The timing of eukaryotic evolution: Does a relaxed molecular clock reconcile proteins and fossils?

In the paper

“For example, trypanosomes and nematodes evolved two and three times faster than mammals, respectively (data not shown).”

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.”

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

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%).”

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.”

In the paper

“Contrary to all previous studies with such a large sample of genes, a reasonable taxonomic diversity (36 species) was sampled.”

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.”

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.”

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.”

In the paper

“Relaxed clock timings were accurate, although slightly deeper when estimated on constant-rate data.”

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”

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]

In the paper

“Molecular ages are more recent than the fossil record for red algae but more ancient for animals.”

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.”

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]

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

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.”

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.”

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]

In the paper

“extrapolation could conduct to rates increasing on average when moving far back in time.”

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

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]

In the paper

“Posterior divergence times were identical for different MCMC started independently, evidencing convergence of the Bayesian dating procedure.”

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.”

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]

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

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.”

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.”

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]

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).”

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

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.”

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.”

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

• Not checked yetcites [31] Sanderson, M. J. (1997) Mol. Biol. Evol. 14, 1218-1231. [Google Scholar] source
• Not checked yetcites [33] Kishino, H., Thorne, J. L. & Bruno, W. J. (2001) Mol. Biol. Evol. 18, 352-361. [DOI] [PubMed] [Google Scholar] source

In the paper

“Around 1,000 Mya, the diversification of plants may have been facilitated by the primary endosymbiotic event that led to plastids.”

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.”

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.”

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

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

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

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]

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.

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

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

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]