The timing of eukaryotic evolution: Does a relaxed molecular clock reconcile proteins and fossils?
Open accessAbstract
The use of nucleotide and amino acid sequences allows improved understanding of the timing of evolutionary events of life on earth. Molecular estimates of divergence times are, however, controversial and are generally much more ancient than suggested by the fossil record. The limited number of genes and species explored and pervasive variations in evolutionary rates are the most likely sources of such discrepancies. Here we compared concatenated amino acid sequences of 129 proteins from 36 eukaryotes to determine the divergence times of several major clades, including animals, fungi, plants, and various protists. Due to significant variations in their evolutionary rates, and to handle the uncertainty of the fossil record, we used a Bayesian relaxed molecular clock simultaneously calibrated by six paleontological constraints. We show that, according to 95% credibility intervals, the eukaryotic kingdoms diversified 950–1,259 million years ago (Mya), animals diverged from choanoflagellates 761–957 Mya, and the debated age of the split between protostomes and deuterostomes occurred 642–761 Mya. The divergence times appeared to be robust with respect to prior assumptions and paleontological calibrations. Interestingly, these relaxed clock time estimates are much more recent than those obtained under the assumption of a global molecular clock, yet bilaterian diversification appears to be ≈100 million years more ancient than the Cambrian boundary.
AI snapshot
Written from the paper’s full text.
TL;DR
A Bayesian relaxed molecular clock applied to 129 concatenated proteins from 36 eukaryotes yields much more recent divergence times than a global molecular clock, while still placing bilaterian diversification ≈100 million years before the Cambrian boundary. The authors argue that relaxed-clock dates partially reconcile molecular and fossil evidence.
Key findings
- The major eukaryotic kingdoms diversified 950–1,259 Mya (mean 1,085), Plantae originated 892–1,162 Mya (mean 1,010), red algae branched off 825–1,061 Mya (mean 928), and stem land plants separated from green algae 662–812 Mya (mean 729).
- Animals diverged from choanoflagellates 761–957 Mya (mean 849), the protostome/deuterostome split occurred 642–761 Mya (mean 695), animals diverged from fungi 872–1,127 Mya (mean 983), and ascomycetes diverged from basidiomycetes ≈629–837 Mya (mean 727).
- Relaxed-clock estimates were on average 1.5 times more recent than a global-clock time scale; simulations showed that a global clock on variable-rate data overestimated ages (e.g., bilaterians 864 ± 9 Mya vs. expected 695 Mya; root 1,541 ± 14 Mya vs. expected 1,085 Mya).
- Missing data had little effect: across all nodes, the mean difference was −0.2% ± 2.8, and a 1,000-Myr change in the root prior changed posterior divergence ages by only 16 Myr on average.
Methods
- Concatenated amino acid sequences of 129 nuclear proteins from 36 animals, fungi, plants, and protists; after removing two-thirds of sites due to ambiguous alignment, 30,399 positions remained, with ≈25% missing character states. The tree was rooted by *Dictyostelium*, with an alternative kinetoplastid rooting also considered.
- Divergence times were estimated with a Bayesian relaxed molecular clock using `estbranches` and `divtime`, calibrated simultaneously by six independent paleontological constraints; MCMC runs used 10 million generations after 100,000 burn-in generations, with 95% credibility intervals.
- Simulation studies generated 10 matrices of 36 taxa and 30,399 amino acid positions under variable-rate and constant-rate models, and tested the impact of missing data and prior assumptions.
Limitations
- Stated: molecular dating is controversial; discrepancies arise from limited gene/species sampling, pervasive rate variation, and uncertainty in the fossil record. The authors note that calibration choice affects estimates, root location is uncertain among eukaryotes, ≈25% of amino acids are missing, and extrapolation beyond calibrations may bias deeper nodes.
- Stated: the six calibrations are restricted to green plants, animals, and fungi, so many protist divergences lack direct fossil calibration; improved gene and species sampling and more realistic rate models are needed.
- Evident from the text: some genes are absent for some taxa, and the study relies on prior gamma distributions for root age, root rate, and rate autocorrelation, although sensitivity analyses suggested posterior ages were only slightly sensitive to root-age priors.
Model-written summary. Check it against the paper before relying on it.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
0 of 49 cited sources checked · 0 supported · 0 flagged
- Findingown data§ Results
The major eukaryotic kingdoms diversified in less than 200 Myr after their basal split.
“followed by their diversification in <200 Myr (Fig. 1).”
Quote in the paperSubstantial claim - Findingown data§ Results
The divergence between animals and fungi was estimated 872-1,127 Mya (mean 983).
“The divergence between animals and fungi was, for example, estimated 872–1,127 Mya (mean 983 Mya)”
Quote in the paperSubstantial claim - Findingown data§ Results
The basal split between the major eukaryotic kingdoms documented here occurred 950-1,259 Mya (mean 1,085).
“Credibility intervals at 95% indicated that the basal split between the major eukaryotic kingdoms documented here occurred 950–1,259 Mya (mean 1,085), followed by their diversification in <200 Myr (Fig. 1).”
- Also stated in: § Abstract · hedged
“We show that, according to 95% credibility intervals, the eukaryotic kingdoms diversified 950–1,259 million years ago (Mya)”
Quote in the paperSubstantial claim - Also stated in: § Abstract · hedged
- Findingown data§ Results
The rate of amino acid replacements extensively changed among the eukaryote lineages analyzed.
“Thus, the rate of amino acid replacements extensively changed among the eukaryote lineages here analyzed.”
Quote in the paperSubstantial claim - Findingown data§ Results
Red algae branched off 825-1,061 Mya (mean 928).
“red algae branched off 825–1,061 Mya (mean 928)”
Quote in the paperSubstantial claim
- Findingown data§ Results
A likelihood ratio test significantly rejected the hypothesis of a clocklike behavior of the data (P < 0.0001).
“A likelihood ratio test significantly rejected the hypothesis of a clocklike behavior of our data (P < 0.0001).”
Quote in the paperSubstantial claim - Findingown data§ Results
The divergence between choanoflagellates and animals was estimated between 761 and 957 Mya (mean 849).
“The divergence between choanoflagellates and animals was estimated during the Late Proterozoic, between 761 and 957 Mya (mean 849).”
- Also stated in: § Abstract · plain
“animals diverged from choanoflagellates 761–957 Mya”
Quote in the paperSubstantial claim - Also stated in: § Abstract · plain
- Findingown data§ Results
Plantae originated 892-1,162 Mya (mean 1,010).
“Plantae originated 892–1,162 Mya (mean 1,010)”
Quote in the paperSubstantial claim - Findingown data§ Results
Stem land plants separated from green algae 662-812 Mya (mean 729).
“stem land plants separated from green algae 662–812 Mya (mean 729)”
Quote in the paperSubstantial claim - Findingown data§ Results
The divergence time between protostomes and deuterostomes was 642-761 Mya (mean 695).
“Interestingly, the divergence time between protostomes and deuterostomes (Fig. 1) was 642–761 Mya (mean 695).”
- Also stated in: § Abstract · plain
“the debated age of the split between protostomes and deuterostomes occurred 642–761 Mya”
Quote in the paperSubstantial claim - Also stated in: § Abstract · plain
- Findingown data§ Discussion
When a perfect molecular clock was constrained under the Bayesian approach, the Saccharomyces/Candida divergence was estimated at 439-468 Mya (mean 454).
“When we constrained a perfect molecular clock under the Bayesian approach, this divergence was estimated at 439–468 Mya (mean 454).”
Quote in the paperSubstantial claim - Findingown data§ Results
The minimum and maximum divergence time estimates may dramatically vary depending upon the choice of a given combination of fossil references.
“the minimum and maximum estimates may dramatically vary depending upon the choice of a given combination of fossil references (Table 2).”
Quote in the paperSubstantial claim - Findingown data§ Results
Divergence times averaged over all possibilities of using a given number of simultaneous calibrations do not vary much with the number of calibrations.
“Whereas divergence times averaged over all possibilities of using a given number of simultaneous calibrations seems not to vary much with those numbers”
Quote in the paperNot a substantial claim - Findingown data§ Results
Posterior divergence times appeared only slightly sensitive to huge changes in prior specification of root age.
“Posterior divergence times thus appeared only slightly sensitive to huge changes in prior specification of root age.”
Quote in the paperSubstantial claim - Findingown data§ Results
The kinetoplastid rooting involved deeper divergences among Plantae (899-1,191 Mya).
“The kinetoplastid rooting actually involved deeper divergences among Plantae (899–1,191 Mya).”
Quote in the paperNot a substantial claim - Findingown data§ Discussion
The use of simultaneous calibrations reduces the uncertainty on age estimates.
“Accordingly, we have shown that the use of simultaneous calibrations reduces the uncertainty on age estimates (Table 2).”
Quote in the paperSubstantial claim - Findingown data§ Results
A reduction of the uncertainty on divergence times was associated with an increase in the number of simultaneous calibrations.
“However, a reduction of the uncertainty on divergence times was clearly associated to the increase of the number of simultaneous calibrations.”
Quote in the paperSubstantial claim - Findingown data§ Discussion
Saccharomyces and Candida appear to be fast evolving.
“These two fungi appear to be fast evolving (data not shown)”
Quote in the paperSubstantial claim - Findingown data§ Results
Constant-rate extrapolations conducted with all other conditions being identical yield less accurate, i.e., 1.2-1.4 deeper divergence times when actual rates do vary.
“However, constant-rate extrapolations conducted with all other conditions being identical yield less accurate, i.e., 1.2–1.4 deeper divergence times when actual rates do vary.”
Quote in the paperSubstantial claim - Findingown data§ Results
Within fungi, the divergence between ascomycetes and basidiomycetes is estimated approximately 629-837 Mya (mean 727).
“Within fungi, the divergence between ascomycetes and basidiomycetes is estimated ≈629–837 Mya (mean 727)”
Quote in the paperNot a substantial claim - Findingown data§ Discussion
The relaxed clock approach retrieves the true divergence times when substitution rates are distributed according to the autocorrelated-rate model developed by Thorne et al.
“Moreover, the relaxed clock approach retrieves the true divergence times (Table 1) when substitution rates are distributed according to the autocorrelated-rate model developed by Thorne et al. (32).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [32] Thorne, J. L., Kishino, H. & Painter, I. S. (1998) Mol. Biol. Evol. 15, 1647-1657. [DOI] [PubMed] [Google Scholar] source
Not checked in the free run.
- Findingown data§ Abstract
The divergence times appeared to be robust with respect to prior assumptions and paleontological calibrations.
“The divergence times appeared to be robust with respect to prior assumptions and paleontological calibrations.”
Quote in the paperSubstantial claim - Findingreasoning§ Results
Under kinetoplastid rooting, the main clades of eukaryotes diverged earlier (1,042-1,412 Mya).
“The main clades of eukaryotes also diverged earlier (1,042–1,412 Mya; Fig. 4, which is published as supporting information on the PNAS web site)”
Quote in the paperNot a substantial claim - Findingown data§ Results
The random introduction of an additional 25% of missing data, yielding a data set with 50% of missing amino acids, again provides very similar dates relative to the original data set.
“Interestingly, the random introduction of an additional 25% of missing data, yielding a data set with 50% of missing amino acids, again provides very similar dates relative to the original data set (data not shown).”
Quote in the paperSubstantial claim - Findingcitation§ Discussion
The greatest discrepancy between age estimates without and with the clock assumption is observed for the Saccharomyces/Candida split, estimated at 168-308 (mean 235) Mya compared with 841 Mya.
“The greatest discrepancy between age estimates without and with the clock assumption is observed for the Saccharomyces/Candida split, here estimated at 168–308 (mean 235) Mya (Fig. 1) compared with 841 Mya (45).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [45] Heckman, D. S., Geiser, D. M., Eidell, B. R., Stauffer, R. L., Kardos, N. L. & Hedges, S. B. (2001) Science 293, 1129-1133. [DOI] [PubMed] [Google Scholar] source
Not checked in the free run.
- Findingcitation§ Results
The phylogeny resulting from the maximum likelihood analysis of the 30,399 unambiguously aligned amino acid positions is in agreement with current opinion about eukaryotic relationships.
“The phylogeny resulting from the maximum likelihood analysis of the 30,399 unambiguously aligned amino acid positions (Fig. 1) is in agreement with current opinion about eukaryotic relationships (44).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [44] Baldauf, S. L. (2003) Science 300, 1703-1706. [DOI] [PubMed] [Google Scholar] source
Not checked in the free run.
- Findingown data§ Discussion
The relaxed molecular clock datings appear to be robust to the specification of prior distributions on model parameters.
“Second, our relaxed molecular clock datings (Fig. 1) appear to be robust to the specification of prior distributions on model parameters.”
Quote in the paperSubstantial claim - Findingown data§ Results
Divergence time estimates under the single vertebrate calibration were on average 1.4 times deeper than those measured with the six calibrations.
“For example, divergence time estimates under the single vertebrate calibration were on average 1.4 times deeper than those measured with the six calibrations (Table 4, which is published as supporting information on the PNAS web site).”
Quote in the paperNot a substantial claim - Findingown data§ Results
For the root age, these values are twice less than the actual SD measured by the Bayesian approach.
“For the root age, these values are indeed twice less than the actual SD measured by the Bayesian approach.”
Quote in the paperNot a substantial claim - Findingown data§ Results
Under kinetoplastid rooting, bilaterian divergence times were 627-738 Mya.
“e.g., we obtained 627–738 Mya for bilaterians”
Quote in the paperNot a substantial claim - Findingown data§ Results
The datings were robust against the random exclusion of one or two calibration points.
“Importantly, our datings were robust against the random exclusion of one or two calibration points.”
Quote in the paperSubstantial claim - Findingcitation§ Discussion
The 129 proteins did not record the Late Precambrian episodic burst of evolutionary rates detected on 22 mitochondrial and nuclear genes.
“In particular, our 129 proteins did not record the Late Precambrian episodic burst of evolutionary rates detected on 22 mitochondrial and nuclear genes (22).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [22] Aris-Brosou, S. & Yang, Z. (2003) Mol. Biol. Evol. 20, 1947-1954. [DOI] [PubMed] [Google Scholar] source
Not checked in the free run.
- Findingown data§ Discussion
Simulation studies indicate that, at least in the present case, the autocorrelated rates model does not underestimate divergence times, neither on clocklike nor on relaxed clock sequences.
“Second, simulation studies (Table 1) indicate that, at least in the present case, the autocorrelated rates model does not underestimate divergence times, neither on clocklike nor on relaxed clock sequences.”
Quote in the paperSubstantial claim - Findingreasoning§ Results
This corresponds to variations of approximately +17 Myr to -25 Myr for a 1,000-Myr-old node.
“This corresponds to variations of approximately +17 Myr to -25 Myr for a 1,000-Myr-old node.”
Quote in the paperNot a substantial claim - Findingown data§ Discussion
On average, divergence times among eukaryotes were 1.7 times deeper with a global clock than with a relaxed clock.
“On average, the divergence times among eukaryotes were 1.7 times deeper with a global clock than with a relaxed clock (Table 5, which is published as supporting information on the PNAS web site).”
Quote in the paperSubstantial claim - Findingreasoning§ Discussion
The dating estimates are robust upon missing data.
“Nevertheless, our dating estimates are robust upon missing data (Fig. 3, which is published as supporting information on the PNAS web site).”
Quote in the paperSubstantial claim - Findingcitation§ Results
The molecular time scale for the major eukaryotic clades is on average 1.5 times more recent than the one based on a global clock.
“Our molecular time scale for the major eukaryotic clades is on average 1.5 times more recent than the one based on a global clock (12).”
- Also stated in: § Abstract · plain
“these relaxed clock time estimates are much more recent than those obtained under the assumption of a global molecular clock”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [12] Hedges, S. B. (2002) Nat. Rev. Genet. 3, 838-849. [DOI] [PubMed] [Google Scholar] source
Not checked in the free run.
- Also stated in: § Abstract · plain
- Findingown data§ Results
Divergence times in opisthokonts, especially among animals, were not sensitive to moving the root from the cellular slime mold branch to the kinetoplastid branch.
“Divergence times in opisthokonts, especially among animals, were not sensitive to this modification (e.g., we obtained 627–738 Mya for bilaterians).”
Quote in the paperSubstantial claim - Findingown data§ Discussion
Our reanalysis of this data set under the divtime relaxed molecular clock approach suggests a major incompatibility between "green" and "red" calibrations.
“Our reanalysis of this data set under the divtime relaxed molecular clock approach suggests a major incompatibility between “green” and “red” calibrations.”
Quote in the paperSubstantial claim - Findingown data§ Discussion
For bilaterians, the discrepancy between our molecular estimates (642-761 Mya) and the fossil record is reduced to a minimum of 40 Myr.
“For bilaterians, the discrepancy between our molecular estimates (642–761 Mya) and the fossil record (7) is reduced to a minimum of 40 Myr.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [7] Chen, J.-Y., Bottjer, D. J., Oliveri, P., Dornbos, S. Q., Gao, F., Ruffins, S., Chi, H., Li, C.-W. & Davidson, E. H. (2004) Science 305, 218-222. [DOI] [PubMed] [Google Scholar] source
Not checked in the free run.
- Findingown data§ Discussion
This is incompatible with the respective 1,174- to 1,222- and 594- to 603-Mya constraints used in reference (50).
“This is incompatible with the respective 1,174- to 1,222- and 594- to 603-Mya constraints used in reference (50).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [50] Yoon, H. S., Hackett, J. D., Ciniglia, C., Pinto, G. & Bhattacharya, D. (2004) Mol. Biol. Evol. 21, 809-818. [DOI] [PubMed] [Google Scholar] source
Not checked in the free run.
- Findingown data§ Discussion
Our molecular dating does not appear to be biased in such a systematic way.
“Interestingly, our molecular dating (Fig. 1) does not appear to be biased in such a systematic way.”
Quote in the paperSubstantial claim - Findingown data§ Discussion
The divergence between green plants and red algae was dated between 825 and 1,061 Mya.
“We dated the divergence between green plants and red algae between 825 and 1,061 Mya (Fig. 1)”
Quote in the paperSubstantial claim - Findingown data§ Discussion
The use of a relaxed molecular clock on the large data set estimated the diversification time of most extant eukaryotic kingdoms at ≈1,100 Mya in the mid-Proterozoic.
“The use of a relaxed molecular clock on our large data set estimated the diversification time of most extant eukaryotic kingdoms at ≈1,100 Mya in the mid-Proterozoic (Fig. 1).”
Quote in the paperSubstantial claim - Findingreasoning§ Discussion
If the latter two "red" calibrations are used, angiosperms, spermatophytes, and land plants would have diversified 106-336, 344-809, and 626-1,237 Mya.
“Reciprocally, if we use the latter two “red” calibrations, angiosperms, spermatophytes, and land plants would have diversified 106–336, 344–809, and 626–1,237 Mya.”
Quote in the paperSubstantial claim - Findingreasoning§ Discussion
Calibrations among land plants only yield a red algae/chlorobionts split between 925 and 1,576 Mya, a credibility interval that partially overlaps with ours.
“Actually, calibrations among land plants only yield a red algae/chlorobionts split between 925 and 1,576 Mya, a credibility interval that partially overlaps with ours.”
Quote in the paperNot a substantial claim - Interpretationcitation§ Results
The minimum gap between the protein relaxed clock timing and the first indisputable bilaterian fossil is approximately 40 Myr.
“reducing to ≈40 Myr the minimum gap between the protein relaxed clock timing and the first indisputable bilaterian fossil (7).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [7] Chen, J.-Y., Bottjer, D. J., Oliveri, P., Dornbos, S. Q., Gao, F., Ruffins, S., Chi, H., Li, C.-W. & Davidson, E. H. (2004) Science 305, 218-222. [DOI] [PubMed] [Google Scholar] source
Not checked in the free run.
- Premisecitation§ Abstract
Molecular estimates of divergence times are generally much more ancient than suggested by the fossil record.
“Molecular estimates of divergence times are, however, controversial and are generally much more ancient than suggested by the fossil record.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [12] Hedges, S. B. (2002) Nat. Rev. Genet. 3, 838-849. [DOI] [PubMed] [Google Scholar] source
Not checked in the free run.
- Interpretationown data§ Results
The secondary endosymbiosis event in which a red alga was engulfed and retained by a flagellate protist probably happened along the branch leading to stramenopiles + alveolates, between 767 and 1,072 Mya, shortly after the primary endosymbiosis.
“This event probably happened along the branch leading to stramenopiles + alveolates, i.e., between 767 and 1,072 Mya, shortly after the primary endosymbiosis (Fig. 1).”
Quote in the paperSubstantial claim- Rests on an assumption: Plastids surrounded by four membranes originated from secondary endosymbiosis, in which a red alga was engulfed and retained by a flagellate protist.
- Interpretationreasoning§ Results
The endosymbiosis of a free-living cyanobacterium that led to primary plastids occurred between 825 and 1,162 Mya.
“This suggests that the endosymbiosis of a free-living cyanobacterium that led to primary plastids (surrounded by two membranes) occurred between 825 and 1,162 Mya (Fig. 1).”
Quote in the paperSubstantial claim - Interpretationreasoning§ Results
The major transition during animal evolution from unicellular to multicellular state might have occurred at least 200 Myr before the Cambrian explosion.
“The major transition during animal evolution from unicellular to multicellular state might have thus occurred at least 200 Myr before the Cambrian explosion.”
Quote in the paperSubstantial claim - Interpretationown data§ Abstract
Bilaterian diversification appears to be approximately 100 million years more ancient than the Cambrian boundary.
“yet bilaterian diversification appears to be ≈100 million years more ancient than the Cambrian boundary.”
Quote in the paperSubstantial claim - Interpretationown data§ Results
The autocorrelation model of substitution-rate evolution does not underestimate ages on clocklike data.
“The simulations therefore indicate that the autocorrelation model of substitution-rate evolution does not underestimate ages on clocklike data”
Quote in the paperSubstantial claim - Interpretationreasoning§ Results
The earlier divergence of main eukaryotic clades under kinetoplastid rooting is likely because such an alternative root location involves a pectinate tree shape.
“likely because such an alternative root location involves a pectinate tree shape.”
Quote in the paperNot a substantial claim - Interpretationown data§ Results
A linear extrapolation on rate-variable data markedly overestimates divergence times.
“whereas a linear extrapolation on rate-variable data markedly overestimates divergence times (Table 1).”
Quote in the paperSubstantial claim - Premisecitation§ Results
The root location is uncertain among eukaryotes.
“Because the root location is uncertain among eukaryotes (44), we recalculated divergence times after moving the root from the branch leading to the cellular slime mold to the one leading to kinetoplastids (Fig. 1).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [44] Baldauf, S. L. (2003) Science 300, 1703-1706. [DOI] [PubMed] [Google Scholar] source
Not checked in the free run.
- Interpretationown data§ Discussion
The analyses have not been affected by a trend of increased rates far back in time.
“Two elements suggest that our analyses have not been affected by such a trend.”
Quote in the paperSubstantial claim - Premisecitation§ Discussion
A potentially reduced phylogenetic and/or dating accuracy associated with missing data is primarily caused by the occurrence of too few complete characters rather than too many missing positions.
“Indeed, a potentially reduced phylogenetic (and/or dating) accuracy associated with missing data is primarily caused by the occurrence of too few complete characters rather than too many missing positions (47).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [47] Wiens, J. J. (2003) Syst. Biol. 52, 528-538. [DOI] [PubMed] [Google Scholar] source
Not checked in the free run.
- Interpretationown data§ Results
The relaxed clock method is efficient, even when the alignment contains partial sequences.
“The relaxed clock method is therefore efficient, even when the alignment contains partial sequences.”
Quote in the paperNot a substantial claim - Interpretationreasoning§ Results
The Middle to Late Proterozoic cladogeneses among most eukaryotes were not the result of a rooting artifact.
“Thus, we confirm that the above-mentioned observations of Middle to Late Proterozoic cladogeneses among most eukaryotes were not the result of a rooting artifact.”
Quote in the paperSubstantial claim - Premisecitation§ Discussion
Two relaxed clock dating studies, among metazoans and photosynthetic eukaryotes, yielded results that are at first sight incongruent with our estimates.
“Recently, two relaxed clock dating studies, among metazoans (23) and photosynthetic eukaryotes (50), yielded results that are at first sight incongruent with our estimates.”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites [23] Peterson, K. J., Lyons, J. B., Nowak, K. S., Takacs, C. M., Wargo, M. J. & McPeek, M. A. (2004) Proc. Natl. Acad. Sci. USA 101, 6536-6541. [DOI] [PMC free article] [PubMed] [Google Scholar] source
Not checked in the free run.
- cites [50] Yoon, H. S., Hackett, J. D., Ciniglia, C., Pinto, G. & Bhattacharya, D. (2004) Mol. Biol. Evol. 21, 809-818. [DOI] [PubMed] [Google Scholar] source
Not checked in the free run.
- Interpretationown data§ Discussion
Such high rates are probably not accommodated by global clock based methods.
“and such high rates are probably not accommodated by global clock based methods.”
Quote in the paperSubstantial claim - Premisecitation§ Results
Molecular clock approaches are sensitive to the choice of calibrations.
“Molecular clock approaches are also sensitive to the choice of calibrations (48).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [48] Douzery, E. J. P., Delsuc, F., Stanhope, M. J. & Huchon, D. (2003) J. Mol. Evol. 57, S201-S213. [DOI] [PubMed] [Google Scholar] source
Not checked in the free run.
- Interpretationreasoning§ Discussion
Much posterior dating information regarding divergence times among eukaryotes is attributable to the 129 concatenated proteins rather than to prior specifications.
“This suggests that much posterior dating information regarding measure of divergence times among eukaryotes is attributable to the 129 concatenated proteins rather than to prior specifications.”
Quote in the paperSubstantial claim - Premisereasoning§ Discussion
Estimating a time scale by age extrapolation beyond animal, fungi, and plant calibrations may possibly lead to biased estimates.
“Estimating a time scale by the mean of age extrapolation beyond animal, fungi, and plant calibrations may possibly lead to biased estimates.”
Quote in the paperSubstantial claim - Study design and conductown data§ Discussion
The divergence time estimates should not be seriously affected by stochastic error because the study used a very large data set (129 genes; 30,399 amino acid positions).
“Our divergence time estimates should not be seriously affected by the stochastic error, because we used a very large data set (129 genes; 30,399 amino acid positions), corresponding to proteins involved in different functional pathways like translation, transcription, cytoskeleton, and metabolism.”
Quote in the paperSubstantial claim - Premisereasoning§ Discussion
Interpolation of date estimates is less biased than extrapolation because evolutionary rates are bounded by zero.
“Whereas interpolation of date estimates is certainly less biased because evolutionary rates are bounded by zero”
Quote in the paperSubstantial claim - Interpretationown data§ Discussion
The complete alignment retains a strong phylogenetic and dating signal because the shortest concatenated sequence includes 7,500 amino acids.
“Presently, because the shortest concatenated sequence includes 7,500 amino acids, our complete alignment retains a strong phylogenetic and dating signal.”
Quote in the paperSubstantial claim - Premisecitation§ Discussion
These estimates were obtained without taking into account among-site rate variation.
“Importantly, these estimates were obtained without taking into account among-site rate variation.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [23] Peterson, K. J., Lyons, J. B., Nowak, K. S., Takacs, C. M., Wargo, M. J. & McPeek, M. A. (2004) Proc. Natl. Acad. Sci. USA 101, 6536-6541. [DOI] [PMC free article] [PubMed] [Google Scholar] source
Not checked in the free run.
- Premisecitation§ Discussion
The age of the Bangiomorpha assemblage is bounded between 1,267 and 723 Mya.
“Illustrating the latter case, the age of the Bangiomorpha assemblage is in fact bounded between 1,267 and 723 Mya (52).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [52] Butterfield, N. J. (2001) Precamb. Res. 111, 235-256. [Google Scholar] source
Not checked in the free run.
- Interpretationreasoning§ Discussion
The stem lineages would have been organisms with a poor fossil record because of their small size, taphonomic problems, or undistinguishable morphology.
“This suggests that the stem lineages would have been organisms with a poor fossil record because of their small size, taphonomic problems, or undistinguishable morphology.”
Quote in the paperSubstantial claim - Premisecitation§ Discussion
Single fossils may also bear uncertainty in taxonomy identification and geological ages.
“Actually, single fossils may also bear their load of uncertainty in taxonomy identification and geological ages (11).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [11] Bromham, L. & Penny, D. (2003) Nat. Rev. Genet. 4, 216-224. [DOI] [PubMed] [Google Scholar] source
Not checked in the free run.
- Premisecitation§ Discussion
Deeper molecular dates are expected because the fossil record documents only the first appearance of a morphologically recognizable (crown) group and not the actual time of genetic divergence.
“Deeper molecular dates are actually expected, because the fossil record documents only the first appearance of a morphologically recognizable (crown) group and not the actual time of genetic divergence (51).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [51] Bromham, L., Phillips, M. J. & Penny, D. (1999) Trends Ecol. Evol. 14, 113-118. [DOI] [PubMed] [Google Scholar] source
Not checked in the free run.
- May combine two claims. 32
- Classified as probably not a substantial claim. 22
May combine two claims.
Findingown data§ ResultsTrypanosomes and nematodes evolved two and three times faster than mammals, respectively.
“For example, trypanosomes and nematodes evolved two and three times faster than mammals, respectively (data not shown).”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown data§ ResultsOn average, the relative differences are +1.7% and -2.5% for ages that are over- and underestimated by missing data.
“On average, the relative differences are, respectively, + 1.7% and -2.5% for ages that are over- and underestimated by missing data.”
Quote in the paperSubstantial claimMay combine two claims.
Findingcitation§ ResultsRelaxed clock timings were less precise than global clock estimates, as attested by 95% credibility interval widths relative to global clock estimates, because of the greater number of parameters involved.
“They were also less precise, as attested by 95% credibility interval widths relative to global clock estimates, because of the greater number of parameters involved (22).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [22] Aris-Brosou, S. & Yang, Z. (2003) Mol. Biol. Evol. 20, 1947-1954. [DOI] [PubMed] [Google Scholar] source
Not checked in the free run.
May combine two claims.
Findingown data§ ResultsThe presence of missing data leads to slightly under- or overestimated divergence ages, depending on the node under focus, and induces a mean difference of -0.2% ± 2.8 over all nodes (extreme values, -9.8 to +8.7%).
“The presence of missing data leads to slightly under- or overestimated divergence ages, depending on the node under focus, and induces a mean difference of -0.2% ± 2.8 over all nodes (extreme values, -9.8 to + 8.7%).”
Quote in the paperSubstantial claimMay combine two claims.
Findingown data§ DiscussionNo trend toward a rate increase far back in time is observed, and the rate for the last common bilaterian ancestor is close to the mean rate measured along the eukaryotic phylogeny.
“No trend toward a rate increase far back in time is observed, and the rate for the last common bilaterian ancestor is close to the mean rate measured along the eukaryotic phylogeny.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Findingnone given§ DiscussionThe study sampled a reasonable taxonomic diversity (36 species), contrary to all previous studies with such a large sample of genes.
“Contrary to all previous studies with such a large sample of genes, a reasonable taxonomic diversity (36 species) was sampled.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown data§ DiscussionThe greatest contrast (ratio >2.0) between global and relaxed clock ages is observed for alveolates, nematodes, and kinetoplastids, the fastest-evolving taxa for the 129 proteins evaluated.
“The greatest contrast (ratio >2.0) between global and relaxed clock ages is observed for alveolates, nematodes, and kinetoplastids, i.e., the fastest-evolving taxa for the 129 proteins here evaluated.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown data§ ResultsA 1,000-Myr variation of the root prior will involve a posterior divergence age variation of only 16 Myr, which is far less than the order of magnitude of the uncertainty on the divergence ages themselves.
“Such an average impact over all nodes indicated that a 1,000-Myr variation of the root prior will involve a posterior divergence age variation of only 16 Myr, which is far less than the order of magnitude of the uncertainty on the divergence ages themselves.”
Quote in the paperSubstantial claimMay combine two claims.
Findingown data§ DiscussionHalf of the total number of proteins contains at most three missing taxa over 36, and 25% of the amino acids are missing in the final alignment.
“Here, half of the total number of proteins contains at most three missing taxa over 36, and 25% of the amino acids are missing in our final alignment.”
Quote in the paperSubstantial claimMay combine two claims.
Findingown data§ ResultsRelaxed clock timings were accurate, although slightly deeper when estimated on constant-rate data.
“Relaxed clock timings were accurate, although slightly deeper when estimated on constant-rate data.”
Quote in the paperSubstantial claimMay combine two claims.
Findingown data§ ResultsComparison of a priori and a posteriori age estimates for calibration nodes did not reveal any systematic trend, suggesting that paleontological uncertainties did not bias the calculations, because they were incorporated in the dating.
“Furthermore, comparison of a priori and a posteriori age estimates for calibration nodes did not reveal any systematic trend (Table 3, which is published as supporting information on the PNAS web site), suggesting that paleontological uncertainties did not bias our calculations, because they were incorporated in the dating”
Quote in the paperSubstantial claimMay combine two claims.
Findingown data§ DiscussionUnder the maximum likelihood topology inferred from the five plastid proteins, and enforcing the angiosperms, spermatophytes, and land plant nodes between 90 and 130, 290 and 320, and 432 and 476 Mya, red algae diversification would be between 392 and 761 Mya (mean 551 Mya) and a Chondrus/Palmaria split between 165 and 381 Mya.
“Under the maximum likelihood topology inferred from the five plastid proteins, and enforcing the angiosperms, spermatophytes, and land plant nodes between 90 and 130, 290 and 320, and 432 and 476 Mya (50), would involve a red algae diversification between 392 and 761 Mya (mean 551 Mya) and a Chondrus/Palmaria split between 165 and 381 Mya.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [50] Yoon, H. S., Hackett, J. D., Ciniglia, C., Pinto, G. & Bhattacharya, D. (2004) Mol. Biol. Evol. 21, 809-818. [DOI] [PubMed] [Google Scholar]
Not checked in the free run.
May combine two claims.
Findingown data§ DiscussionMolecular ages are more recent than the fossil record for red algae but more ancient for animals.
“Molecular ages are more recent than the fossil record for red algae but more ancient for animals.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing), S4 (based). May combine two claims.
Findingnone given§ DiscussionClose to the Meso-/Neo-Proterozoic transition, choanoflagellates diverged from their closest animal relatives, marking the dawn of cellular cooperation in animals.
“Close to the Meso-/Neo-Proterozoic transition, choanoflagellates diverged from their closest animal relatives, marking the dawn of cellular cooperation in animals.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingcitation§ DiscussionMolecular dating with a kinetoplastid rooting would be in better agreement with this fossil (95% credibility interval, 899-1191), but such a rooting might represent a tree reconstruction artifact.
“Molecular dating with a kinetoplastid rooting would be in better agreement with this fossil (95% credibility interval, 899-1191; Fig. 1), but such a rooting might represent a tree reconstruction artifact (36).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [36] Philippe, H., Lopez, P., Brinkmann, H., Budin, K., Germot, A., Laurent, J., Moreira, D., Müller, M. & Le Guyader, H. (2000) Philos. Trans. R. Soc. London B 267, 1213-1221. [DOI] [PMC free article] [PubMed] [Google Scholar]
Not checked in the free run.
May combine two claims.
Interpretationown data§ ResultsThe protostome/deuterostome divergence estimate is much lower than most previously published estimates but close to recent estimates.
“This value is much lower than most of the previously published ones (12, 17, 46) but is close to recent estimates (22, 23)”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites [12] Hedges, S. B. (2002) Nat. Rev. Genet. 3, 838-849. [DOI] [PubMed] [Google Scholar] source
Not checked in the free run.
- cites [17] Wang, D. Y., Kumar, S. & Hedges, S. B. (1999) Proc. R. Soc. London Ser. B 266, 163-171. [DOI] [PMC free article] [PubMed] [Google Scholar] source
Not checked in the free run.
- cites [46] Wray, G. A., Levinton, J. S. & Shapiro, L. H. (1996) Science 274, 568-573. [Google Scholar] source
Not checked in the free run.
May combine two claims.
Interpretationnone given§ AbstractThe limited number of genes and species explored and pervasive variations in evolutionary rates are the most likely sources of discrepancies between molecular and fossil estimates.
“The limited number of genes and species explored and pervasive variations in evolutionary rates are the most likely sources of such discrepancies.”
Quote in the paperSubstantial claimClassified as probably not a substantial claim.
Study design and conductreasoning§ Materials and MethodsEach primary calibration was defined as a prior time constraint, with lower and/or upper bounds, to explicitly incorporate the inherent uncertainty of paleontological estimates.
“To explicitly incorporate the inherent uncertainty of paleontological estimates, each primary calibration was defined as a prior time constraint, with lower and/or upper bounds.”
Quote in the paperSubstantial claimClassified as probably not a substantial claim.
Premisecitation§ ResultsChanges in reference topology may potentially affect molecular dating.
“Changes in reference topology may potentially affect molecular dating (39).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [39] Sanderson, M. J. & Doyle, J. A. (2001) Am. J. Bot. 88, 1499-1516. [PubMed] [Google Scholar]
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
Premisereasoning§ DiscussionExtrapolation could lead to rates increasing on average when moving far back in time.
“extrapolation could conduct to rates increasing on average when moving far back in time.”
Quote in the paperNot a substantial claimMay combine two claims.
Premisecitation§ DiscussionA similar result was obtained for animals under various models of clock relaxation and for mitochondrial genomes of mammals.
“A similar result was obtained for animals under various models of clock relaxation (22, 28) and for mitochondrial genomes of mammals (29).”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites [22] Aris-Brosou, S. & Yang, Z. (2003) Mol. Biol. Evol. 20, 1947-1954. [DOI] [PubMed] [Google Scholar] source
Not checked in the free run.
- cites [28] Aris-Brosou, S. & Yang, Z. (2002) Syst. Biol. 51, 703-714. [DOI] [PubMed] [Google Scholar] source
Not checked in the free run.
- cites [29] Hasegawa, M., Thorne, J. L. & Kishino, H. (2003) Genes Genet. Syst. 78, 267-283. [DOI] [PubMed] [Google Scholar] source
Not checked in the free run.
May combine two claims.
Study design and conductcitation§ Materials and MethodsThe best topology was rooted by Dictyostelium, as suggested by a derived gene fusion separating opisthokonts from bikonts.
“The best topology (Fig. 1) was rooted by Dictyostelium, as suggested by a derived gene fusion separating opisthokonts (animals, choanoflagellates, and fungi) from bikonts (eukaryotes ancestrally with two cilia) (36, 37).”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites [36] Philippe, H., Lopez, P., Brinkmann, H., Budin, K., Germot, A., Laurent, J., Moreira, D., Müller, M. & Le Guyader, H. (2000) Philos. Trans. R. Soc. London B 267, 1213-1221. [DOI] [PMC free article] [PubMed] [Google Scholar]
Not checked in the free run.
- cites [37] Stechmann, A. & Cavalier-Smith, T. (2002) Science 297, 89-91. [DOI] [PubMed] [Google Scholar]
Not checked in the free run.
Classified as probably not a substantial claim. May combine two claims.
Study design and conductown data§ Materials and MethodsPosterior divergence times were identical for different MCMC started independently, evidencing convergence of the Bayesian dating procedure.
“Posterior divergence times were identical for different MCMC started independently, evidencing convergence of the Bayesian dating procedure.”
Quote in the paperSubstantial claimMay combine two claims.
Interpretationown data§ DiscussionThe concomitant use of six calibration constraints chosen among plants, fungi, and animals helped to more accurately measure the absolute amino acid replacement rates in these three clades and stabilized the Bayesian divergence times on the whole tree.
“Third, the concomitant use of six calibration constraints chosen among plants, fungi, and animals (Fig. 1) also helped to more accurately measure the absolute amino acid replacement rates in these three distinct clades and stabilized the Bayesian divergence times on the whole tree.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Premisecitation§ ResultsA recent study using a global clock method on a similar number of proteins, but a lower number of taxa and calibration points, yielded 1,200 Mya for the ascomycete/basidiomycete divergence.
“whereas a recent study using a global clock method on a similar number of proteins, but a lower number of taxa and calibration points, yielded 1,200 Mya (45).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [45] Heckman, D. S., Geiser, D. M., Eidell, B. R., Stauffer, R. L., Kardos, N. L. & Hedges, S. B. (2001) Science 293, 1129-1133. [DOI] [PubMed] [Google Scholar]
Not checked in the free run.
Classified as probably not a substantial claim.
Study design and conductcitation§ Materials and MethodsDivergence times were estimated under a Bayesian relaxed molecular clock constrained by six independent fossil references.
“Divergence times were estimated under a Bayesian relaxed molecular clock (33), constrained by six independent fossil references.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [33] Kishino, H., Thorne, J. L. & Bruno, W. J. (2001) Mol. Biol. Evol. 18, 352-361. [DOI] [PubMed] [Google Scholar] source
Not checked in the free run.
Classified as probably not a substantial claim.
Study design and conductown data§ Materials and MethodsTwo-thirds of the sites were conservatively removed due to ambiguous alignment to ensure the sitewise homology of the remaining 30,399 positions at this deep evolutionary time scale.
“Due to ambiguous alignment, two-thirds of the sites were conservatively removed to ensure the sitewise homology of the remaining 30,399 positions at this deep evolutionary time scale.”
Quote in the paperSubstantial claimClassified as probably not a substantial claim. May combine two claims.
Interpretationreasoning§ DiscussionIncreased rates, faster earlier and slower since the Neoproterozoic/Cambrian transition, may result in estimates that are apparently too recent for deeper nodes.
“Thus, increased rates, faster earlier and slower since the Neoproterozoic/Cambrian transition, may result in estimates that are apparently too recent for deeper nodes.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Premisecitation§ DiscussionMolecular clocks are highly controversial, with dates from various sources often so different that some researchers doubt that molecular dating of evolutionary events is possible.
“Molecular clocks are highly controversial, dates from various sources being often so different that some researchers doubt that molecular dating of evolutionary events is possible (49).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [49] Shields, R. (2004) Trends Genet. 20, 221-222. [DOI] [PubMed] [Google Scholar]
Not checked in the free run.
Classified as probably not a substantial claim. May combine two claims.
Study design and conductown data§ Materials and MethodsOrthology was verified through the analysis of each gene with standard phylogenetic methods, and several proteins, including tubulins, actin, and HSP70, were discarded.
“We verified orthology through the analysis of each gene with standard phylogenetic methods, and we discarded several proteins, including some that were frequently used for studying eukaryotic evolution (tubulins, actin, and HSP70).”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Premisecitation§ DiscussionThe use of seven concatenated proteins and the nonparametric rate smoothing r8s approach indicate a more recent occurrence of the last common bilaterian ancestor, between 556 and 592 Mya, instead of 642-761 here.
“The use of seven concatenated proteins and the nonparametric rate smoothing r8s approach (31) indicate a more recent occurrence of the last common bilaterian ancestor, between 556 and 592 Mya (23) instead of 642–761 here.”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites [31] Sanderson, M. J. (1997) Mol. Biol. Evol. 14, 1218-1231. [Google Scholar] source
Not checked in the free run.
- cites [23] Peterson, K. J., Lyons, J. B., Nowak, K. S., Takacs, C. M., Wargo, M. J. & McPeek, M. A. (2004) Proc. Natl. Acad. Sci. USA 101, 6536-6541. [DOI] [PMC free article] [PubMed] [Google Scholar] source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Study design and conductown data§ Materials and MethodsThe uncertainty of divergence time estimates was characterized by 95% credibility intervals, calculated after sorting the 100,000 MCMC samples, and then reporting the 2,501st and 97,500th values.
“The uncertainty of divergence time estimates was characterized by 95% credibility intervals, calculated after sorting the 100,000 MCMC samples, and then reporting the 2,501st and 97,500th values.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductown data§ Materials and MethodsThe taxon coverage involves some genes lacking for some taxa, leading to approximately 25% of missing character states.
“Our reasonable taxon coverage in this large multiprotein framework involves that some genes are lacking for some taxa, leading to ≈25% of missing character states.”
Quote in the paperNot a substantial claimMay combine two claims.
Interpretationcitation§ ResultsPaleontological uncertainties did not bias the divergence time calculations because they were incorporated in the dating procedure.
“suggesting that paleontological uncertainties did not bias our calculations, because they were incorporated in the dating procedure (31, 33).”
Quote in the paperSubstantial claim0 of 2 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing), S4 (based).
Interpretationnone given§ DiscussionAround 1,000 Mya, the diversification of plants may have been facilitated by the primary endosymbiotic event that led to plastids.
“Around 1,000 Mya, the diversification of plants may have been facilitated by the primary endosymbiotic event that led to plastids.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S4 (based).
Interpretationnone given§ DiscussionThe present study illustrates how geological and biological records of organismal evolution might be partially reconciliated by using molecular relaxed clock datings from large genomic comparisons.
“The present study illustrates how geological and biological records of organismal evolution might be partially reconciliated by using molecular relaxed clock datings from large genomic comparisons.”
Quote in the paperNot a substantial claimMay combine two claims.
Interpretationown data§ DiscussionAccording to protein data, the divergence of the main stem groups of metazoans (Deuterostomia, Ecdysozoa, and Lophotrochozoa) would have occurred in the Late Neoproterozoic, but their diversification would date close to the Precambrian-Cambrian boundary.
“According to protein data, the divergence of the main stem groups of metazoans (Deuterostomia, Ecdysozoa, and Lophotrochozoa) would have occurred in the Late Neoproterozoic, but their diversification would date close to the Precambrian–Cambrian boundary.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S1 (asserted), S3 (load-bearing).
Premisecitation§ DiscussionA major increase in atmospheric oxygen level occurred between 1,000 and 640 Mya.
“Moreover, it has been proposed that a major increase in atmospheric oxygen level occurred between 1,000 and 640 Mya (54).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [54] Canfield, D. E. & Teske, A. (1996) Nature 382, 127-132. [DOI] [PubMed] [Google Scholar] source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
Premisecitation§ DiscussionThe postulated anoxic and sulfidic redox status of oceans between ≈2,000 and 1,000 Mya might have limited the rise of photosynthetic eukaryotes.
“Even if cytoskeletal and ecological prerequisites for eukaryote diversification were already established some 1,500 Mya (3), the postulated anoxic and sulfidic redox status of oceans between ≈2,000 and 1,000 Mya might have limited the rise of photosynthetic eukaryotes (53).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [53] Anbar, A. D. & Knoll, A. H. (2002) Science 297, 1137-1142. [DOI] [PubMed] [Google Scholar] source
Not checked in the free run.
May combine two claims.
Premisecitation§ DiscussionPrevious molecular datings yielded molecular ages always more ancient than paleontological ones, but often to a large extent.
“Previous molecular datings yielded molecular ages always more ancient than paleontological ones, but often to a large extent (12, 15, 20, 46).”
Quote in the paperSubstantial claim0 of 3 sources checked- cites [12] Hedges, S. B. (2002) Nat. Rev. Genet. 3, 838-849. [DOI] [PubMed] [Google Scholar] source
Not checked in the free run.
- cites [15] Gu, X. (1998) J. Mol. Evol. 47, 369-371. [DOI] [PubMed] [Google Scholar] source
Not checked in the free run.
- cites [20] Nei, M., Xu, P. & Glazko, G. (2001) Proc. Natl. Acad. Sci. USA 98, 2497-2502. [DOI] [PMC free article] [PubMed] [Google Scholar] source
Not checked in the free run.
Classified as probably not a substantial claim. May combine two claims.
Premisecitation§ DiscussionYoon et al. suggested a red-green algae split between 1,591 and 1,757 Mya, instead of 825-1,061 or 899-1,191 Mya here, depending on the root location.
“On the basis of a tree derived from five concatenated plastid proteins, calibrated by five intervals under the r8s approach, Yoon et al. (50) suggested a red–green algae split between 1,591 and 1,757 Mya, instead of 825–1,061 or 899–1,191 Mya here, depending on the root location.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [50] Yoon, H. S., Hackett, J. D., Ciniglia, C., Pinto, G. & Bhattacharya, D. (2004) Mol. Biol. Evol. 21, 809-818. [DOI] [PubMed] [Google Scholar]
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
Interpretationcitation§ DiscussionThe major transition toward a more oxygenic environment could possibly have accelerated the diversification of eukaryotic organisms, thanks to aerobic respiration provided by mitochondria.
“In association with the Neoproterozoic appearance of more fully oxic oceans (53), this major transition toward a more oxygenic environment could possibly have accelerated the diversification of the eukaryotic organisms, thanks to the aerobic respiration provided by mitochondria (55).”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites [53] Anbar, A. D. & Knoll, A. H. (2002) Science 297, 1137-1142. [DOI] [PubMed] [Google Scholar] source
Not checked in the free run.
- cites [55] Philippe, H. & Adoutte, A. (1998) in Evolutionary Relationships Among Protozoa, eds. Coombs, G., Vickerman, K., Sleigh, M. & Warren, A. (Kluwer, Dordrecht, The Netherlands), pp. 25-56.
Not checked in the free run.
May combine two claims.
Premisecitation§ DiscussionIn the same paper, calculations modeling rate variation with a gamma distribution yield a confidence interval of 636-678 Mya for the bilaterian diversification, overlapping with ours.
“In the same paper, calculations conducted by modeling such a rate variation with a gamma distribution yield a confidence interval of 636–678 Mya for the bilaterian diversification, i.e., an estimate overlapping with ours.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [23] Peterson, K. J., Lyons, J. B., Nowak, K. S., Takacs, C. M., Wargo, M. J. & McPeek, M. A. (2004) Proc. Natl. Acad. Sci. USA 101, 6536-6541. [DOI] [PMC free article] [PubMed] [Google Scholar] source
Not checked in the free run.
Classified as probably not a substantial claim.
Premisecitation§ DiscussionA fossil of 1,200 Mya has been interpreted as belonging to a specific subgroup of red algae, i.e., bangiophytes.
“whereas a fossil of 1,200 Mya has been interpreted as belonging to a specific subgroup of red algae, i.e., bangiophytes (4).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [4] Butterfield, N. J. (2000) Paleobiology 26, 386-404. [Google Scholar] source
Not checked in the free run.
May combine two claims.
Interpretationcitation§ DiscussionThe major eukaryotic kingdoms originated much more recently than previously thought but did not seem to have been affected by the postulated global glaciations ("snowball Earth" hypothesis) between 750 and 600 Mya.
“The major eukaryotic kingdoms therefore originated much more recently than previously thought (12) but did not seem to have been affected by the postulated global glaciations (“snowball Earth” hypothesis) between 750 and 600 Mya (56).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites [12] Hedges, S. B. (2002) Nat. Rev. Genet. 3, 838-849. [DOI] [PubMed] [Google Scholar] source
Not checked in the free run.
- cites [56] Lubick, N. (2002) Nature 417, 12-13. [DOI] [PubMed] [Google Scholar]
Not checked in the free run.
The paper relies on this without support.
Plastids surrounded by four membranes originated from secondary endosymbiosis, in which a red alga was engulfed and retained by a flagellate protist.
“Plastids surrounded by four membranes originated from secondary endosymbiosis, in which a red alga was engulfed and retained by a flagellate protist.”
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?
Much of metazoan divergence appears closely tied to the Marinoan glaciation, but broad uncertainties in molecular clock studies prevent claims of any direct relationship to this paleoecological event.
“Here, much of metazoan divergence appears closely tied to the Marinoan glaciation, although with the broad uncertainties inherent in molecular clock studies, we can make no claims for any”
From An integrated view of precambrian eumetazoan evolution (2009) · cites this paper as Douzery et al. (2004)
The Results date the protostome–deuterostome split to 642–761 Mya, and the Discussion places divergence of the main metazoan stem groups in the Late Neoproterozoic. The paper acknowledges uncertainty in molecular dating, but our copy does not identify the Marinoan glaciation or say that metazoan divergence was closely tied to it. Its Discussion instead says that the major eukaryotic kingdoms did not seem to have been affected by the postulated global glaciations. (LLM, conf=0.84)
Experimental — accuracy not yet measuredThe suggestion that fungi diverged from animals ca 1000 Myr ago was confirmed by all our analyses that did not assume a particular age for the root node.
“The suggestion that fungi diverged from animals ca 1000 Myr ago (Knoll 1992; Douzery et al. 2004) was confirmed by all our analyses that did not assume a particular age for the root node.”
From The Ediacaran emergence of bilaterians: congruence between the genetic and the geological fossil records (2008) · cites this paper as Douzery et al. 2004
The cnidarian-bilaterian split lies about 30% of the way between the protostome-deuterostome and choanoflagellate-metazoan divergence nodes, suggesting that the eumetazoan ancestor lived between 670 and 820 Mya.
“We see from Figure 2b that the cnidarian-bilaterian split lies ~30% of the way between these two nodes (adopting the midpoint rooting as shown), suggesting that the eumetazoan ancestor lived between 670 and 820 Mya.”
From Sea Anemone Genome Reveals Ancestral Eumetazoan Gene Repertoire and Genomic Organization (2007) · cites this paper as [39]
Cites
Inferring the historical patterns of biological evolution
Pagel, M. (1999) · Nature · doi:10.1038/44766 · Cited by 5,200 · see citing works
Evolutionary divergence and convergence in proteins.
ZUCKERKANDL, E., & PAULING, L. (1965) · Evolving Genes and Proteins · doi:10.1016/b978-1-4832-2734-4.50017-6 · Cited by 3,020 · see citing works
Rambaut, A., & Grass, N. C. (1997) · Computer applications in the biosciences · doi:10.1093/bioinformatics/13.3.235 · Cited by 1,545 · see citing works
The origin and early evolution of plants on land
Kenrick, P., & Crane, P. R. (1997) · Nature · doi:10.1038/37918 · Cited by 1,466 · see citing works
Bryson, V., & Vogel, H. J. (1965) · Science · doi:10.1126/science.147.3653.68 · Cited by 1,343 · see citing works
Estimating the rate of evolution of the rate of molecular evolution
Thorne, J. L., Kishino, H., & Painter, I. S. (1998) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a025892 · Cited by 1,317 · see citing works
Archean Molecular Fossils and the Early Rise of Eukaryotes
Brocks, J. J., Logan, G. A., Buick, R., & Summons, R. E. (1999) · Science · doi:10.1126/science.285.5430.1033 · Cited by 1,275 · see citing works
Proterozoic Ocean Chemistry and Evolution: A Bioinorganic Bridge?
Anbar, A. D., & Knoll, A. H. (2002) · Science · doi:10.1126/science.1069651 · Cited by 1,191 · see citing works
A nonparametric approach to estimating divergence times in the absence of rate constancy.
Sanderson, M. J. (1997) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a025731 · Cited by 1,156 · see citing works
Molecular Evidence for the Early Colonization of Land by Fungi and Plants
Heckman, D. S., Geiser, D. M., Eidell, B. R., Stauffer, R. L., Kardos, N. L., & Hedges, S. B. (2001) · Science · doi:10.1126/science.1061457 · Cited by 1,020 · see citing works
A Molecular Timeline for the Origin of Photosynthetic Eukaryotes
Yoon, H. S., Hackett, J. D., Ciniglia, C., Pinto, G., & Bhattacharya, D. (2004) · Molecular Biology and Evolution · doi:10.1093/molbev/msh075 · Cited by 945 · see citing works
Canfield, D. E., & Teske, A. (1996) · Nature · doi:10.1038/382127a0 · Cited by 869 · see citing works
The origin and evolution of model organisms
Hedges, S. B. (2002) · Nature Reviews Genetics · doi:10.1038/nrg929 · Cited by 806 · see citing works
Baldauf, S. L. (2003) · Science · doi:10.1126/science.1085544 · Cited by 782 · see citing works
Missing Data, Incomplete Taxa, and Phylogenetic Accuracy
Wiens, J. J. (2003) · Systematic Biology · doi:10.1080/10635150390218330 · Cited by 691 · see citing works
The origin and early diversification of land plants: a cladistic study
(1998) · Choice Reviews Online · doi:10.5860/choice.35-3849 · Cited by 647 · see citing works
Performance of a divergence time estimation method under a probabilistic model of rate evolution.
Kishino, H., Thorne, J. L., & Bruno, W. J. (2001) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a003811 · Cited by 633 · see citing works
Bromham, L., & Penny, D. (2003) · Nature Reviews Genetics · doi:10.1038/nrg1020 · Cited by 615 · see citing works
Determining Divergence Times of the Major Kingdoms of Living Organisms with a Protein Clock
Doolittle, R. F., Feng, D.-F., Tsang, S., Cho, G., & Little, E. (1996) · Science · doi:10.1126/science.271.5248.470 · Cited by 581 · see citing works
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 · see citing works
Wang, D. Y.-C., Kumar, S., & Hedges, S. B. (1999) · Proceedings of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rspb.1999.0617 · Cited by 493 · see citing works
Estimating metazoan divergence times with a molecular clock
Peterson, K. J., Lyons, J. B., Nowak, K. S., Takacs, C. M., Wargo, M. J., & McPeek, M. A. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0401670101 · Cited by 461 · see citing works
Life on a young planet: the first three billion years of evolution on Earth
(2003) · Choice Reviews Online · doi:10.5860/choice.41-2190 · Cited by 442 · see citing works
Morphological and ecological complexity in early eukaryotic ecosystems
Javaux, E. J., Knoll, A. H., & Walter, M. R. (2001) · Nature · doi:10.1038/35083562 · Cited by 418 · see citing works
Determining divergence times with a protein clock: Update and reevaluation
Feng, D.-F., Cho, G. S., & Doolittle, R. F. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.24.13028 · Cited by 416 · see citing works
Phylogenomics of Eukaryotes: Impact of Missing Data on Large Alignments
Philippe, H., Snell, E. A., Bapteste, E. P., Lopez, P., Holland, P. W. H., & Casañe, D. (2004) · Molecular Biology and Evolution · doi:10.1093/molbev/msh182 · Cited by 398 · see citing works
Self-citationEvolutionary relationships among protozoa.
Coombs, G. H., Vickerman, K., Sleigh, M. A., & Warren, A. (1998) · Kluwer Academic Publishers eBooks · Cited by 383 · 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
Rooting the Eukaryote Tree by Using a Derived Gene Fusion
Stechmann, A., & Cavalier‐Smith, T. (2002) · Science · doi:10.1126/science.1071196 · Cited by 335 · see citing works
Nei, M., Xu, P., & Glazko, G. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.051611498 · Cited by 329 · see citing works
The Cambrian “explosion”: Slow-fuse or megatonnage?
Morris, S. C. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.9.4426 · Cited by 311 · see citing works
Small Bilaterian Fossils from 40 to 55 Million Years Before the Cambrian
Chen, J.-Y., Bottjer, D. J., Oliveri, P., Dornbos, S. Q., Gao, F., Ruffins, S., Chi, H., Li, C.-W., & Davidson, E. H. (2004) · Science · doi:10.1126/science.1099213 · Cited by 284 · see citing works
Paleobiology of the Neoproterozoic Svanbergfjellet Formation, Spitsbergen
Butterfield, N. J. F., Knoll, A. H., & Swett, K. (1994) · Fossils and strata · doi:10.18261/8200376494-1994-01 · Cited by 282 · see citing works
Early–branching or fast–evolving eukaryotes? An answer based on slowly evolving positions
Philippe, H., Lopez, P., Brinkmann, H., Budin, K., Germot, A., Laurent, J., Moreira, D., Müller, M., & Guyader, H. L. (2000) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2000.1130 · Cited by 247 · see citing works
Self-citationSanderson, M. J., & Doyle, J. A. (2001) · American Journal of Botany · doi:10.2307/3558458 · Cited by 243 · see citing works
Aris-Brosou, S., & Yang, Z. (2002) · Systematic Biology · doi:10.1080/10635150290102375 · Cited by 230 · 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
Snel, ., Bork, P., & Huynen, M. A. (2000) · Trends in Genetics · doi:10.1016/s0168-9525(99)01924-1 · Cited by 183 · see citing works
Taylor, T. N., Hass, H., & Kerp, H. (1999) · Nature · doi:10.1038/21349 · Cited by 180 · 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
Aris-Brosou, S. (2003) · Molecular Biology and Evolution · doi:10.1093/molbev/msg226 · Cited by 164 · see citing works
Time scale of eutherian evolution estimated without assuming a constant rate of molecular evolution.
Hasegawa, M., Thorne, J. L., & Kishino, H. (2003) · Genes & Genetic Systems · doi:10.1266/ggs.78.267 · Cited by 145 · 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
A methodological bias toward overestimation of molecular evolutionary time scales
Rodríguez-Trelles, F., Tarrío, R., & Ayala, F. J. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.122231299 · Cited by 116 · see citing works
Molecular data from 27 proteins do not support a Precambrian origin of land plants
Sanderson, M. J. (2003) · American Journal of Botany · doi:10.3732/ajb.90.6.954 · Cited by 115 · see citing works
Planetary Biology--Paleontological, Geological, and Molecular Histories of Life
Benner, S. A., Caraco, M. D., Thomson, J. M., & Gaucher, E. A. (2002) · Science · doi:10.1126/science.1069863 · Cited by 111 · see citing works
Douzery, E. J. P., Delsuc, F., Stanhope, M. J., & Huchon, D. (2003) · Journal of Molecular Evolution · doi:10.1007/s00239-003-0028-x · Cited by 102 · see citing works
Self-citationEstimating Divergence Times in the Presence of an Overdispersed Molecular Clock
Cutler, D. J. (2000) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a026264 · Cited by 86 · see citing works
Butterfield, N. J. (2001) · Precambrian Research · doi:10.1016/s0301-9268(01)00162-0 · Cited by 85 · see citing works
Early Metazoan Divergence Was About 830 Million Years Ago
Gu, X. (1998) · Journal of Molecular Evolution · doi:10.1007/pl00013150 · Cited by 82 · see citing works
THE 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
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 · see citing works
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 38 · see citing works
Vijg, J., & Calder, R. B. (2004) · Trends in Genetics · doi:10.1016/j.tig.2004.04.007 · Cited by 22 · see citing works
Pushing the envelope on molecular dating
Shields, R. (2004) · Trends in Genetics · doi:10.1016/j.tig.2004.03.011 · Cited by 13 · see citing works
Lubick, N. (2002) · Nature · doi:10.1038/417012a · Cited by 7 · see citing works
Collins, A. G. (2000) · doi:10.1666/0094-8373(2000)026
Flagged first, then by citations
1 of the 58 references couldn’t be matched to a known paper.
Research works printed but not linked: 5
- 10.1666/0094-8373(2000)026 · DOI
- Philippe, H., Snell, E. A., Bapteste, E., Lopez, P., Holland, P. W. H. & Casane, D. (2004) Mol. Biol. Evol. 9, 1740-1752.
- Philippe, H., Lopez, P., Brinkmann, H., Budin, K., Germot, A., Laurent, J., Moreira, D., Müller, M. & Le Guyader, H. (2000) Philos. Trans. R. Soc. London B 267, 1213-1221.
- Grassly, N. C., Adachi, J. & Rambaut, A. (1997) Comput. Appl. Biosci. 13, 559-560.9367131
- Shields, R. (2004) Trends Genet. 20, 221-222.
Cited by
Sorted by citations
Sea Anemone Genome Reveals Ancestral Eumetazoan Gene Repertoire and Genomic Organization
Putnam, N. H., Srivastava, M., Hellsten, U., Dirks, B., Chapman, J., Salamov, A., Terry, A., Shapiro, H., Lindquist, E., Kapitonov, V. V., et al. (2007) · Science · doi:10.1126/science.1139158 · Cited by 1,555 · see citing works
PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating
Lartillot, N., Lepage, T., & Blanquart, S. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp368 · Cited by 1,297 · see citing works
Horizontal gene transfer in eukaryotic evolution
Keeling, P. J., & Palmer, J. D. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2386 · Cited by 1,355 · see citing works
Gene Regulatory Networks and the Evolution of Animal Body Plans
Davidson, E. H., & Erwin, D. H. (2006) · Science · doi:10.1126/science.1113832 · Cited by 1,207 · see citing works
Estimating the timing of early eukaryotic diversification with multigene molecular clocks
Parfrey, L. W., Lahr, D. J. G., Knoll, A. H., & Katz, L. A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1110633108 · Cited by 899 · see citing works
Phylogeny and Molecular Evolution of the Green Algae
Leliaert, F., Smith, D. R., Moreau, H., Herron, M. D., Verbruggen, H., Delwiche, C. F., & Clerck, O. D. (2012) · Critical Reviews in Plant Sciences · doi:10.1080/07352689.2011.615705 · Cited by 900 · see citing works
Comparative Genomics of Trypanosomatid Parasitic Protozoa
El-Sayed, N. M., Myler, P. J., Blandin, G., Berriman, M., Crabtree, J., Aggarwal, G., Caler, E. V., Renauld, H., Worthey, E. A., Hertz‐Fowler, C., et al. (2005) · Science · doi:10.1126/science.1112181 · Cited by 818 · see citing works
Hohmann-Marriott, M. F., & Blankenship, R. E. (2011) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-042110-103811 · Cited by 744 · see citing works
The Ediacara biota: Neoproterozoic origin of animals and their ecosystems
Narbonne, G. M. (2005) · Annual Review of Earth and Planetary Sciences · doi:10.1146/annurev.earth.33.092203.122519 · Cited by 714 · see citing works
Eukaryotic organisms in Proterozoic oceans
Knoll, A. H., Javaux, E. J., Hewitt, D., & Cohen, P. (2006) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2006.1843 · Cited by 701 · see citing works
Phylogenomics: The beginning of incongruence?
JEFFROY, O., BRINKMANN, H., DELSUC, F., & PHILIPPE, H. (2006) · Trends in Genetics · doi:10.1016/j.tig.2006.02.003 · Cited by 698 · see citing works
Self-citationSchnittger, L., Rodríguez, A. E., Florin‐Christensen, M., & Morrison, D. A. (2012) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2012.07.004 · Cited by 601 · see citing works
A general comparison of relaxed molecular clock models
Lepage, T., Bryant, D., Philippe, H., & Lartillot, N. (2007) · Molecular Biology and Evolution · doi:10.1093/molbev/msm193 · Cited by 546 · see citing works
Self-citationKeeling, P. J., Burger, G., Durnford, D. G., Lang, B. F., Lee, R. W., Pearlman, R. E., Roger, A. J., & Gray, M. W. (2005) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2005.09.005 · Cited by 579 · see citing works
Monophyly of Primary Photosynthetic Eukaryotes: Green Plants, Red Algae, and Glaucophytes
Rodríguez‐Ezpeleta, N., Brinkmann, H., Burey, S. C., Roure, B., Burger, G., Löffelhardt, W., Bohnert, H. J., Philippe, H., & Lang, B. F. (2005) · Current Biology · doi:10.1016/j.cub.2005.06.040 · Cited by 559 · see citing works
Self-citationPhilippe, H., Lartillot, N., & Brinkmann, H. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msi111 · Cited by 551 · see citing works
Self-citationRAG1 Core and V(D)J Recombination Signal Sequences Were Derived from Transib Transposons
Kapitonov, V. V., & Jurka, J. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030181 · Cited by 521 · see citing works
The Origin and Establishment of the Plastid in Algae and Plants
Reyes-Prieto, A., Weber, A. P. M., & Bhattacharya, D. (2007) · Annual Review of Genetics · doi:10.1146/annurev.genet.41.110306.130134 · Cited by 453 · see citing works
Freeling, M., & Thomas, B. C. (2006) · Genome Research · doi:10.1101/gr.3681406 · Cited by 451 · see citing works
Molecular Phylogeny and Divergence Times of Deuterostome Animals
Blair, J. E., & Hedges, S. B. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msi225 · Cited by 448 · see citing works
Systematic humanization of yeast genes reveals conserved functions and genetic modularity
Kachroo, A. H., Laurent, J. M., Yellman, C. M., Meyer, A. G., Wilke, C. O., & Marcotte, E. M. (2015) · Science · doi:10.1126/science.aaa0769 · Cited by 423 · see citing works
Domazet‐Lošo, T., Brajković, J., & Tautz, D. (2007) · Trends in Genetics · doi:10.1016/j.tig.2007.08.014 · Cited by 410 · see citing works
Dating divergences in the Fungal Tree of Life: review and new analyses
Taylor, J. W., & Berbee, M. L. (2006) · Mycologia · doi:10.3852/mycologia.98.6.838 · Cited by 424 · see citing works
Genomic adaptation to polyphagy and insecticides in a major East Asian noctuid pest
Cheng, T., Wu, J., Wu, Y., Chilukuri, R. V. E., Huang, L., Yamamoto, K., Feng, L., Li, W., Chen, Z., Guo, H., et al. (2017) · Nature Ecology & Evolution · doi:10.1038/s41559-017-0314-4 · Cited by 412 · see citing works
Paleobiological Perspectives on Early Eukaryotic Evolution
Knoll, A. H. (2014) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a016121 · Cited by 394 · see citing works
Unexpected complexity of the Aquaporin gene family in the moss Physcomitrella patens
Danielson, J. Å., & Johanson, U. (2008) · BMC Plant Biology · doi:10.1186/1471-2229-8-45 · Cited by 409 · see citing works
Animal Evolution and the Molecular Signature of Radiations Compressed in Time
Rokas, A., Krüger, D., & Carroll, S. B. (2005) · Science · doi:10.1126/science.1116759 · Cited by 371 · see citing works
Peterson, K. J., & Butterfield, N. J. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503660102 · Cited by 361 · see citing works
The origin and evolution of mycorrhizal symbioses: from palaeomycology to phylogenomics
Strullu‐Derrien, C., Selosse, M., Kenrick, P., & Martin, F. M. (2018) · New Phytologist · doi:10.1111/nph.15076 · Cited by 355 · see citing works
Identification of the Maturation Factor for Dual Oxidase
Grasberger, H., & Refetoff, S. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.c600095200 · Cited by 333 · see citing works
Couvreur, T. L. P., Franzke, A., Al-Shehbaz, I. A., Bakker, F. T., Koch, М. A., & Mummenhoff, K. (2009) · Molecular Biology and Evolution · doi:10.1093/molbev/msp202 · Cited by 332 · see citing works
Nowack, E. C. M., Melkonian, M., & Glöckner, G. (2008) · Current Biology · doi:10.1016/j.cub.2008.02.051 · Cited by 329 · see citing works
Marcet‐Houben, M., & Gabaldón, T. (2015) · PLoS Biology · doi:10.1371/journal.pbio.1002220 · Cited by 322 · see citing works
Origin of land plants: Do conjugating green algae hold the key?
Wodniok, S., Brinkmann, H., Glöckner, G., Heidel, A. J., Philippe, H., Melkonian, M., & Becker, B. (2011) · BMC Evolutionary Biology · doi:10.1186/1471-2148-11-104 · Cited by 326 · see citing works
Self-citationEarly photosynthetic eukaryotes inhabited low-salinity habitats
Sánchez-Baracaldo, P., Raven, J., Pisani, D., & Knoll, A. (2017) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1620089114 · Cited by 294 · see citing works
Peterson, K. J., Cotton, J. A., Gehling, J. G., & Pisani, D. (2008) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2007.2233 · Cited by 313 · see citing works
Estimating the Phanerozoic history of the Ascomycota lineages: Combining fossil and molecular data
Beimforde, C., Feldberg, K., Nylinder, S., Rikkinen, J. K., Tuovila, H., Dörfelt, H., Gube, M., Jackson, D. J., Joachim Reitner, A., Seyfullah, L. J., et al. (2014) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2014.04.024 · Cited by 311 · see citing works
The Origins of Multicellularity and the Early History of the Genetic Toolkit For Animal Development
Rokas, A. (2008) · Annual Review of Genetics · doi:10.1146/annurev.genet.42.110807.091513 · Cited by 312 · see citing works
The evolution, metabolism and functions of the apicoplast
Lim, L., & McFadden, G. I. (2010) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2009.0273 · Cited by 356 · see citing works
Hauser, F., Cazzamali, G., Williamson, M. P., Blenau, W., & Grimmelikhuijzen, C. J. P. (2006) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2006.07.005 · Cited by 302 · see citing works
Simionato, E., Ledent, V., Richards, G. S., Thomas‐Chollier, M., Kerner, P., Coornaert, D., Degnan, B. M., & Vervoort, M. (2007) · BMC Evolutionary Biology · doi:10.1186/1471-2148-7-33 · Cited by 289 · see citing works
On the Age of Eukaryotes: Evaluating Evidence from Fossils and Molecular Clocks
Eme, L., Sharpe, S. C., Brown, M. W., & Roger, A. J. (2014) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a016139 · Cited by 287 · see citing works
Dating the molecular clock in fungi – how close are we?
Berbee, M. L., & Taylor, J. W. (2010) · Fungal Biology Reviews · doi:10.1016/j.fbr.2010.03.001 · Cited by 285 · see citing works
An Empirical Assessment of Long-Branch Attraction Artefacts in Deep Eukaryotic Phylogenomics
Brinkmann, H., van der Giezen, M., Zhou, Y., de Raucourt, G. P., & Philippe, H. (2005) · Systematic Biology · doi:10.1080/10635150500234609 · Cited by 281 · see citing works
Self-citationBengtson, S., Sallstedt, T., Belivanova, V., & Whitehouse, M. (2017) · PLOS Biology · doi:10.1371/journal.pbio.2000735 · Cited by 284 · see citing works
Cell evolution and Earth history: stasis and revolution
Cavalier‐Smith, T. (2006) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2006.1842 · Cited by 277 · see citing works
The origin of eukaryotes: a reappraisal
Duve, C. D. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2071 · Cited by 273 · see citing works
The sea cucumber genome provides insights into morphological evolution and visceral regeneration
Zhang, X., Sun, L., Yuan, J., Sun, Y., Gao, Y., Zhang, L., Li, S., Dai, H., Hamel, J., Liu, C., et al. (2017) · PLoS Biology · doi:10.1371/journal.pbio.2003790 · Cited by 264 · see citing works
Waters, M. T., & Langdale, J. A. (2009) · The EMBO Journal · doi:10.1038/emboj.2009.264 · Cited by 261 · see citing works
Distinct Dynamics of HISTONE3 Variants between the Two Fertilization Products in Plants
Ingouff, M., Hamamura, Y., Gourgues, M., Higashiyama, T., & Berger, F. (2007) · Current Biology · doi:10.1016/j.cub.2007.05.019 · Cited by 258 · see citing works
The Evolution of Invertebrate Gene Body Methylation
Sarda, S., Zeng, J., Hunt, B. G., & Yi, S. V. (2012) · Molecular Biology and Evolution · doi:10.1093/molbev/mss062 · Cited by 255 · see citing works
The Geological Succession of Primary Producers in the Oceans
KNOLL, A. H., SUMMONS, R. E., WALDBAUER, J. R., & ZUMBERGE, J. E. (2007) · Evolution of Primary Producers in the Sea · doi:10.1016/b978-012370518-1/50009-6 · Cited by 249 · see citing works
Deciphering deuterostome phylogeny: molecular, morphological and palaeontological perspectives
Swalla, B. J., & Smith, A. B. (2008) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2007.2246 · Cited by 252 · see citing works
Hsu, A. P., Johnson, K. D., Falcone, E. L., Sanalkumar, R., Sanchez, L. A., Hickstein, D. D., Cuellar‐Rodríguez, J., Lemieux, J. E., Zerbe, C. S., Bresnick, E. H., et al. (2013) · Blood · doi:10.1182/blood-2012-08-452763 · Cited by 246 · see citing works
Initial Diversification of Living Amphibians Predated the Breakup of Pangaea
Mauro, D. S., Miguel Vences, B., Alcobendas, M., Zardoya, R., & Meyer, A. (2005) · The American Naturalist · doi:10.1086/429523 · Cited by 246 · see citing works
Relaxed molecular clocks for dating historical plant dispersal events
Renner, S. S. (2005) · Trends in Plant Science · doi:10.1016/j.tplants.2005.09.010 · Cited by 244 · see citing works
Modern proteomes contain putative imprints of ancient shifts in trace metal geochemistry
Dupont, C. L., Yang, S., Palenik, B., & Bourne, P. E. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605798103 · Cited by 236 · see citing works
A genome-wide inventory of neurohormone GPCRs in the red flour beetle Tribolium castaneum
Hauser, F., Cazzamali, G., Williamson, M. P., Park, Y., Li, B., Tanaka, Y., Predel, R., Neupert, S., Schachtner, J., Verleyen, P., et al. (2007) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2007.10.003 · Cited by 239 · see citing works
Evolution and pathology in Chagas disease: a review
Teixeira, A. R., Nascimento, R. J., & Sturm, N. R. (2006) · Memórias do Instituto Oswaldo Cruz · doi:10.1590/s0074-02762006000500001 · Cited by 233 · see citing works
Pimanda, J. E., Ottersbach, K., Knezevic, K., Kinston, S., Chan, W. Y. I., Wilson, N. K., Landry, J.-R., Wood, A. D., Kolb-Kokocinski, A., Green, A. R., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0707045104 · Cited by 228 · see citing works
Lücking, R., Huhndorf, S. M., Pfister, D. H., Plata, E. R., & Lumbsch, H. T. (2009) · Mycologia · doi:10.3852/09-016 · Cited by 232 · see citing works
Rutschmann, F. (2005) · Diversity and Distributions · doi:10.1111/j.1366-9516.2006.00210.x · Cited by 230 · see citing works
Molecular dating when rates vary
Welch, J. J., & Bromham, L. D. (2005) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2005.02.007 · Cited by 227 · see citing works
Rooting the tree of life by transition analyses.
Cavalier‐Smith, T. (2006) · Biology Direct · doi:10.1186/1745-6150-1-19 · Cited by 221 · see citing works
Early Diverging Fungi: Diversity and Impact at the Dawn of Terrestrial Life
Berbee, M. L., James, T. Y., & Strullu‐Derrien, C. (2017) · Annual Review of Microbiology · doi:10.1146/annurev-micro-030117-020324 · Cited by 218 · see citing works
Early evolution of the Eukaryota
Butterfield, N. J. F. (2014) · Palaeontology · doi:10.1111/pala.12139 · Cited by 219 · see citing works
The Genomic and Cellular Foundations of Animal Origins
Richter, D. J., & King, N. (2013) · Annual Review of Genetics · doi:10.1146/annurev-genet-111212-133456 · Cited by 196 · see citing works
Zhu, S., Zhu, M., Knoll, A. H., Yin, Z., Zhao, F., Sun, S., Qu, Y., Shi, M., & Liu, H. (2016) · Nature Communications · doi:10.1038/ncomms11500 · Cited by 199 · see citing works
Marshall, C. P., Javaux, E., Knoll, A. H., & Walter, M. R. (2005) · Precambrian Research · doi:10.1016/j.precamres.2005.05.006 · Cited by 197 · see citing works
Szöllősi, G. J., Boussau, B., Abby, S. S., Tannier, É., & Daubin, V. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1202997109 · Cited by 194 · see citing works
Evolutionary mysteries in meiosis
Lenormand, T., Engelstädter, J., Johnston, S. E., Wijnker, T. G., & Haag, C. R. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0001 · Cited by 194 · see citing works
Yang, Y., Yang, E., An, Z., & Liu, X. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0702770104 · Cited by 192 · see citing works
Evolutionary conservation of early mesoderm specification by mechanotransduction in Bilateria
Brunet, T., Bouclet, A., Ahmadi, P., Mitrossilis, D., Driquez, B., Brunet, A., Henry, L., Serman, F., Béalle, G., Ménager, C., et al. (2013) · Nature Communications · doi:10.1038/ncomms3821 · Cited by 192 · see citing works
Michel, G., Tonon, T., Scornet, D., Cock, J. M., & Kloareg, B. (2010) · New Phytologist · doi:10.1111/j.1469-8137.2010.03345.x · Cited by 188 · see citing works
Dating the Diversification of the Major Lineages of Ascomycota (Fungi)
Prieto, M., & Wedin, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0065576 · Cited by 187 · see citing works
Did an ancient chlamydial endosymbiosis facilitate the establishment of primary plastids?
Huang, J.-L., & Gogarten, J. (2007) · Genome Biology · doi:10.1186/gb-2007-8-6-r99 · Cited by 185 · see citing works
Hayden, C. A., & Jorgensen, R. A. (2007) · BMC Biology · doi:10.1186/1741-7007-5-32 · Cited by 182 · see citing works
Galewski, T., Mauffrey, J.-F., Leite, Y. L. R., Patton, J. L., & Douzery, E. (2005) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2004.11.015 · Cited by 181 · see citing works
Self-citationChang, Y., Wang, S., Sekimoto, S., Aerts, A. L., Choi, C., Clum, A., LaButti, K. M., Lindquist, E. A., Ngan, C. Y., Ohm, R. A., et al. (2015) · Genome Biology and Evolution · doi:10.1093/gbe/evv090 · Cited by 178 · see citing works
Cloning and identification of an oxytocin/vasopressin-like receptor and its ligand from insects
Stafflinger, E., Hansen, K. K., Hauser, F., Schneider, M., Cazzamali, G., Williamson, M. P., & Grimmelikhuijzen, C. J. P. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0710897105 · Cited by 180 · see citing works
Roger, A. J., & Hug, L. A. (2006) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2006.1845 · Cited by 180 · see citing works
Hibbett, D. S., & Matheny, P. B. (2009) · BMC Biology · doi:10.1186/1741-7007-7-13 · Cited by 179 · see citing works
Nordström, K. J. V., Almén, M. S., Edstam, M. M., Fredriksson, R., & Schiöth, H. B. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msr061 · Cited by 178 · see citing works
Ancient signals: comparative genomics of green plant CDPKs
Hamel, L., Sheen, J., & Séguin, A. (2013) · Trends in Plant Science · doi:10.1016/j.tplants.2013.10.009 · Cited by 177 · see citing works
Hibbett, D. S., Bauer, R., Binder, M., Giachini, A. J., Hosaka, K., Justo, A., Larsson, E., Larsson, K., Lawrey, J. D., Miettinen, O., et al. (2014) · Springer eBooks · doi:10.1007/978-3-642-55318-9_14 · Cited by 176 · see citing works
A “Holistic” Kinesin Phylogeny Reveals New Kinesin Families and Predicts Protein Functions
Wickstead, B., & Gull, K. (2006) · Molecular Biology of the Cell · doi:10.1091/mbc.e05-11-1090 · Cited by 168 · see citing works
Rice, D. W., & Palmer, J. D. (2006) · BMC Biology · doi:10.1186/1741-7007-4-31 · Cited by 169 · see citing works
Philip, G. K., Creevey, C. J., & McInerney, J. O. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msi102 · Cited by 170 · see citing works
Metabolic evolution and the self-organization of ecosystems
Braakman, R., Follows, M. J., & Chisholm, S. W. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1619573114 · Cited by 164 · see citing works
Network dynamics of eukaryotic LTR retroelements beyond phylogenetic trees
Lloréns, C., Fuentes, A. M.-P., Bernad, L., Botella, H., & Moyá, A. (2009) · Biology Direct · doi:10.1186/1745-6150-4-41 · Cited by 161 · see citing works
A molecular time-scale for eukaryote evolution recalibrated with the continuous microfossil record
Berney, C., & Pawlowski, J. (2006) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2006.3537 · Cited by 212 · see citing works
Song, X., Huang, Z., Duan, W., Ren, J., Liu, T., Li, Y., & Hou, X. (2013) · Molecular Genetics and Genomics · doi:10.1007/s00438-013-0791-3 · Cited by 162 · see citing works
Diversity and evolution of marine phytoplankton
Simon, N., Cras, A.-L., Foulon, E., & Rodolphe Lemée, B. (2008) · Comptes Rendus Biologies · doi:10.1016/j.crvi.2008.09.009 · Cited by 162 · see citing works
Amphioxus and tunicates as evolutionary model systems
Schubert, M., Escrivá, H., Xavier‐Neto, J., & Laudet, V. (2006) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2006.01.009 · Cited by 161 · see citing works
Symbiosis in eukaryotic evolution
López-García, P., Eme, L., & Moreira, D. (2017) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2017.02.031 · Cited by 154 · see citing works
Evolution 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 · see citing works
Ancient collagen reveals evolutionary history of the endemic South American ‘ungulates’
Buckley, M. (2015) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2014.2671 · Cited by 152 · see citing works
A soft-bodied mollusc with radula from the Middle Cambrian Burgess Shale
Caron, J., Scheltema, A. H., Schänder, C., & Rudkin, D. M. (2006) · Nature · doi:10.1038/nature04894 · Cited by 152 · see citing works
Wever, A. D., Leliaert, F., Verleyen, E., Vanormelingen, P., der Gucht, K. V., Hodgson, D. A., Sabbe, K., & Vyverman, W. (2009) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2009.0994 · Cited by 151 · see citing works
- Authors
- Douzery, E. J. P., Snell, E. A., Bapteste, E., Delsuc, F., & Philippe, H.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2004-10-19
- Volume
- 101
- Issue
- 43
- Pages
- 15386-15391
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC524432
- OpenAlex
- W2059383371
- Semantic Scholar
- 6a68deca477b58d5dc602813227badc0c34c5b9f
- Cited by
- 638
- References
- 58
- Citations by year
- 2026: 11 · 2025: 13 · 2024: 14 · 2023: 17 · 2022: 15 · 2021: 34 · 2020: 34 · 2019: 27 · 2018: 24 · 2017: 38 · 2016: 24 · 2015: 27 · 2014: 33 · 2013: 30 · 2012: 33
- FWCI
- 13.85
- 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)
- CentAUR (University of Reading) (acceptedVersion)
- HAL (submittedVersion, other-oa)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protist diversity and phylogeny
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- eukaryotic evolution, divergence time estimation, relaxed molecular clock, protein sequences, fossil calibration, choanoflagellates, protists, animals, fungi, plants
- MeSH terms
- Animals, Biological Evolution, Fossils, Likelihood Functions
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-06.
Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-06.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
