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
AI snapshot
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.
Model-written summary. Check it against the paper before relying on it.
Integrity signals
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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.
- 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.
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
“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.
- 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.
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.
- 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.
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 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.
- 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.
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.
- 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.
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.
- 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.
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
“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.
- 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.
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 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.
- 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.
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.
- 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.
- 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.
- 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.
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.
- 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.
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.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
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.
- 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.
It may state two separate claims as one.
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.
- 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.
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.
- 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.
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.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
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.
- 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.
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.
- Checkable: fails — It may be too vague to check against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: fails — The paper may give no reason why it holds.
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.
- 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.
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.
- 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.
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.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: unclear — It is unclear whether the paper’s conclusions depend on it.
- Based: passes — The paper gives a 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
“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.
- 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.
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.
- 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.
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.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: unclear — It is unclear whether the paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
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).
Cited by
Sorted by citations
Inferring the historical patterns of biological evolution
Pagel, M. (1999) · Nature · doi:10.1038/44766 · Cited by 5,200
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
Bromham, L., & Penny, D. (2003) · Nature Reviews Genetics · doi:10.1038/nrg1020 · Cited by 615
Self-citationEstimating Divergence Times from Molecular Data on Phylogenetic and Population Genetic Timescales
Arbogast, B. S., Edwards, S. V., Wakeley, J., Beerli, P., & Slowinski, J. B. (2002) · Annual Review of Ecology and Systematics · doi:10.1146/annurev.ecolsys.33.010802.150500 · Cited by 574
Inferring speciation times under an episodic molecular clock
Rannala, B., & Yang, Z. (2007) · Systematic Biology · doi:10.1080/10635150701420643 · Cited by 475
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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