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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.
Overview
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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.
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44 Own result · 37 Not checked yet · 20 Own interpretation · 10 No basis given · 7 Own method
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“followed by their diversification in <200 Myr (Fig. 1).”
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“The divergence between animals and fungi was, for example, estimated 872–1,127 Mya (mean 983 Mya)”
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“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)”
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“Thus, the rate of amino acid replacements extensively changed among the eukaryote lineages here analyzed.”
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“red algae branched off 825–1,061 Mya (mean 928)”
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“A likelihood ratio test significantly rejected the hypothesis of a clocklike behavior of our data (P < 0.0001).”
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“The divergence between choanoflagellates and animals was estimated during the Late Proterozoic, between 761 and 957 Mya (mean 849).”
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“animals diverged from choanoflagellates 761–957 Mya”
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“Plantae originated 892–1,162 Mya (mean 1,010)”
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“stem land plants separated from green algae 662–812 Mya (mean 729)”
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“Interestingly, the divergence time between protostomes and deuterostomes (Fig. 1) was 642–761 Mya (mean 695).”
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“the debated age of the split between protostomes and deuterostomes occurred 642–761 Mya”
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“When we constrained a perfect molecular clock under the Bayesian approach, this divergence was estimated at 439–468 Mya (mean 454).”
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“the minimum and maximum estimates may dramatically vary depending upon the choice of a given combination of fossil references (Table 2).”
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“Whereas divergence times averaged over all possibilities of using a given number of simultaneous calibrations seems not to vary much with those numbers”
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“Posterior divergence times thus appeared only slightly sensitive to huge changes in prior specification of root age.”
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“The kinetoplastid rooting actually involved deeper divergences among Plantae (899–1,191 Mya).”
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“Accordingly, we have shown that the use of simultaneous calibrations reduces the uncertainty on age estimates (Table 2).”
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“However, a reduction of the uncertainty on divergence times was clearly associated to the increase of the number of simultaneous calibrations.”
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“These two fungi appear to be fast evolving (data not shown)”
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“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.”
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“Within fungi, the divergence between ascomycetes and basidiomycetes is estimated ≈629–837 Mya (mean 727)”
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“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).”
What the sources say
- Not checked yetcites [32] Thorne, J. L., Kishino, H. & Painter, I. S. (1998) Mol. Biol. Evol. 15, 1647-1657. [DOI] [PubMed] [Google Scholar] source
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“The divergence times appeared to be robust with respect to prior assumptions and paleontological calibrations.”
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“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)”
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“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).”
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“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).”
What the sources say
- Not checked yetcites [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
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“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).”
What the sources say
- Not checked yetcites [44] Baldauf, S. L. (2003) Science 300, 1703-1706. [DOI] [PubMed] [Google Scholar] source
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“Second, our relaxed molecular clock datings (Fig. 1) appear to be robust to the specification of prior distributions on model parameters.”
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“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).”
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“For the root age, these values are indeed twice less than the actual SD measured by the Bayesian approach.”
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“e.g., we obtained 627–738 Mya for bilaterians”
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“Importantly, our datings were robust against the random exclusion of one or two calibration points.”
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“In particular, our 129 proteins did not record the Late Precambrian episodic burst of evolutionary rates detected on 22 mitochondrial and nuclear genes (22).”
What the sources say
- Not checked yetcites [22] Aris-Brosou, S. & Yang, Z. (2003) Mol. Biol. Evol. 20, 1947-1954. [DOI] [PubMed] [Google Scholar] source
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“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.”
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“This corresponds to variations of approximately +17 Myr to -25 Myr for a 1,000-Myr-old node.”
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“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).”
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“Nevertheless, our dating estimates are robust upon missing data (Fig. 3, which is published as supporting information on the PNAS web site).”
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“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”
What the sources say
- Not checked yetcites [12] Hedges, S. B. (2002) Nat. Rev. Genet. 3, 838-849. [DOI] [PubMed] [Google Scholar] source
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“Divergence times in opisthokonts, especially among animals, were not sensitive to this modification (e.g., we obtained 627–738 Mya for bilaterians).”
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“Our reanalysis of this data set under the divtime relaxed molecular clock approach suggests a major incompatibility between “green” and “red” calibrations.”
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“For bilaterians, the discrepancy between our molecular estimates (642–761 Mya) and the fossil record (7) is reduced to a minimum of 40 Myr.”
What the sources say
- Not checked yetcites [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
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“This is incompatible with the respective 1,174- to 1,222- and 594- to 603-Mya constraints used in reference (50).”
What the sources say
- Not checked yetcites [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
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“Interestingly, our molecular dating (Fig. 1) does not appear to be biased in such a systematic way.”
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“We dated the divergence between green plants and red algae between 825 and 1,061 Mya (Fig. 1)”
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“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).”
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“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.”
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“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.”
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“reducing to ≈40 Myr the minimum gap between the protein relaxed clock timing and the first indisputable bilaterian fossil (7).”
What the sources say
- Not checked yetcites [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
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In the paper
“Molecular estimates of divergence times are, however, controversial and are generally much more ancient than suggested by the fossil record.”
What the sources say
- Not checked yetcites [12] Hedges, S. B. (2002) Nat. Rev. Genet. 3, 838-849. [DOI] [PubMed] [Google Scholar] source
plaincorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“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).”
hedged- Asserted: passes — The authors put it forward as true.
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- 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.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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).”
hedgeddirect- Asserted: passes — The authors put it forward as true.
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In the paper
“The major transition during animal evolution from unicellular to multicellular state might have thus occurred at least 200 Myr before the Cambrian explosion.”
hedged- Asserted: passes — The authors put it forward as true.
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In the paper
“yet bilaterian diversification appears to be ≈100 million years more ancient than the Cambrian boundary.”
hedged- Asserted: passes — The authors put it forward as true.
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In the paper
“The simulations therefore indicate that the autocorrelation model of substitution-rate evolution does not underestimate ages on clocklike data”
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In the paper
“likely because such an alternative root location involves a pectinate tree shape.”
hedgedconditional- Asserted: passes — The authors put it forward as true.
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A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“whereas a linear extrapolation on rate-variable data markedly overestimates divergence times (Table 1).”
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“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).”
What the sources say
- Not checked yetcites [44] Baldauf, S. L. (2003) Science 300, 1703-1706. [DOI] [PubMed] [Google Scholar] source
plain- Asserted: passes — The authors put it forward as true.
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In the paper
“Two elements suggest that our analyses have not been affected by such a trend.”
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In the paper
“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).”
What the sources say
- Not checked yetcites [47] Wiens, J. J. (2003) Syst. Biol. 52, 528-538. [DOI] [PubMed] [Google Scholar] source
hedgeddirect- Asserted: passes — The authors put it forward as true.
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A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The relaxed clock method is therefore efficient, even when the alignment contains partial sequences.”
plain- Asserted: passes — The authors put it forward as true.
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A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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.”
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None of the sources cited for this claim have been checked yet.
In the paper
“Recently, two relaxed clock dating studies, among metazoans (23) and photosynthetic eukaryotes (50), yielded results that are at first sight incongruent with our estimates.”
What the sources say
- Not checked yetcites [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 yetcites [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
plain- Asserted: passes — The authors put it forward as true.
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A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“and such high rates are probably not accommodated by global clock based methods.”
hedged- Asserted: passes — The authors put it forward as true.
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In the paper
“Molecular clock approaches are also sensitive to the choice of calibrations (48).”
What the sources say
- Not checked yetcites [48] Douzery, E. J. P., Delsuc, F., Stanhope, M. J. & Huchon, D. (2003) J. Mol. Evol. 57, S201-S213. [DOI] [PubMed] [Google Scholar] source
plaincorrelational- Asserted: passes — The authors put it forward as true.
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A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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.”
hedgeddirect- Asserted: passes — The authors put it forward as true.
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The paper states this without a source or data behind it here, so there is nothing to check it against. The quote shows it is in the paper.
In the paper
“Estimating a time scale by the mean of age extrapolation beyond animal, fungi, and plant calibrations may possibly lead to biased estimates.”
hedgedconditional- Asserted: passes — The authors put it forward as true.
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What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“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.”
plain- Asserted: passes — The authors put it forward as true.
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The paper states this without a source or data behind it here, so there is nothing to check it against. The quote shows it is in the paper.
In the paper
“Whereas interpolation of date estimates is certainly less biased because evolutionary rates are bounded by zero”
boosteddirect- Asserted: passes — The authors put it forward as true.
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A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Presently, because the shortest concatenated sequence includes 7,500 amino acids, our complete alignment retains a strong phylogenetic and dating signal.”
boosteddirect- Asserted: passes — The authors put it forward as true.
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In the paper
“Importantly, these estimates were obtained without taking into account among-site rate variation.”
What the sources say
- Not checked yetcites [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
plain- Asserted: passes — The authors put it forward as true.
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In the paper
“Illustrating the latter case, the age of the Bangiomorpha assemblage is in fact bounded between 1,267 and 723 Mya (52).”
What the sources say
- Not checked yetcites [52] Butterfield, N. J. (2001) Precamb. Res. 111, 235-256. [Google Scholar] source
plain- Asserted: passes — The authors put it forward as true.
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A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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.”
hedgeddirect- Asserted: passes — The authors put it forward as true.
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In the paper
“Actually, single fossils may also bear their load of uncertainty in taxonomy identification and geological ages (11).”
What the sources say
- Not checked yetcites [11] Bromham, L. & Penny, D. (2003) Nat. Rev. Genet. 4, 216-224. [DOI] [PubMed] [Google Scholar] source
hedged- Asserted: passes — The authors put it forward as true.
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In the paper
“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).”
What the sources say
- Not checked yetcites [51] Bromham, L., Phillips, M. J. & Penny, D. (1999) Trends Ecol. Evol. 14, 113-118. [DOI] [PubMed] [Google Scholar] source
plaindirect- Asserted: passes — The authors put it forward as true.
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- It may state two separate claims as one. 32
- Probably not a substantial claim. 22
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“For example, trypanosomes and nematodes evolved two and three times faster than mammals, respectively (data not shown).”
plaincorrelational- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“On average, the relative differences are, respectively, + 1.7% and -2.5% for ages that are over- and underestimated by missing data.”
plaincorrelational- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
In the paper
“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).”
What the sources say
- Not checked yetcites [22] Aris-Brosou, S. & Yang, Z. (2003) Mol. Biol. Evol. 20, 1947-1954. [DOI] [PubMed] [Google Scholar] source
plaindirect- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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%).”
plaindirect- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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.”
plain- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
The paper states this without a source or data behind it here, so there is nothing to check it against. The quote shows it is in the paper.
In the paper
“Contrary to all previous studies with such a large sample of genes, a reasonable taxonomic diversity (36 species) was sampled.”
plain- Asserted: passes — The authors put it forward as true.
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- Load-bearing: fails — The paper’s conclusions may not depend on it.
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Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The 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.”
plaincorrelational- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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.”
hedgeddirect- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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.”
plain- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Relaxed clock timings were accurate, although slightly deeper when estimated on constant-rate data.”
plaincorrelational- Asserted: passes — The authors put it forward as true.
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- Load-bearing: passes — The paper’s conclusions depend on it.
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It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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”
hedged- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
In the paper
“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.”
What the sources say
- Not checked yetcites [50] Yoon, H. S., Hackett, J. D., Ciniglia, C., Pinto, G. & Bhattacharya, D. (2004) Mol. Biol. Evol. 21, 809-818. [DOI] [PubMed] [Google Scholar]
hedgeddirect- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Molecular ages are more recent than the fossil record for red algae but more ancient for animals.”
plaincorrelational- Asserted: passes — The authors put it forward as true.
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- Load-bearing: passes — The paper’s conclusions depend on it.
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It may state two separate claims as one.
The paper states this without a source or data behind it here, so there is nothing to check it against. The quote shows it is in the paper.
In the paper
“Close to the Meso-/Neo-Proterozoic transition, choanoflagellates diverged from their closest animal relatives, marking the dawn of cellular cooperation in animals.”
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
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Probably not a substantial claim. The paper’s conclusions may not depend on it. The paper may give no reason why it holds. It may state two separate claims as one.
In the paper
“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).”
What the sources say
- Not checked yetcites [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]
hedgedcorrelational- Asserted: passes — The authors put it forward as true.
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- Load-bearing: unclear — It is unclear whether the paper’s conclusions depend on it.
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It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“This value is much lower than most of the previously published ones (12, 17, 46) but is close to recent estimates (22, 23)”
What the sources say
- Not checked yetcites [12] Hedges, S. B. (2002) Nat. Rev. Genet. 3, 838-849. [DOI] [PubMed] [Google Scholar] source
- Not checked yetcites [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 yetcites [46] Wray, G. A., Levinton, J. S. & Shapiro, L. H. (1996) Science 274, 568-573. [Google Scholar] source
plain- Asserted: passes — The authors put it forward as true.
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- Load-bearing: unclear — It is unclear whether the paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The limited number of genes and species explored and pervasive variations in evolutionary rates are the most likely sources of such discrepancies.”
hedgeddirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“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.”
plaindirect- Asserted: passes — The authors put it forward as true.
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- Load-bearing: passes — The paper’s conclusions depend on it.
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Probably not a substantial claim.
In the paper
“Changes in reference topology may potentially affect molecular dating (39).”
What the sources say
- Not checked yetcites [39] Sanderson, M. J. & Doyle, J. A. (2001) Am. J. Bot. 88, 1499-1516. [PubMed] [Google Scholar]
hedgedconditional- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
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Probably not a substantial claim.
The paper states this without a source or data behind it here, so there is nothing to check it against. The quote shows it is in the paper.
In the paper
“extrapolation could conduct to rates increasing on average when moving far back in time.”
hedgedconditional- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
None of the sources cited for this claim have been checked yet.
In the paper
“A similar result was obtained for animals under various models of clock relaxation (22, 28) and for mitochondrial genomes of mammals (29).”
What the sources say
- Not checked yetcites [22] Aris-Brosou, S. & Yang, Z. (2003) Mol. Biol. Evol. 20, 1947-1954. [DOI] [PubMed] [Google Scholar] source
- Not checked yetcites [28] Aris-Brosou, S. & Yang, Z. (2002) Syst. Biol. 51, 703-714. [DOI] [PubMed] [Google Scholar] source
- Not checked yetcites [29] Hasegawa, M., Thorne, J. L. & Kishino, H. (2003) Genes Genet. Syst. 78, 267-283. [DOI] [PubMed] [Google Scholar] source
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: unclear — It is unclear whether the paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“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).”
What the sources say
- Not checked yetcites [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 yetcites [37] Stechmann, A. & Cavalier-Smith, T. (2002) Science 297, 89-91. [DOI] [PubMed] [Google Scholar]
hedgeddirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: unclear — It is unclear whether the paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“Posterior divergence times were identical for different MCMC started independently, evidencing convergence of the Bayesian dating procedure.”
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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.”
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
In the paper
“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).”
What the sources say
- Not checked yetcites [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]
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
In the paper
“Divergence times were estimated under a Bayesian relaxed molecular clock (33), constrained by six independent fossil references.”
What the sources say
- Not checked yetcites [33] Kishino, H., Thorne, J. L. & Bruno, W. J. (2001) Mol. Biol. Evol. 18, 352-361. [DOI] [PubMed] [Google Scholar] source
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“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.”
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Thus, increased rates, faster earlier and slower since the Neoproterozoic/Cambrian transition, may result in estimates that are apparently too recent for deeper nodes.”
hedgedconditional- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. It may state two separate claims as one.
In the paper
“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).”
What the sources say
- Not checked yetcites [49] Shields, R. (2004) Trends Genet. 20, 221-222. [DOI] [PubMed] [Google Scholar]
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“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).”
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“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.”
What the sources say
- Not checked yetcites [31] Sanderson, M. J. (1997) Mol. Biol. Evol. 14, 1218-1231. [Google Scholar] source
- Not checked yetcites [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
hedgeddirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“The 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.”
plainn = 100,000- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“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.”
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
None of the sources cited for this claim have been checked yet.
In the paper
“suggesting that paleontological uncertainties did not bias our calculations, because they were incorporated in the dating procedure (31, 33).”
What the sources say
hedged- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Around 1,000 Mya, the diversification of plants may have been facilitated by the primary endosymbiotic event that led to plastids.”
hedgedconditional- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: fails — The paper may give no reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it. The paper may give no reason why it holds.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The 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.”
hedgedconditional- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: fails — The paper may give no reason why it holds.
Probably not a substantial claim. The paper may give no reason why it holds.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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.”
hedged- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
In the paper
“Moreover, it has been proposed that a major increase in atmospheric oxygen level occurred between 1,000 and 640 Mya (54).”
What the sources say
- Not checked yetcites [54] Canfield, D. E. & Teske, A. (1996) Nature 382, 127-132. [DOI] [PubMed] [Google Scholar] source
hedged- Asserted: fails — The authors may not put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The authors may not put it forward as true. The paper’s conclusions may not depend on it.
In the paper
“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).”
What the sources say
- Not checked yetcites [53] Anbar, A. D. & Knoll, A. H. (2002) Science 297, 1137-1142. [DOI] [PubMed] [Google Scholar] source
hedgedconditional- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
None of the sources cited for this claim have been checked yet.
In the paper
“Previous molecular datings yielded molecular ages always more ancient than paleontological ones, but often to a large extent (12, 15, 20, 46).”
What the sources say
- Not checked yetcites [12] Hedges, S. B. (2002) Nat. Rev. Genet. 3, 838-849. [DOI] [PubMed] [Google Scholar] source
- Not checked yetcites [15] Gu, X. (1998) J. Mol. Evol. 47, 369-371. [DOI] [PubMed] [Google Scholar] source
- Not checked yetcites [20] Nei, M., Xu, P. & Glazko, G. (2001) Proc. Natl. Acad. Sci. USA 98, 2497-2502. [DOI] [PMC free article] [PubMed] [Google Scholar] source
plaincorrelational- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
In the paper
“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.”
What the sources say
- Not checked yetcites [50] Yoon, H. S., Hackett, J. D., Ciniglia, C., Pinto, G. & Bhattacharya, D. (2004) Mol. Biol. Evol. 21, 809-818. [DOI] [PubMed] [Google Scholar]
hedged- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“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).”
What the sources say
- Not checked yetcites [53] Anbar, A. D. & Knoll, A. H. (2002) Science 297, 1137-1142. [DOI] [PubMed] [Google Scholar] source
- Not checked yetcites [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.
hedgedconditional- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
In the paper
“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.”
What the sources say
- Not checked yetcites [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
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
In the paper
“whereas a fossil of 1,200 Mya has been interpreted as belonging to a specific subgroup of red algae, i.e., bangiophytes (4).”
What the sources say
- Not checked yetcites [4] Butterfield, N. J. (2000) Paleobiology 26, 386-404. [Google Scholar] source
hedgedSingle case- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim.
None of the sources cited for this claim have been checked yet.
In the paper
“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).”
What the sources say
- Not checked yetcites [12] Hedges, S. B. (2002) Nat. Rev. Genet. 3, 838-849. [DOI] [PubMed] [Google Scholar] source
- Not checked yetcites [56] Lubick, N. (2002) Nature 417, 12-13. [DOI] [PubMed] [Google Scholar]
hedged- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
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?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“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)
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“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
In the citing paper
“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]
Citations
Cites
Inferring the historical patterns of biological evolution
Pagel, M. (1999) · Nature · doi:10.1038/44766 · Cited by 5,200
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
Rambaut, A., & Grass, N. C. (1997) · Computer applications in the biosciences · doi:10.1093/bioinformatics/13.3.235 · Cited by 1,545
The origin and early evolution of plants on land
Kenrick, P., & Crane, P. R. (1997) · Nature · doi:10.1038/37918 · Cited by 1,466
Bryson, V., & Vogel, H. J. (1965) · Science · doi:10.1126/science.147.3653.68 · Cited by 1,343
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
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
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
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
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
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
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
Horizontal gene transfer in eukaryotic evolution
Keeling, P. J., & Palmer, J. D. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2386 · Cited by 1,355
“Only 20 of these genes were common to all three trypanosomes, whereas 6 genes were found in only two of the three, and 21 were unique to a single genome, indicating considerable variability in gain and/or loss of bacterial genes within the estimated 250 million year divergenc”
BackgroundGene 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
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
Metadata
- 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 › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › 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.
A language model drew the claims from the paper on 2026-10-06, under version 3 of the claim definition (model deepseek-v4.1-flash, prompt extract-v3).
A second model labelled each claim on 2026-10-06 (model jev-1.13-20260917, definition revision gold-guideline-v0.2).
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