The DOI matches its Crossref record; 36 of the 36 references it cites were found in a registry or an index; none of the 19 sources its claims cite is checked for support yet.
Testing the Cambrian explosion hypothesis by using a molecular dating technique
Open accessAbstract
Molecular studies have the potential to shed light on the origin of the animal phyla by providing independent estimates of the divergence times, but have been criticized for failing to account adequately for variation in rate of evolution. A method of dating divergence times from molecular data addresses the criticisms of earlier studies and provides more realistic, but wider, confidence intervals. The data are not compatible with the Cambrian explosion hypothesis as an explanation for the origin of metazoan phyla, and provide additional support for an extended period of Precambrian metazoan diversification.
Overview
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Written from the paper’s full text.
TL;DR
Using a maximum-likelihood quartet dating method that tests rate constancy, the authors estimate that the echinoderm-vertebrate and protostome-deuterostome divergences are older than 680 Ma. They conclude the molecular data are incompatible with the Cambrian explosion hypothesis and support an extended period of Precambrian metazoan diversification.
Key findings
- The majority of quartets were rejected by the rate-constancy test, implying widespread rate heterogeneity among metazoan taxa for these sequences.
- Date estimates from quartets with no detectable rate variation were obtained for two nodes, the echinoderm-vertebrate split and the protostome-deuterostome split; all estimates are older than 680 Ma, excluding divergence at or near the base of the Cambrian.
- Because sister taxa to the dated nodes, such as Brachiopoda, Porifera, and Cnidaria, must also have been present earlier, the authors infer these lineages existed before the Vendian (600 Ma) despite the lack of earlier fossils.
- The authors reject the Cambrian explosion hypothesis and state their findings are in broad agreement with some earlier molecular studies.
Methods
- Two data sets were used: protein-coding mitochondrial DNA from whole mitochondrial genome sequences (5,676 bp) and nuclear-encoded 18S rRNA (1,710 bp); sequences were aligned by eye and saturated or unconfidently aligned regions were removed.
- Dated pairs were formed using fossil dates from the literature between 540 and 200 Ma, and quartets were formed from all possible combinations of monophyletic dated pairs. The maximum-likelihood quartet method used the HKY85 model with gamma-distributed rates across sites; for mitochondrial DNA the transition/transversion ratio was 1.21 and gamma shape parameter 0.38, and for 18S rRNA these were 1.74 and 0.38.
- Rate constancy was tested by comparing rate-constrained and free-rate models; 1,000 sequence data sets were simulated per quartet with seq-gen, and a quartet was rejected if its observed log-likelihood difference exceeded that of 95% of simulations. Confidence intervals for divergence dates were obtained from the tZ value giving a log likelihood 1.92 below the maximum, based on a χ² distribution with 1 df at the 5% level.
Limitations
- The paper states that uncertainty in phylogenetic reconstruction and the stochastic nature of the molecular clock preclude precise dating, that confidence intervals are wide, and that the results cannot put an absolute date on the origin of phyla; direct date estimates are provided for only two nodes.
- The paper states that the branching order of phyla remains controversial and that the tree used is for illustrative purposes; it also notes that date estimates differ between the two sequence sets, possibly reflecting differences in model fit, and that rRNA paired-site evolution is not adequately modeled and may cause overestimation of divergence times.
- Evident from the text: the conclusions depend on fossil calibration dates taken from the literature and on the subset of quartets that passed the rate-constancy test; the paper does not quantify uncertainty in those fossil calibration dates.
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Claims the paper makes
11 Not checked yet · 11 Own interpretation · 4 Own result · 4 No basis given · 1 Own method
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Date estimates from quartets with no detectable rate variation between pairs were obtained for two nodes, the echinoderm-vertebrate split and the protostome-deuterostome split (Fig. 2).”
plain- Asserted: passes — The authors put it forward as true.
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In the paper
“The majority of the quartets were rejected (Fig. 2), implying that rate heterogeneity is widespread among metazoan taxa for these sequences and demonstrating the value of testing each comparison separately rather than basing the expectation of clock-like evolution on inferred general trends.”
plain- Asserted: passes — The authors put it forward as true.
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None of the sources cited for this claim have been checked yet.
In the paper
“Underestimating the degree of rate heterogeneity between sites will tend to underestimate the dates of divergence (16, 25) caused by a nonlinear effect of heterogeneity on branch length.”
What the sources say
- Not checked yetcites [16]
- Not checked yetcites [25] source
hedgeddirect- Asserted: passes — The authors put it forward as true.
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In the paper
“The results from molecular studies are consistent with the interpretation of fossil evidence for a Precambrian history of modern phyla, either by new discoveries or through the reinterpretation of previous finds.”
plaincorrelational- Asserted: passes — The authors put it forward as true.
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A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The majority of the quartets were rejected (Fig. 2), implying that rate heterogeneity is widespread among metazoan taxa for these sequences and demonstrating the value of testing each comparison separately rather than basing the expectation of clock-like evolution on inferred general trends.”
boosted- Asserted: passes — The authors put it forward as true.
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- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The difference in the date estimates from our two sets of sequences illustrates the importance of basing estimates on several sequences and may reflect differences in the fit between model and data for different types of sequences.”
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“Therefore, the absence of appropriate Precambrian fossils is not necessarily evidence for an explosive evolutionary radiation near the beginning of the Cambrian period.”
hedged- Asserted: passes — The authors put it forward as true.
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In the paper
“The data are not compatible with the Cambrian explosion hypothesis as an explanation for the origin of metazoan phyla, and provide additional support for an extended period of Precambrian metazoan diversification.”
plaincorrelational- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
In the paper
“All sister taxa to the dated nodes, such as Brachiopoda, Porifera, and Cnidaria (17), must also have been present before the Vendian period (600 Ma), despite the lack of earlier fossils.”
What the sources say
- Not checked yetcites [17]
plain- Asserted: passes — The authors put it forward as true.
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None of the sources cited for this claim have been checked yet.
In the 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).”
- Also stated in: § RESULTS · boosted
“The method presented here is a significant advance on previous studies (20–23), because (i) the confidence intervals reflect the stochastic error in the substitution process; (ii) assumptions of rate heterogeneity between lineages are explicitly tested within the maximum likelihood framework; and (iii) multiple rates of molecular evolution are included in the model.”
What the sources say
boosted- Asserted: passes — The authors put it forward as true.
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- Also stated in: § RESULTS · boosted
- It may state two separate claims as one. 10
- Probably not a substantial claim. 9
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“However, the confidence intervals permit us to exclude the divergence of these lineages at or near the base of the Cambrian and all are older than 680 Ma, predating the recent metazoan fossil discoveries.”
plain- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
In the paper
“The confidence intervals are wide, as expected for molecular date estimates (8), therefore these results cannot be used to put an absolute date on the origin of phyla.”
What the sources say
- Not checked yetcites [8]
plaindirect- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“For the mitochondrial DNA, we obtained a transition/transversion ratio of 1.21 and gamma shape parameter of 0.38. For the 18S rRNA, these parameters were 1.74 and 0.38, respectively.”
plain- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“One aspect of the evolution of rRNA that is not adequately modeled is the evolution of paired sites (18, 19), the effect of which is likely to be an increase in the count of independent changes between two sequences, thus causing an overestimation of time since divergence.”
What the sources say
- Not checked yetcites [18]
- Not checked yetcites [19]
hedgedconditional- Asserted: passes — The authors put it forward as true.
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What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“The use of many dates permits testing for rate constancy between taxa and avoids reliance on a single calibration rate to date all lineages.”
plaindirect- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. It may state two separate claims as one.
In the paper
“However, the absence of earlier metazoan fossils could be caused by systematic biases in preservation that left the Precambrian history of recognized phyla unrecorded (7).”
What the sources say
- Not checked yetcites [7] source
hedgedconditional- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim.
None of the sources cited for this claim have been checked yet.
In the paper
“Our findings are in broad agreement with some earlier molecular studies (20–22), despite differences in method and sequences used.”
What the sources say
plaincorrelational- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it.
In the paper
“The uncertainty in phylogenetic reconstruction and the stochastic nature of the molecular clock preclude precise dating (8), but when the imprecision is expressed as appropriate confidence intervals, molecular data are ideally suited to testing specific hypotheses.”
What the sources say
- Not checked yetcites [8]
plaindirect- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
The paper states this without a source or data behind it here, so there is nothing to check it against. The quote shows it is in the paper.
In the paper
“By contrast, the Precambrian phylogenetic fuse hypothesis assumes no more than we already know to be reasonable: that lineages can diverge gradually over time and that the fossil record contains gaps that can greatly reduce the chances of finding fossils for certain periods or particular types of organisms.”
plaindirect- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. It may be too vague to check against evidence. The paper may give no reason why it holds. It may state two separate claims as one.
The paper states this without a source or data behind it here, so there is nothing to check it against. The quote shows it is in the paper.
In the paper
“Molecular dating provides a means of testing hypotheses about the timing of origin of lineages, provided that molecular dates are presented with realistic estimates of confidence intervals.”
plainconditional- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim.
The paper states this without a source or data behind it here, so there is nothing to check it against. The quote shows it is in the paper.
In the paper
“The Cambrian explosion hypothesis—that the phyla and even classes of the animal kingdom originated in a rapid evolutionary radiation at the base of the Cambrian at 545 million yr ago (Ma) or 10–15 Ma before this date—rests on the sudden appearance of a diverse range of animals in the fossil record.”
- Also stated in: § RESULTS · plain
“The Cambrian explosion hypothesis rests on the interpretation of the sudden appearance of metazoans in the fossil record as evidence for a rapid radiation of animals late in the Proterozoic.”
plaindirect- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim.
- Also stated in: § RESULTS · plain
In the paper
“Pre-Vendian animals are likely to have been small and soft-bodied, because known fossils of Precambrian animals lack hard parts (26) and thus would have had poor fossilization potential.”
What the sources say
- Not checked yetcites [26] source
hedgeddirect- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
The paper states this without a source or data behind it here, so there is nothing to check it against. The quote shows it is in the paper.
In the paper
“Although we cannot provide precise estimates of the origin of metazoan phyla, we can use our results to confidently reject the Cambrian explosion hypothesis, which rests on a literal interpretation of the fossil record and assumes that special evolutionary phenomena, capable of producing profound differentiation in a short period, operated in the Cambrian but not before or since.”
plain- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim.
In the paper
“We note that the branching order of phyla on the “tree of life” is still controversial (we have used the tree from ref. 17 for illustrative purposes because it is largely based on morphology) but all versions express these two fundamental dichotomies regardless of differences elsewhere in the tree.”
What the sources say
- Not checked yetcites ref. 17
plain- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The shorter confidence intervals of mitochondrial estimates may result from longer sequences and a better fit between model and data.”
hedgedconditional- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“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 Bromham et al., 1998
Experimental — accuracy not yet measuredIn the citing paper
“But molecular dates for the origins of animal phyla 27 and orders of mammals and birds 68 are generally twice as old as the dates of origin indicated by the fossil record.”
From The modern molecular clock (2003) · cites this paper as [27]
In the citing paper
“First, the sloppy nature of the substitution rate results in large variance around the amount of genetic difference expected for any given time period, adding a large degree of imprecision to molecular date estimates 27 .”
From The modern molecular clock (2003) · cites this paper as [27]
In the citing paper
“Such confidence intervals allow molecular dates to be used to test evolutionary hypotheses within the bounds of the accuracy and precision of molecular clocks, by asking whether the range of possible date estimates is consistent with a specific evolutionary hypotheses 26 (for example, that the animal phyla arose in the early Cambrian 27 ) (BOX 2).”
From The modern molecular clock (2003) · cites this paper as [27]
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 [14]
Citations
Cites
Evolutionary trees from DNA sequences: A maximum likelihood approach.
Felsenstein, J. (1981) · Journal of Molecular Evolution · doi:10.1007/bf01734359 · Cited by 14,571
Dating of the human–ape splitting by a molecular clock of mitochondrial DNA.
Hasegawa, M., Kishino, H., & Yano, T.-A. (1985) · Journal of Molecular Evolution · doi:10.1007/bf02101694 · Cited by 8,687
Yang, Z. (1994) · Journal of Molecular Evolution · doi:10.1007/bf00160154 · Cited by 2,960
Rambaut, A., & Grass, N. C. (1997) · Computer applications in the biosciences · doi:10.1093/bioinformatics/13.3.235 · Cited by 1,545
Self-citationAmong-site rate variation and its impact on phylogenetic analyses
Yang, Z. (1996) · Trends in Ecology & Evolution · doi:10.1016/0169-5347(96)10041-0 · Cited by 1,202
Animal evolution: interrelationships of the living phyla
(2012) · Choice Reviews Online · doi:10.5860/choice.50-1469 · Cited by 1,041
Three-dimensional preservation of algae and animal embryos in a Neoproterozoic phosphorite
Xiao, S., Zhang, Y., & Knoll, A. H. (1998) · Nature · doi:10.1038/35318 · Cited by 783
Statistical tests of models of DNA substitution
Goldman, N. (1993) · Journal of Molecular Evolution · doi:10.1007/bf00166252 · Cited by 736
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
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
Research works printed but not linked: 3
- A Rambaut, N C Grassly Comput Appl Biosci 13, 235–238 (1997).
- W C Wheeler, R L Honeycutt Mol Biol Evol 5, 90–96 (1988).
- M T Dixon, D M Hillis Mol Biol Evol 10, 256–267 (1993).
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Knoll, A. H., & Carroll, S. B. (1999) · Science · doi:10.1126/science.284.5423.2129 · Cited by 821
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Shu, D.-G., Luo, H.-L., Conway Morris, S., Zhang, X.-L., Hu, S.-X., Chen, L., Han, J., Zhu, M., Li, Y., & Chen, L.-Z. (1999) · Nature · doi:10.1038/46965 · Cited by 459
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Donoghue, P. C. J., & Benton, M. J. (2007) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2007.05.005 · Cited by 413
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Maloof, A. C., Porter, S. M., Moore, J. L., Dudas, F. O., Bowring, S. A., Higgins, J. A., Fike, D. A., & Eddy, M. P. (2010) · Geological Society of America Bulletin · doi:10.1130/b30346.1 · Cited by 419
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Brochu, C. A. (2003) · Annual Review of Earth and Planetary Sciences · doi:10.1146/annurev.earth.31.100901.141308 · Cited by 410
Peterson, K. J., & Butterfield, N. J. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503660102 · Cited by 361
Xiao, S., Yuan, X., Steiner, M., & Knoll, A. H. (2002) · Journal of Paleontology · doi:10.1666/0022-3360(2002)076 · Cited by 370
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Reisz, R. R., & Müller, J. (2004) · Trends in Genetics · doi:10.1016/j.tig.2004.03.007 · Cited by 170
Aris-Brosou, S. (2003) · Molecular Biology and Evolution · doi:10.1093/molbev/msg226 · Cited by 164
Bromham, L. D., & Degnan, B. M. (1999) · Evolution & Development · doi:10.1046/j.1525-142x.1999.99026.x · Cited by 155
Self-citationEvolution of centralized nervous systems: Two schools of evolutionary thought
Northcutt, R. G. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1201889109 · Cited by 141
Steiper, M. E., Young, N. M., & Sukarna, T. Y. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0407270101 · Cited by 149
A critical reappraisal of the fossil record of the bilaterian phyla
BUDD, G. E., & JENSEN, S. (2000) · Biological Reviews · doi:10.1111/j.1469-185x.1999.tb00046.x · Cited by 145
Discoidal Impressions and Trace-Like Fossils More Than 1200 Million Years Old
Rasmussen, B., Bengtson, S., Fletcher, I. R., & McNaughton, N. J. (2002) · Science · doi:10.1126/science.1070166 · Cited by 145
Molecular Clock Calibrations and Metazoan Divergence Dates
Lee, M. S. Y. (1999) · Journal of Molecular Evolution · doi:10.1007/pl00006562 · Cited by 142
Triggers for the Cambrian explosion: Hypotheses and problems
Zhang, X., Shu, D., Han, J., Zhang, Z., Liu, J., & Fu, D. (2014) · Gondwana Research · doi:10.1016/j.gr.2013.06.001 · Cited by 140
Bilaterian Origins: Significance of New Experimental Observations
Peterson, K. J., Cameron, R. A., & Davidson, E. H. (2000) · Developmental Biology · doi:10.1006/dbio.1999.9475 · Cited by 133
Bayesian Phylogenetic Analysis Supports Monophyly of Ambulacraria and of Cyclostomes
Furlong, R. F., & Holland, P. W. H. (2002) · ZOOLOGICAL SCIENCE · doi:10.2108/zsj.19.593 · Cited by 133
Why are human G-protein-coupled receptors predominantly intronless?
Gentles, A. J., & Karlin, S. (1999) · Trends in Genetics · doi:10.1016/s0168-9525(98)01648-5 · Cited by 131
Dating the arthropod tree based on large-scale transcriptome data
Rehm, P., Borner, J., Meusemann, K., von Reumont, B. M., Simon, S., Hadrys, H., Misof, B., & Burmester, T. (2011) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2011.09.003 · Cited by 121
The Origin of Animal Body Plans
Erwin, D. H., Valentine, J. W., & Jablonski, D. (1997) · American Scientist · Cited by 125
Fedonkin, M. A., Simonetta, A., & Ivantsov, A. Y. (2007) · Geological Society, London, Special Publications · doi:10.1144/sp286.12 · Cited by 116
Steroid and sterol 7-hydroxylation: ancient pathways.
Lathe, R. (2002) · Steroids · doi:10.1016/s0039-128x(02)00044-2 · Cited by 104
Meert, J. G., & Lieberman, B. S. (2004) · Journal of the Geological Society · doi:10.1144/0016-764903-107 · Cited by 104
Origins, Evolution, and Diversification of Zooplankton
Rigby, S., & Milsom, C. V. (2000) · Annual Review of Ecology and Systematics · doi:10.1146/annurev.ecolsys.31.1.293 · Cited by 101
Chandler, M. A., & Sohl, L. E. (2000) · Journal of Geophysical Research Atmospheres · doi:10.1029/2000jd900221 · Cited by 102
Wonderful strife: systematics, stem groups, and the phylogenetic signal of the Cambrian radiation
Briggs, D. E. G., & Fortey, R. A. (2005) · Paleobiology · doi:10.1666/0094-8373(2005)031[0094:wsssga]2.0.co;2 · Cited by 98
Self-citationAccounting for phylogenetic uncertainty in comparative studies of evolution and adaptation
Pagel, M. D., & Lutzoni, F. M. (2007) · Springer eBooks · doi:10.1007/3-540-45692-9_8 · Cited by 92
The Cambrian "explosion" of metazoans and molecular biology: would Darwin be satisfied?
Conway-Morris, S. (2003) · The International Journal of Developmental Biology · doi:10.1387/ijdb.14756326 · Cited by 89
Penny, D., Hasegawa, M., Waddell, P. J., & Hendy, M. D. (1999) · Systematic Biology · doi:10.1080/106351599260454 · Cited by 86
Self-citationA More Comprehensive Habitable Zone for Finding Life on Other Planets
Ramirez, R. M. (2018) · Geosciences · doi:10.3390/geosciences8080280 · Cited by 92
Early Evolution of the Bilateria
Hausdorf, B. (2000) · Systematic Biology · doi:10.1080/10635150050207438 · Cited by 83
CO2 levels required for deglaciation of a “near‐snowball” Earth
Crowley, T. J., Hyde, W. T., & Peltier, W. R. (2001) · Geophysical Research Letters · doi:10.1029/2000gl011836 · Cited by 79
Morris, S. C. (2000) · Cell · doi:10.1016/s0092-8674(00)81679-7 · Cited by 78
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Bromham, L. D. (2019) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2019.01.017 · Cited by 75
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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
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
Kawashita, S. Y., Sanson, G. F. O., Fernandes, O., Zingales, B. S., & Briones, M. R. S. (2001) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a003771 · Cited by 74
Toffoli, D., Hrbek, T., de Araújo, M. L. G., Almeida, M. P. D., Charvet, P., & Farias, I. P. (2008) · Genetics and Molecular Biology · doi:10.1590/s1415-47572008000200028 · Cited by 73
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
Molecular 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
Bromham, L. D., & Woolfit, M. (2004) · Systematic Biology · doi:10.1080/10635150490522278 · Cited by 66
Self-citationSchenk, J. J., & Hufford, L. D. (2010) · Systematic Botany · doi:10.1600/036364410792495809 · Cited by 60
Molecular dates for the “cambrian explosion”: The influence of prior assumptions.
Welch, J. J., Fontanillas, E., & Bromham, L. (2005) · Systematic Biology · doi:10.1080/10635150590947212 · Cited by 53
Self-citationA Parvancorina -like arthropod from the Cambrian of South China
Lin, J.-P., Gon, S. M., Gehling, J. G., Babcock, L. E., Zhao, Y.-L., Zhang, X.-L., Hu, S.-X., Yuan, J.-L., Yu, M.-Y., & Peng, J. (2006) · Historical Biology · doi:10.1080/08912960500508689 · Cited by 53
Molecular clocks and the early evolution of metazoan nervous systems
Wray, G. A. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2015.0046 · Cited by 51
Can fast early rates reconcile molecular dates with the Cambrian explosion?
Bromham, L. D., & Hendy, M. D. (2000) · Proceedings of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rspb.2000.1108 · Cited by 50
Self-citationCALIBRATION AGE AND QUARTET DIVERGENCE DATE ESTIMATION
Brochu, C. A. (2004) · Evolution · doi:10.1111/j.0014-3820.2004.tb01715.x · Cited by 47
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Bromham, L. (2003) · Journal of Molecular Evolution · doi:10.1007/s00239-003-0002-7 · Cited by 40
Self-citationHybridization in the evolution of animal form and life-cycle
Williamson, D. I. (2006) · Zoological Journal of the Linnean Society · doi:10.1111/j.1096-3642.2006.00236.x · Cited by 42
Taking the Pulse of the Cambrian Radiation
Lieberman, B. S. (2003) · Integrative and Comparative Biology · doi:10.1093/icb/43.1.229 · Cited by 41
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Bromham, L. D. (2003) · Integrative and Comparative Biology · doi:10.1093/icb/43.1.148 · Cited by 42
Self-citationNeoproterozoic Glaciations and the Fossil Record
Xiao, S. (2011) · Geophysical monograph · doi:10.1029/146gm16 · Cited by 41
The Fact of Evolution: Implications for Science Education
Hofmann, J. R., & Weber, B. H. (2003) · Science & Education · doi:10.1023/b:sced.0000004556.80802.3a · Cited by 39
The Lantian biota: A new window onto the origin and early evolution of multicellular organisms
Yuan, X., Chen, Z., Xiao, S., Wan, B., Guan, C., Wang, W., Zhou, C., & Hua, H. (2012) · Chinese Science Bulletin · doi:10.1007/s11434-012-5483-6 · Cited by 40
Cooke, T. J., Poli, D., & Cohen, J. D. (2004) · Elsevier eBooks · doi:10.1016/b978-012339552-8/50006-8 · Cited by 37
Dating branches on the tree of life using DNA.
Wray, G. A. (2001) · Genome biology · doi:10.1186/gb-2001-3-1-reviews0001 · Cited by 37
Chen, J., Waloszek, D., Maas, A., Braun, A., Huang, D., Wang, X., & Stein, M. (2007) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2007.03.018 · Cited by 36
Evolutionary challenges of extreme environments (part 2)
Waterman, T. H. (2001) · Journal of Experimental Zoology · doi:10.1002/jez.1065 · Cited by 32
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Lieberman, B. S. (2001) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2001.1712 · Cited by 31
Aguileta, G., Bielawski, J. P., & Yang, Z. (2006) · Gene · doi:10.1016/j.gene.2006.04.019 · Cited by 31
The Cambrian Explosion Exploded?
Fortey, R. A. (2001) · Science · doi:10.1126/science.1062987 · Cited by 28
Self-citationChand, D. S., de Lannoy, L., Tucker, R. P., & Lovejoy, D. A. (2013) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2013.02.006 · Cited by 27
Ōtsuka, J., & Sugaya, N. (2003) · Journal of Theoretical Biology · doi:10.1016/s0022-5193(03)00057-2 · Cited by 27
Taphonomic alteration and evolutionary taphonomy
López, S. R. F. (2006) · LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) · Cited by 25
The evolutionary history of krill inferred from nuclear large subunit rDNA sequence analysis
Jarman, S. (2001) · Biological Journal of the Linnean Society · doi:10.1006/bijl.2001.0538 · Cited by 24
Global Rate Variation in Bony Vertebrates
Takezaki, N. (2018) · Genome Biology and Evolution · doi:10.1093/gbe/evy125 · Cited by 21
Arthur, W., & Kettle, C. J. (2001) · Evolution & Development · doi:10.1046/j.1525-142x.2001.00083.x · Cited by 21
Sanson, G. F. O., Kawashita, S. Y., Brunstein, A., & Briones, M. R. S. (2002) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a004069 · Cited by 21
The genetic response to Snowball Earth: role of HSP90 in the Cambrian explosion
Baker, M. E. (2006) · Geobiology · doi:10.1111/j.1472-4669.2006.00067.x · Cited by 19
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
Eukaryotization of the early biosphere: A biogeochemical aspect
Fedonkin, M. A. (2009) · Geochemistry International · doi:10.1134/s0016702909130011 · Cited by 15
Reconstructing Divergence Times for Supertrees
Vos, R. A., & Mooers, A. Ø. (2004) · Computational biology · doi:10.1007/978-1-4020-2330-9_14 · Cited by 14
Mónge-Nájera, J., & Hou, X. (1969) · Revista de Biología Tropical · doi:10.15517/rbt.v48i2-3.18718 · Cited by 13
Blaxter, M. (2001) · Nature · doi:10.1038/35093191 · Cited by 13
Metadata
- Authors
- Bromham, L., Rambaut, A., Fortey, R., Cooper, A., & Penny, D.
- Affiliations
- Natural History Museum (GB)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 1998-10-13
- Volume
- 95
- Issue
- 21
- Pages
- 12386-12389
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC22841
- OpenAlex
- W2126267818
- Cited by
- 148
- References
- 35
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 2 · 2023: 2 · 2022: 3 · 2021: 1 · 2020: 1 · 2019: 1 · 2018: 4 · 2017: 1 · 2016: 1 · 2015: 1 · 2013: 5 · 2012: 3
- FWCI
- 17.68
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Figshare (submittedVersion, cc-by)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, other-oa)
- Funders
- Wellcome Trust
- 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 › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Protist diversity and phylogeny
- Keywords
- Cambrian explosion, divergence time estimation, metazoan origin, confidence intervals
- MeSH terms
- Animals, Biological Evolution, Models, Biological, RNA, Ribosomal, Confidence Intervals, Likelihood Functions
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