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.
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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
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- Findingown data§ RESULTS
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.
“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).”
Quote in the paperSubstantial claim - Findingown data§ RESULTS
The majority of the quartets were rejected.
“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.”
Quote in the paperSubstantial claim - Premisecitation§ RESULTS
Underestimating the degree of rate heterogeneity between sites will tend to underestimate the dates of divergence caused by a nonlinear effect of heterogeneity on branch length.
“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.”
Quote in the paperSubstantial claim0 of 2 sources checked- cites [16]
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- cites [25] source
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- Interpretationown data§ RESULTS
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.
“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.”
Quote in the paperSubstantial claim - Interpretationreasoning§ RESULTS
Rate heterogeneity is widespread among metazoan taxa for these sequences.
“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.”
Quote in the paperSubstantial claim
- Interpretationreasoning§ RESULTS
The difference in the date estimates from our two sets of sequences illustrates the importance of basing estimates on several sequences.
“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.”
Quote in the paperSubstantial claim - Interpretationown data§ RESULTS
The absence of appropriate Precambrian fossils is not necessarily evidence for an explosive evolutionary radiation near the beginning of the Cambrian period.
“Therefore, the absence of appropriate Precambrian fossils is not necessarily evidence for an explosive evolutionary radiation near the beginning of the Cambrian period.”
Quote in the paperSubstantial claim - Interpretationown data§ Abstract
The molecular data provide additional support for an extended period of Precambrian metazoan diversification.
“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.”
Quote in the paperSubstantial claim - Interpretationcitation§ RESULTS
All sister taxa to the dated nodes, such as Brachiopoda, Porifera, and Cnidaria, must also have been present before the Vendian period (600 Ma), despite the lack of earlier fossils.
“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.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [17]
Not checked in the free run.
- Study design and conductreasoning§ Abstract
The method presented here is more reliable than previous molecular dating techniques.
“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.”
Quote in the paperSubstantial claim0 of 5 sources checked - Also stated in: § RESULTS · boosted
- Interpretationcitation§ RESULTS
It seems probable that metazoan diversity is recorded for the first time in the Cambrian because of a combination of ideal fossilization conditions and the advent of hard parts, or larger bodies, or both, that made many animal lineages "visible" in the fossil record.
“It seems probable that metazoan diversity is recorded for the first time in the Cambrian because of a combination of ideal fossilization conditions and the advent of hard parts, or larger bodies, or both, that made many animal lineages “visible” in the fossil record (7).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [7] source
Not checked in the free run.
- Interpretationown data§ RESULTS
Testing each comparison separately is valuable rather than basing the expectation of clock-like evolution on inferred general trends.
“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.”
Quote in the paperSubstantial claim - Interpretationown data§ RESULTS
We can use our results to confidently reject the Cambrian explosion hypothesis.
“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.”
Quote in the paperSubstantial claim - Interpretationreasoning§ RESULTS
The evolution of protein-coding genes is likely to be more accurately modeled than rRNA.
“The evolution of protein-coding genes is likely to be more accurately modeled than rRNA.”
Quote in the paperSubstantial claim - Interpretationown data§ Abstract
The molecular data are not compatible with the Cambrian explosion hypothesis as an explanation for the origin of metazoan phyla.
“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.”
Quote in the paperSubstantial claim - Interpretationown data§ RESULTS
Our results indicate that more metazoan lineages may have been present in the Precambrian than were unequivocally recorded in the fossil record.
“Our results indicate that more metazoan lineages may have been present in the Precambrian than were unequivocally recorded in the fossil record.”
Quote in the paperSubstantial claim
- May combine two claims. 10
- Classified as probably not a substantial claim. 9
May combine two claims.
Findingown data§ RESULTSThe confidence intervals permit exclusion of 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.
“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.”
Quote in the paperSubstantial claimMay combine two claims.
Findingcitation§ RESULTSThe confidence intervals are wide, as expected for molecular date estimates, therefore these results cannot be used to put an absolute date on the origin of phyla.
“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.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [8]
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Findingown data§ METHODSFor the mitochondrial DNA, the transition/transversion ratio was 1.21 and gamma shape parameter was 0.38; for the 18S rRNA, these parameters were 1.74 and 0.38, respectively.
“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.”
Quote in the paperNot a substantial claimMay combine two claims.
Premisecitation§ RESULTSOne aspect of the evolution of rRNA that is not adequately modeled is the evolution of paired sites, 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.
“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.”
Quote in the paperSubstantial claim0 of 2 sources checked- cites [18]
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- cites [19]
Not checked in the free run.
Classified as probably not a substantial claim. May combine two claims.
Study design and conductnone given§ METHODSThe use of many dates permits testing for rate constancy between taxa and avoids reliance on a single calibration rate to date all lineages.
“The use of many dates permits testing for rate constancy between taxa and avoids reliance on a single calibration rate to date all lineages.”
Quote in the paperSubstantial claimClassified as probably not a substantial claim.
Premisecitation§ AbstractThe absence of earlier metazoan fossils could be caused by systematic biases in preservation that left the Precambrian history of recognized phyla unrecorded.
“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).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [7] source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
Interpretationcitation§ RESULTSOur findings are in broad agreement with some earlier molecular studies, despite differences in method and sequences used.
“Our findings are in broad agreement with some earlier molecular studies (20–22), despite differences in method and sequences used.”
Quote in the paperNot a substantial claim0 of 3 sources checkedMay combine two claims.
Premisecitation§ AbstractThe uncertainty in phylogenetic reconstruction and the stochastic nature of the molecular clock preclude precise dating, but when the imprecision is expressed as appropriate confidence intervals, molecular data are ideally suited to testing specific hypotheses.
“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.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [8]
Not checked in the free run.
Probably not a substantial claim: may not pass S2 (checkable), S4 (based). May combine two claims.
Premisenone given§ RESULTSThe 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.
“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.”
Quote in the paperNot a substantial claimClassified as probably not a substantial claim.
Premisenone given§ RESULTSMolecular 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.
“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.”
Quote in the paperSubstantial claimClassified as probably not a substantial claim.
Premisenone given§ AbstractThe Cambrian explosion hypothesis rests on the sudden appearance of a diverse range of animals in the fossil record.
“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.”
Quote in the paperSubstantial claim- Also stated in: § RESULTS · plain
May combine two claims.
Interpretationcitation§ RESULTSPre-Vendian animals are likely to have been small and soft-bodied, because known fossils of Precambrian animals lack hard parts and thus would have had poor fossilization potential.
“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.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [26] source
Not checked in the free run.
Classified as probably not a substantial claim.
Premisenone given§ RESULTSThe Cambrian explosion hypothesis assumes that special evolutionary phenomena, capable of producing profound differentiation in a short period, operated in the Cambrian but not before or since.
“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.”
Quote in the paperSubstantial claimClassified as probably not a substantial claim. May combine two claims.
Premisecitation§ RESULTSThe branching order of phyla on the "tree of life" is still controversial, but all versions express the two fundamental dichotomies (echinoderm-vertebrate and protostome-deuterostome) regardless of differences elsewhere.
“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.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites ref. 17
Not checked in the free run.
May combine two claims.
Interpretationreasoning§ RESULTSThe shorter confidence intervals of mitochondrial estimates may result from longer sequences and a better fit between model and data.
“The shorter confidence intervals of mitochondrial estimates may result from longer sequences and a better fit between model and data.”
Quote in the paperNot a substantial claim
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?
Molecular clock estimates mostly place the latest PDA much deeper in time than the latest Neoproterozoic, with dates ranging from 600 to 1200 Mya depending on proteins, calibration points, and substitution models.
“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
The Results report divergence estimates older than 680 Ma and say estimates differ between the two sequence datasets; the Methods also describe multiple fossil calibrations and a substitution model. But the paper does not give the attributed 600–1200 Ma range, and its estimates have wide confidence intervals rather than precise dates. The cited paper therefore supports the general point about older, method-dependent molecular dates, not the stated range. (LLM, conf=0.84)
Experimental — accuracy not yet measuredMolecular dates for the origins of animal phyla and orders of mammals and birds are generally twice as old as the dates of origin indicated by the fossil record.
“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]
The sloppy nature of the substitution rate results in large variance around the amount of genetic difference expected for any given time period, adding imprecision to molecular date estimates.
“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]
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 hypothesis.
“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]
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 Ma ago.
“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]
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- 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
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › 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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