evolution rate, substitution rate variation
- MeSH terms
- Animals, Biological Evolution, Fossils, Models, Biological
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