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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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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.
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44 Own result · 37 Not checked yet · 20 Own interpretation · 10 No basis given · 7 Own method
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
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“followed by their diversification in <200 Myr (Fig. 1).”
plain- Asserted: passes — The authors put it forward as true.
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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)”
plain- Asserted: passes — The authors put it forward as true.
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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).”
- Also stated in: § Abstract · plain
“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).”
- Also stated in: § Abstract · plain
“the debated age of the split between protostomes and deuterostomes occurred 642–761 Mya”
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- It may state two separate claims as one. 32
- Probably not a substantial claim. 22
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“For example, trypanosomes and nematodes evolved two and three times faster than mammals, respectively (data not shown).”
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“On average, the relative differences are, respectively, + 1.7% and -2.5% for ages that are over- and underestimated by missing data.”
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“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
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“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%).”
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“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.”
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“Contrary to all previous studies with such a large sample of genes, a reasonable taxonomic diversity (36 species) was sampled.”
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“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.”
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“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.”
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“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.”
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“Relaxed clock timings were accurate, although slightly deeper when estimated on constant-rate data.”
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“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”
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“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]
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In the paper
“Molecular ages are more recent than the fossil record for red algae but more ancient for animals.”
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“Close to the Meso-/Neo-Proterozoic transition, choanoflagellates diverged from their closest animal relatives, marking the dawn of cellular cooperation in animals.”
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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]
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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
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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.
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“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.”
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“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]
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In the paper
“extrapolation could conduct to rates increasing on average when moving far back in time.”
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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.
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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]
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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.
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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.
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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.
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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.
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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.
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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.”
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“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]
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“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.
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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.
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What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“The 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.
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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 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.
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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.
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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
“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.
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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.
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.
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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.
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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.
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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.
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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
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plaincorrelational- Asserted: passes — The authors put it forward as true.
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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.
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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.
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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.
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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.
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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.
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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
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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
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“By the time a second increase in atmospheric oxygen concentration occurred by the late Precambrian, or 1100–550 Ma, the eukaryotic lineage was diversifying (Douzery et al. 2004), hence providing anaerobic niches and allowing persistence of an evolutionary layer that was originally associated with primordial anoxic or…”
BackgroundCarbon Isotope Fractionation by Cyanobacteria under light-limiting conditions
Bubphamanee, K. (2019) · CU Scholar (University of Colorado Boulder) · Cited by 2
Migliore, J. (2011) · theses.fr (ABES) · doi:10.70675/f95026a8ze843z40a6zb003zfb93e3c117cd · Cited by 2
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Minelli, A. (2008) · Cambridge University Press eBooks · doi:10.1017/cbo9780511541582.016 · Cited by 1
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Redecker, D. (2006) · Science · doi:10.1126/science.312.5770.53c · Cited by 1
Vlad, M. O., Oefner, P. J., & Ross, J. (2006) · The Journal of Physical Chemistry B · doi:10.1021/jp0600458 · Cited by 1
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Danchin, É., Gaucher, E. A., & Pontarotti, P. (2007) · doi:10.1093/acprof:oso/9780199299188.003.0013 · Cited by 1
“Deuterostomes and Protostomes separated more than 700 million years ago from the last commonancestor of bilaterian species ( Douzery et al., 2004 ).”
BackgroundBoore, J. L., & Fuerstenberg, S. I. (2009) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199549429.003.0013 · Cited by 1
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Gaubitz, C., Liu, X., Magrino, J., Stone, N. P., Landeck, J. T., Hedglin, M., & Kelch, B. A. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.02.18.953257 · Cited by 1
“The structural similarity observed here using a functional version of the hRFC complex suggests that this state is actually well-populated in solution and is conserved across ~1 billion years of evolution since the S. cerevisiae and H. sapiens lineages diverged (Douzery et al. 2004).”
BackgroundThe animal in the genome: comparative genomics and evolution
Copley, R. R. (2009) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199549429.003.0014 · Cited by 1
Footprints of human migration in the population structure of wild wine yeastPreprint
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島野, 智. (2010) · タクサ : 日本動物分類学会誌 · doi:10.19004/taxa.29.0_31
Bioinformatics of Seven-Transmembrane Receptors in Plant Genomes
Moriyama, E. N., & Opiyo, S. O. (2009) · Signaling and communication in plants · doi:10.1007/978-3-642-03524-1_13
“It indicates that plant 7TMRs have dramatically diverged from the major groups of metazoan 7TMRs since the plant and metazoan lineages separated more than 1 billion years ago ( Douzery et al. 2004; Hedges et al. 2004).”
BackgroundEvolution, diversity, and biogeography in pelagic calcifying protists
Liu, H. (2009) · Rutgers University Community Repository (Rutgers University) · doi:10.7282/t32j6c1h
The sea urchin regulome in development
Ashby, M. (2007) · doi:10.7907/523t-5r49
Evolution of Cellular Pattern Formation during Early Nematode Embryogenesis
Schierenberg, E. (2012) · Springer eBooks · doi:10.1007/978-3-642-30425-5_7
2. Dating Methods and Corresponding Chronometers in Astrobiology
Gargaud, M., Albarède, F., Boiteau, L., Chaussidon, M., Douzery, E., & Montmerle, T. (2006) · Earth Moon and Planets · doi:10.1007/s11038-006-9086-6
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Backgroundsuccess despite increasing susceptibility to generalist herbivores
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Chan, C. X. (2013) · Malaysian Journal of Science · doi:10.22452/mjs.vol32no3.2
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Protein Complex Prediction in the Era of Systems Biology
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Salomaki, E. D. (2017) · Digital Commons - URI (University of Rhode Island) · doi:10.23860/diss-salomaki-eric-2017
“…that contain a relict plastid (apicoplast) obtained through an ancient secondary endosymbiosis (Fast et al. 2001, Zhu et al. 2002), illustrating plastid genome reduction in a lineage that lost its photosynthetic abilities long ago (Douzery et al. 2004, Kuo et al. 2008, Lim et al. 38 2010).”
BackgroundShort Branch Attraction, the Fundamental Bipartition in Cellular Life, and Eukaryogenesis
Dick, & Amanda, A. (2016)
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Patterns of Diversification and Extinction
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Additional file 3 of Codon usage pattern of the ancestor of green plants revealed through Rhodophyta
Yao, H., Li, T., Ma, Z., Wang, X., Xu, L., Zhang, Y., Cai, Y., & Tang, Z.-Z. (2023) · Figshare · doi:10.6084/m9.figshare.24123788
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Additional file 4 of Codon usage pattern of the ancestor of green plants revealed through Rhodophyta
Yao, H., Li, T., Ma, Z., Wang, X., Xu, L., Zhang, Y., Cai, Y., & Tang, Z. (2023) · Figshare · doi:10.6084/m9.figshare.24123791
Additional file 8 of Codon usage pattern of the ancestor of green plants revealed through Rhodophyta
Yao, H., Li, T., Ma, Z., Wang, X., Xu, L., Zhang, Y., Cai, Y., & Tang, Z. (2023) · Figshare · doi:10.6084/m9.figshare.24123806
Zhang, Z., Sun, D., Cheng, K., & Chen, F. (2021) · Figshare · doi:10.6084/m9.figshare.13719484
Additional file 2 of Codon usage pattern of the ancestor of green plants revealed through Rhodophyta
Yao, H., Li, T., Ma, Z., Wang, X., Xu, L., Zhang, Y., Cai, Y., & Tang, Z. (2023) · Figshare · doi:10.6084/m9.figshare.24123785
Additional file 1 of Codon usage pattern of the ancestor of green plants revealed through Rhodophyta
Yao, H., Li, T., Ma, Z., Wang, X., Xu, L., Zhang, Y., Cai, Y., & Tang, Z. (2023) · Figshare · doi:10.6084/m9.figshare.24123782
Wang, J., Chen, K., Yang, J., Zhang, S., Li, Y., Liu, G., Luo, J., Yin, H., Wang, G., & Guan, G. (2022) · Figshare · doi:10.6084/m9.figshare.20235739
Wang, J., Chen, K., Yang, J., Zhang, S., Li, Y., Liu, G., Luo, J., Yin, H., Wang, G., & Guan, G. (2022) · Figshare · doi:10.6084/m9.figshare.20235742
Yao, H., Li, T., Ma, Z., Wang, X., Xu, L., Zhang, Y., Cai, Y., & Tang, Z. (2023) · Figshare · doi:10.6084/m9.figshare.24123812
Zhang, Z., Sun, D., Cheng, K., & Chen, F. (2021) · Figshare · doi:10.6084/m9.figshare.13719481
Additional file 6 of Codon usage pattern of the ancestor of green plants revealed through Rhodophyta
Yao, H., Li, T., Ma, Z., Wang, X., Xu, L., Zhang, Y., Cai, Y., & Tang, Z.-Z. (2023) · Figshare · doi:10.6084/m9.figshare.24123800
Wang, J., Chen, K., Yang, J., Zhang, S., Li, Y., Liu, G., Luo, J., Yin, H., Wang, G., & Guan, G. (2022) · Figshare · doi:10.6084/m9.figshare.20235736
Yao, H., Li, T., Ma, Z., Wang, X., Xu, L., Zhang, Y., Cai, Y., & Tang, Z. (2023) · Figshare · doi:10.6084/m9.figshare.24123815
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
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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.
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