Cited by 657Protist diversity and phylogenyEvolution and Paleontology StudiesGenomics and Phylogenetic Studies

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

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Douzery, Emmanuel J. P., Snell, Elizabeth A., Bapteste, Eric, Delsuc, Frédéric, Philippe, Hervé·2004·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.0403984101PMC PMC524432

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Abstract

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.

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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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Crossref · 10.1073/pnas.0403984101

Cites

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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
“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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In the paper
“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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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
“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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Show all 73 claims

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Probably not a substantial claim. 22

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
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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]
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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
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In the paper
“Changes in reference topology may potentially affect molecular dating (39).”
What the sources say
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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
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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]
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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]
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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
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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]
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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
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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
- 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
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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
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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
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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
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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]
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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
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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
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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
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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
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45 of 45

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.”

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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.

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Background
Evidence of mRNA-Mediated Intron Loss in the Human-Pathogenic Fungus Cryptococcus neoformans
Stajich, J., & Dietrich, F. S. (2006) · Eukaryotic Cell · doi:10.1128/ec.5.5.789-793.2006 · Cited by 53
“To arrive at the current number of approximately 33,000 introns, the common ancestor of the fungi (estimated to have emerged 800 Mya [1, 8]) would have had approximately 40,000 introns in 5,300 genes.”
Background
Consistent and contrasting properties of lineage-specific genes in the apicomplexan parasites and -2
Kuo, C., & Kissinger, J. C. (2011) · Figshare · doi:10.6084/m9.figshare.40550 · Cited by 56
A Parvancorina -like arthropod from the Cambrian of South China
Lin, J.-P., Gon, S. M., Gehling, J. G., Babcock, L. E., Zhao, Y.-L., Zhang, X.-L., Hu, S.-X., Yuan, J.-L., Yu, M.-Y., & Peng, J. (2006) · Historical Biology · doi:10.1080/08912960500508689 · Cited by 53
“2001; Waloszek 2003) and/or living species (Manton 1977; Gupta 1979; Manton and Anderson 1979; Wray et al. 1996; Ayala 1997; Feng et al. 1997; Shubin et al. 1997; Bromham et al. 1998; Douzery et al. 2004; Peterson and Butterfield 2005) suggest that the origin of major arthropod groups occurred long before the Cambrian…”
Background
Hdac3 regulates lymphovenous and lymphatic valve formation
Janardhan, H. P., Milstone, Z. J., Shin, M., Lawson, N. D., Keaney, J. F., & Trivedi, C. M. (2017) · Journal of Clinical Investigation · doi:10.1172/jci92852 · Cited by 52
Global Neuropeptide Annotations From the Genomes and Transcriptomes of Cubozoa, Scyphozoa, Staurozoa (Cnidaria: Medusozoa), and Octocorallia (Cnidaria: Anthozoa)
Koch, T. L., & Grimmelikhuijzen, C. J. P. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00831 · Cited by 53
“During animal evolution, ancestral Cnidaria, Placozoa, Ctenophora, and Porifera diverged from the Bilateria more than 600 million years ago (1).”
Background
Bayesian relaxed clock estimation of divergence times in foraminifera
Groussin, M., Pawlowski, J. W., & Yang, Z. (2011) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2011.06.008 · Cited by 51
“Those results indicate that the Cryogenian oceanic fauna was composed of monothalamous foraminiferal species and that Foraminifera are important to the Neo-Proterozoic protistan communities and the difficulties in finding fossil traces of foraminifers during this period could be due to non-preservation of these specim…”
Influential
An ancient transcriptional regulatory linkage
Rebeiz, M., Stone, T., & Posakony, J. W. (2005) · Developmental Biology · doi:10.1016/j.ydbio.2005.03.004 · Cited by 52
“We suggest that the extensive association of protostome, deuterostome, and cnidarian proneural genes with putative high-affinity bHLH repressor binding sites indicates a common regulatory linkage that has been preserved from a deep metazoan ancestor that lived at least 600–700 Mya (Douzery et al., 2004; Peterson et al…”
Background
Molecular clocks and the early evolution of metazoan nervous systems
Wray, G. A. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2015.0046 · Cited by 51
Early embryogenesis of potential bilaterian animals with polar lobe formation from the Ediacaran Weng’an Biota, South China
Yin, Z., Zhu, M., Tafforeau, P., Chen, J., Liu, P., & Li, G. (2011) · Precambrian Research · doi:10.1016/j.precamres.2011.08.011 · Cited by 51
Characterization and fine mapping of thermo-sensitive chlorophyll deficit mutant1 in rice (Oryza sativa L.)
Liu, J., Wang, J., Yao, X., Zhang, Y., Li, J., Wang, X., Xu, Z., & Chen, W. (2015) · Ikushugaku zasshi · doi:10.1270/jsbbs.65.161 · Cited by 51
Retrograde signaling between plastid and nucleus: A review
Singh, R., Singh, S., Parihar, P., Singh, V. P., & Prasad, S. M. (2015) · Journal of Plant Physiology · doi:10.1016/j.jplph.2015.04.001 · Cited by 51
The zinc cluster transcription factor Ahr1p directs Mcm1p regulation of Candida albicans adhesion
Askew, C., Sellam, A., Epp, E., Mallick, J., Hogues, H., Mullick, A., Nantel, A., & Whiteway, M. S. (2010) · Molecular Microbiology · doi:10.1111/j.1365-2958.2010.07504.x · Cited by 55
“…albicans and the model yeast Saccharomyces cerevisiae diverged from a common ancestor approximately 235–841 million years ago (Heckman et al., 2001; Douzery et al., 2004), and unlike C. albicans, S. cerevisiae does not naturally form biofilms or have orthologues of the ALS gene family, HWP1 or…”
Background
Characterization of the mammalian DEAD-box protein DDX5 reveals functional conservation with S. cerevisiae ortholog Dbp2 in transcriptional control and glucose metabolism
Xing, Z., Wang, S., & Tran, E. J. (2017) · RNA · doi:10.1261/rna.060335.116 · Cited by 47
“This results in very different biochemical activities between these two DEAD-box helicases (Dutta et al. 2011).”
Background
Yeast Genomics and Its Applications in Biotechnological Processes: What Is Our Present and Near Future?
Tullio, V. C. (2022) · Journal of Fungi · doi:10.3390/jof8070752 · Cited by 51
“down to the species level and reflects intense genomic changes, which contrast with yeasts’ long-term conservation of biological properties [23].”
Background
Walking like an ant: a quantitative and experimental approach to understanding locomotor mimicry in the jumping spider Myrmarachne formicaria
Shamble, P. S., Hoy, R., Cohen, I., & Beatus, T. (2017) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2017.0308 · Cited by 47
Plastid Endosymbiosis: Sources and Timing of the Major Events
Hackett, J. D., Yoon, H. S., Butterfield, N. J. F., Sanderson, M. J., & Bhattacharya, D. (2007) · Elsevier eBooks · doi:10.1016/b978-012370518-1/50008-4 · Cited by 50
An integrated view of precambrian eumetazoan evolution
Davidson, E. H., & Erwin, D. H. (2009) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2009.74.042 · Cited by 48
“Because the fossil record only provides minimal estimates of the appearances of distinctive and fossilizable morphologies, molecular clock estimates in principle offer critical additional information on the timing of the diversification of eumetazoan lineages (Aris-Brosou and Yang 2003; Douzery et al. 2004; Peterson a…”
Background
Rhynie chert: a window into a lost world of complex plant–fungus interactions
Berbee, M. L., & Taylor, J. W. (2007) · New Phytologist · doi:10.1111/j.1469-8137.2007.02080.x · Cited by 49
Causes and consequences of low atmospheric pCO2 in the Late Mesoproterozoic
Sheldon, N. D. (2013) · Chemical Geology · doi:10.1016/j.chemgeo.2013.09.006 · Cited by 48
Transcriptionally active TFIIH of the early-diverged eukaryote Trypanosoma brucei harbors two novel core subunits but not a cyclin-activating kinase complex
Lee, J. H., Jung, H. S., & Günzl, A. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp236 · Cited by 60
The neuropeptidomics of Ixodes scapularis synganglion
Neupert, S., Russell, W. K., Predel, R., Russell, D. H., Strey, O. F., Teel, P. D., & Nachman, R. J. (2009) · Journal of Proteomics · doi:10.1016/j.jprot.2009.06.007 · Cited by 49
An ensemble of specifically targeted proteins stabilizes cortical microtubules in the human parasiteToxoplasma gondii
Liu, J., He, Y., Benmerzouga, I., Sullivan, W. J., Morrissette, N. S., Murray, J. M., & Hu, K. (2015) · Molecular Biology of the Cell · doi:10.1091/mbc.e15-11-0754 · Cited by 53
“…coating proteins TLAP2 is conserved among several distinct groups of apicomplexans, including Plasmodium spp. and close relatives of Toxoplasma in the subclass Coccidia, estimated to have diverged several hundred million years ago (Escalante and Ayala, 1995; Douzery et al., 2004; Kuo et al., 2008).”
Adipokinetic hormones and their G protein-coupled receptors emerged in Lophotrochozoa
Li, S., Hauser, F., Skadborg, S. K., Nielsen, S. V., Kirketerp-Møller, N., & Grimmelikhuijzen, C. J. P. (2016) · Scientific Reports · doi:10.1038/srep32789 · Cited by 49
Assembling the spiralian tree of life
Giribet, G., Dunn, C. W., Edgecombe, G. D., Hejnol, A., Martindale, M. Q., & Rouse, G. W. (2009) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199549429.003.0006 · Cited by 50
InsP3 Signaling in Apicomplexan Parasites
Garcia, C. R. S., Alves, E., Pereira, P. H. S., Bartlett, P. J., Thomas, A. P., Mikoshiba, K., Plattner, H., & Sibley, L. (2017) · Current Topics in Medicinal Chemistry · doi:10.2174/1568026617666170130121042 · Cited by 48
“It is estimated that ciliates originated between ~800 and 850 million years [65,66].”
Background
Consistent and contrasting properties of lineage-specific genes in the apicomplexan parasites Plasmodium and Theileria
Kuo, C., & Kissinger, J. C. (2008) · BMC Evolutionary Biology · doi:10.1186/1471-2148-8-108 · Cited by 50
“This tree is consistent with our prior understanding of apicomplexan relationships based on morphology and development [34], rDNA analyses [35,36], and multigene phylogenies [37,38].”
Two complementary recessive genes in duplicated segments control etiolation in rice
Mao, D., Yu, H., Liu, T., Yang, G., & Xing, Y. (2010) · Theoretical and Applied Genetics · doi:10.1007/s00122-010-1453-z · Cited by 47
“5 billion years ago, the chloroplast has become an indivisible portion of its host eukaryotes, and its functions underpin the global ecosystem (Douzery et al. 2004).”
BackgroundInfluential
Transcriptomic analysis of metabolic function in the giant kelp, M acrocystis pyrifera, across depth and season
Konotchick, T., Dupont, C. L., Valas, R. E., Badger, J. H., & Allen, A. E. (2013) · New Phytologist · doi:10.1111/nph.12160 · Cited by 47
“Macrocystis and the Phaeophyceae belong to the Stramenopile lineage which is thought to have diverged from other major eukaryotic groups over a billion years ago (Douzery et al., 2004; Yoon et al., 2004).”
Calcium signaling in closely related protozoan groups (Alveolata): Non-parasitic ciliates (Paramecium, Tetrahymena) vs. parasitic Apicomplexa (Plasmodium, Toxoplasma)
Plattner, H., Sehring, I. M., Mohamed, I. K., de Miranda, K. R., de Souza, W., Billington, R. A., Genazzani, A. A., & Ladenburger, E. (2012) · Cell Calcium · doi:10.1016/j.ceca.2012.01.006 · Cited by 47
The Proterozoic Fossil Record of Heterotrophic Eukaryotes
Porter, S. M. (2007) · Springer eBooks · doi:10.1007/1-4020-5202-2_1 · Cited by 46
“The presence of red algae in rocks 1200 Ma necessarily implies that heterotrophs were present by this time, consistent with molecular clock studies that suggest a diversity of heterotrophic clades in Proterozoic oceans (e.g., Wang et al., 1999; Pawlowski et al., 2003; Douzery et al., 2004; Yoon et al., 2004).”
Background
Horizontal gene transfer of a chloroplast DnaJ-Fer protein to Thaumarchaeota and the evolutionary history of the DnaK chaperone system in Archaea
Petitjean, C., Moreira, D., López‐García, P., & Brochier‐Armanet, C. (2012) · BMC Evolutionary Biology · doi:10.1186/1471-2148-12-226 · Cited by 45
“According to fossil record and molecular dating estimates, the divergence of Viridiplantae from the two other Archaeplastida lineages occurred ~950 million years ago whereas the diversification of Viridiplantae started ~750 million years ago [46].”
Background
MicroRNAs and metazoan phylogeny: big trees from little genes
Sperling, E. A., & Peterson, K. J. (2009) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199549429.003.0015 · Cited by 45
Viral proteins as a potential driver of histone depletion in dinoflagellates
Irwin, N. A. T., Martin, B. J. E., Young, B. P., Browne, M. J. G., Flaus, A., Loewen, C. J. R., Keeling, P. J., & Howe, L. J. (2018) · Nature Communications · doi:10.1038/s41467-018-03993-4 · Cited by 45
Baculovirus genes affecting host function
Thiem, S. M. (2009) · In Vitro Cellular & Developmental Biology - Animal · doi:10.1007/s11626-008-9170-5 · Cited by 44
Vertical Evolution and Horizontal Transfer of CR1 Non-LTR Retrotransposons and Tc1/mariner DNA Transposons in Lepidoptera Species
Sormacheva, I., Smyshlyaev, G., Mayorov, V., Blinov, A. G., Novikov, A., & Novikova, O. (2012) · Molecular Biology and Evolution · doi:10.1093/molbev/mss181 · Cited by 44
Molecular evolution of rbcL in three gymnosperm families: identifying adaptive and coevolutionary patterns
Sen, L., Fares, M. A., Liang, B., Gao, L., Wang, B., Wang, T., & Su, Y. (2011) · Biology Direct · doi:10.1186/1745-6150-6-29 · Cited by 46
“I am not sure that molecular dating is that trustable, even with the use of clock-relaxed models, as illustrated by many controversies in the recent literature (e.g. Graur & Martin 2004 Trends Genet, Douzery et al. 2004 PNAS, Peterson et al. 2004 PNAS, Roger & Hug 2006 Philos Trans, Emerson 2007 Syst Biol), owing to p…”
Method
Opposite Polarity Monospore Genome De Novo Sequencing and Comparative Analysis Reveal the Possible Heterothallic Life Cycle of Morchella importuna
Liu, W., Chen, L., Cai, Y., Zhang, Q., & Bian, Y. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19092525 · Cited by 44
“While more than ten genome sequences were sequenced and are available for each class in Pezizomycotina (Sordariomycetes, Leotiomycetes, Eurotiomycetes, and Dothideomycetes), genome sequencing was only performed for one Orbiliomycetes and two Pezizomycetes species, namely the nematode-trapping fungus, A. oligospora, an…”
BackgroundInfluential
Bisnorgammacerane traces predatory pressure and the persistent rise of algal ecosystems after Snowball Earth
van Maldegem, L. M., Sansjofre, P., Weijers, J. W. H., Wolkenstein, K., Strother, P. K., Wörmer, L., Hefter, J., Nettersheim, B. J., Hoshino, Y., Schouten, S., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-08306-x · Cited by 45
De novo transcriptome assembly of the cubomedusa Tripedalia cystophora, including the analysis of a set of genes involved in peptidergic neurotransmission
Nielsen, S. K. D., Koch, T. L., Hauser, F., Garm, A. L., & Grimmelikhuijzen, C. J. P. (2019) · BMC Genomics · doi:10.1186/s12864-019-5514-7 · Cited by 44
Near Intron Positions Are Reliable Phylogenetic Markers: An Application to Holometabolous Insects
Krauß, V., Thümmler, C., Georgi, F., Lehmann, J., Stadler, P. F., & Eisenhardt, C. (2008) · Molecular Biology and Evolution · doi:10.1093/molbev/msn013 · Cited by 43
Oxytocin/vasopressin-like peptide inotocin regulates cuticular hydrocarbon synthesis and water balancing in ants
Koto, A., Motoyama, N., Tahara, H., McGregor, S., Moriyama, M., Okabe, T., Miura, M., & Keller, L. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1817788116 · Cited by 43
“This places the origin of the oxytocin/vasopressin-like peptide family before the split of the Protostomia and Deuterostomia, >600 Mya (17).”
Subchromosome-Scale Nuclear and Complete Mitochondrial Genome Characteristics of Morchella crassipes
Liu, W., Cai, Y., Zhang, Q., Shu, F., Chen, L., Ma, X., & Bian, Y. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21020483 · Cited by 43
“81 software with Schizophyllum commune, Pleurotus ostreatus, Aspergillus niger, and Neurospora crassa as a fossil calibrated point [64,65].”
Method
Primate Origins: Implications of a Cretaceous Ancestry
Martin, R. D., Soligo, C., & Tavaré, S. (2007) · Folia Primatologica · doi:10.1159/000105145 · Cited by 44
“For a variety of reasons, it has been widely accepted that the earliest primates were quite small-bodied, weighing no more than 500 g and possibly much less [ Dagosto, 1988; Martin, 1990; Cartmill, 1992; Hamrick, 1999; Larson et al., 2000; Gebo, 2004; but see Soligo and Muller, 1999, for an earlier alternative view].”
Background
Evolution of the class C GPCR Venus flytrap modules involved positive selected functional divergence
Cao, J., Huang, S., Qian, J., Huang, J., Li, J., Su, Z., Yang, J. Y., & Liu, J. (2009) · BMC Evolutionary Biology · doi:10.1186/1471-2148-9-67 · Cited by 45
“In this study, a GABAB-like receptor from Dictyostelium discoideum (slime mold), GrlJ, was used as the root (1085 million years ago, Mya) to calibrate the time scale [37,38].”
Method
Recurrent Horizontal Transfers of Chapaev Transposons in Diverse Invertebrate and Vertebrate Animals
Zhang, H., Feschotte, C., Han, M., & Zhang, Z. (2014) · Genome Biology and Evolution · doi:10.1093/gbe/evu112 · Cited by 42
Dynamics of Reductive Genome Evolution in Mitochondria and Obligate Intracellular Microbes
Khachane, A. N., Timmis, K. N., & dos Santos, V. A. P. M. (2006) · Molecular Biology and Evolution · doi:10.1093/molbev/msl174 · Cited by 42
“…from the free-living form to the intracellular environment 2,000 Myr ago (Dyall et al. 2004; Embley and Martin 2006), but prior to the subsequent divergence of the eukaryotic lineages, estimated to have occurred around 1,200 Myr ago (Javaux et al. 2001; Douzery et al. 2004; Embley and Martin 2006).”
BackgroundResult
Macroalgal deep genomics illuminate multiple paths to aquatic, photosynthetic multicellularity
Nelson, D. R., Mystikou, A., Jaiswal, A. K., Rad‐Menéndez, C., Preston, M. J., Boever, F. D., Assal, D. C. E., Daakour, S., Lomas, M. W., Twizere, J., et al. (2024) · Molecular Plant · doi:10.1016/j.molp.2024.03.011 · Cited by 41
Possible import routes of proteins into the cyanobacterial endosymbionts/plastids of Paulinella chromatophora
Mackiewicz, P., Bodył, A., & Gagat, P. (2011) · Theory in Biosciences · doi:10.1007/s12064-011-0147-7 · Cited by 41
“…endosymbiosis and Paulinella chromatophora Available data clearly demonstrate that plastids evolved from free-living cyanobacteria acquired by heterotrophic eukaryotic cells 1–2 billion years ago (Butterfield 2000; Douzery et al. 2004; Yoon et al. 2004; Kutschera and Niklas 2005; Kutschera 2009).”
Background
Accelerated Evolutionary Rate of Housekeeping Genes in Tunicates
Tsagkogeorga, G., Turón, X., Galtier, N., Douzery, E., & Delsuc, F. (2010) · Journal of Molecular Evolution · doi:10.1007/s00239-010-9372-9 · Cited by 43
“We used the previously defined reference topology after pruning Nematostella, and set the prior age of the root at 700 Mya (Douzery et al. 2004) with no additional constraints on nodes.”
MethodSelf-citation
Molecular Phylogeny of Sequenced Saccharomycetes Reveals Polyphyly of the Alternative Yeast Codon Usage
Mühlhausen, S., & Kollmar, M. (2014) · Genome Biology and Evolution · doi:10.1093/gbe/evu152 · Cited by 41
The ghost plastid of Choreocolax polysiphoniae
Salomaki, E. D., Nickles, K. R., & Lane, C. E. (2015) · Journal of Phycology · doi:10.1111/jpy.12283 · Cited by 41
“…parasites 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. 2010).”
Background
Evolution of floral traits and impact of reproductive mode on diversification in the phlox family (Polemoniaceae)
Landis, J. B., Bell, C. D., Hernandez, M., Zenil‐Ferguson, R., McCarthy, E. W., Soltis, P. S., & Soltis, P. S. (2018) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2018.06.035 · Cited by 41
A merciful death for the “earliest bilaterian,” Vernanimalcula
Bengtson, S., Cunningham, J. A., Yin, C., & Donoghue, P. C. J. (2012) · Evolution & Development · doi:10.1111/j.1525-142x.2012.00562.x · Cited by 40
Characterization and Fine Mapping of a Novel Rice Albino Mutant low temperature albino 1
Peng, Y., Zhang, Y., Lv, J., Zhang, J., Li, P., Shi, X., Wang, Y., Zhang, H., He, Z., & Teng, S. (2012) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2012.05.001 · Cited by 40
“The chloroplast of photosynthetic eukaryotes where photosynthesis takes place functions as the most important supporter of carbon fixation and energy transformation (Douzery et al., 2004).”
Background
Genome-wide analysis of basic helix−loop−helix family transcription factors and their role in responses to abiotic stress in carrot
Chen, Y.-Y., Li, M., Wu, X., Huang, Y., Ma, J., & Xiong, A. (2015) · Molecular Breeding · doi:10.1007/s11032-015-0319-0 · Cited by 40
“The growth of the number of bHLH TFs may have occurred independently in plants and metazoans, and some bHLH TFs in metazoans may have originated before their speciation in land plants (Douzery et al. 2004; Peterson et al. 2004).”
A comparative genomics study of neuropeptide genes in the cnidarian subclasses Hexacorallia and Ceriantharia
Koch, T. L., & Grimmelikhuijzen, C. J. P. (2020) · BMC Genomics · doi:10.1186/s12864-020-06945-9 · Cited by 40
Evolution and integration of innate immune systems from fruit flies to man: lessons and questions
Martinelli, C., & Reichhart, J. (2005) · Journal of Endotoxin Research · doi:10.1179/096805105x37411 · Cited by 40
Inverse relationship between longevity and evolutionary rate of mitochondrial proteins in mammals and birds
Galtier, N., Blier, P. U., & Nabholz, B. (2008) · Mitochondrion · doi:10.1016/j.mito.2008.11.006 · Cited by 39
The Expanded Kinesin-13 Repertoire of Trypanosomes Contains Only One Mitotic Kinesin Indicating Multiple Extra-Nuclear Roles
Wickstead, B., Carrington, J. T., Gluenz, E., & Keith Gull, B. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015020 · Cited by 39
“These events are still quite old, predating the split of Leishmania and Trypanosoma ,250 Mya [57], but they do demonstrate a surprising plasticity in Kinesin-13 function.”
Background
Fast and accurate branch lengths estimation for phylogenomic trees
Binet, M., Gascuel, O., Scornavacca, C., Douzery, E., & Pardi, F. (2016) · BMC Bioinformatics · doi:10.1186/s12859-015-0821-8 · Cited by 39
“Yet, evolutionary distance information is essential to answer several important biological questions, from molecular dating [12, 13] of events such as speciations, to the reconciliation of gene trees with a species tree [14], or to the measure of biodiversity in conservation biology [15].”
BackgroundSelf-citation
Nutrient status regulates MED19a phase separation for ORESARA1 ‐dependent senescence
Cheng, S. L. H., Wu, H., Xu, H., Singh, R. M., Yao, T., Jang, I., & Chua, N. (2022) · New Phytologist · doi:10.1111/nph.18478 · Cited by 38
“1600 Ma (Douzery et al ., 2004; Peterson & Butterﬁeld, 2005).”
A Protocol for Diagnosing the Effect of Calibration Priors on Posterior Time Estimates: A Case Study for the Cambrian Explosion of Animal Phyla
Battistuzzi, F. U., Billing-Ross, P., Murillo, O., Filipski, A., & Kumar, S. (2015) · Molecular Biology and Evolution · doi:10.1093/molbev/msv075 · Cited by 34
“…the dates from molecular data and the fossil data (Doolittle et al. 1996; Bromham et al. 1999; Aris-Brosou and Yang 2002; Aris-Brosou and Yang 2003; Douzery et al. 2004; Peterson et al. 2004, 2008; Peterson and Butterfield 2005; Cartwright and Collins 2007; Erwin et al. 2011; Gueidan et al. 2011;…”
Background
The Precambrian emergence of animal life: a geobiological perspective
Gaidos, E. J., DuBuc, T. Q., Dunford, M. D., MCANDREW, P., PADILLA‐GAMIÑO, J., STUDER, B., Weersing, K., & Stanley, S. M. (2007) · Geobiology · doi:10.1111/j.1472-4669.2007.00125.x · Cited by 39
Plastid Origin: Replaying the Tape
Rodríguez‐Ezpeleta, N., & Philippe, H. (2006) · Current Biology · doi:10.1016/j.cub.2006.01.006 · Cited by 38
“Plastids have diverged enormously from their cyanobacterial ancestor during their ~1 billion years of intracellular evolution [9].”
BackgroundSelf-citation
The mouth, the anus, and the blastopore—open questions about questionable openings
Hejnol, A., & Martindale, M. Q. (2009) · Animal Evolution · doi:10.1093/acprof:oso/9780199549429.003.0004 · Cited by 37
The phylogeny, evolutionary developmental biology, and paleobiology of the Deuterostomia: 25 years of new techniques, new discoveries, and new ideas
Peterson, K. J., & Eernisse, D. J. (2016) · Organisms Diversity & Evolution · doi:10.1007/s13127-016-0270-x · Cited by 37
“…become even more curious when viewed from the perspective of the molecular clock, which suggested (e.g., Runnegar 1982) and continues to suggest (Douzery et al. 2004; Peterson et al. 2008; Erwin et al. 2011) that animal divergence times preceded the Cambrian by possibly tens to hundreds of…”
BackgroundInfluential
Genome-wide analysis of the BES1 transcription factor family in Chinese cabbage (Brassica rapa ssp. pekinensis)
Wu, P., Song, X., Wang, Z., Duan, W., Hu, R., Wang, W., Li, Y., & Hou, X. (2016) · Plant Growth Regulation · doi:10.1007/s10725-016-0166-y · Cited by 37
Evolutionary dynamics of protein domain architecture in plants
Zhang, X. C., Wang, Z., Zhang, X., Le, M. H., Sun, J., Xu, D. H., Cheng, J., & Stacey, G. S. (2012) · BMC Evolutionary Biology · doi:10.1186/1471-2148-12-6 · Cited by 38
“It diverged from the lineages leading to higher plants approximately 443-490 million years ago [17].”
Background
Calcium Regulation in the Protozoan Model, Paramecium tetraurelia
Plattner, H. (2013) · Journal of Eukaryotic Microbiology · doi:10.1111/jeu.12070 · Cited by 36
Paulinella longichromatophora sp. nov., a New Marine Photosynthetic Testate Amoeba Containing a Chromatophore.
Kim, S., & Park, M. (2016) · Protist · doi:10.1016/j.protis.2015.11.003 · Cited by 23
Overcoming among‐lineage rate heterogeneity to infer the divergence times and biogeography of the clubmoss family Lycopodiaceae
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Time Calibrated Morpho-molecular Classification of Nassellaria (Radiolaria)
Sandín, M. M., Pillet, L., Biard, T., Poirier, C. L., Bigeard, E., Romac, S., Suzuki, N., & Not, F. (2019) · Protist · doi:10.1016/j.protis.2019.02.002 · Cited by 36
Phycobilisomes and Phycobiliproteins in the Pigment Apparatus of Oxygenic Photosynthetics: From Cyanobacteria to Tertiary Endosymbiosis
Stadnichuk, I. N., & Kusnetsov, V. V. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24032290 · Cited by 35
Unicellular Eukaryotes as Models in Cell and Molecular Biology
Simon, M. C., & Plattner, H. (2014) · International review of cytology · doi:10.1016/b978-0-12-800255-1.00003-x · Cited by 35
“800 million years (Douzéry et al., 2004; Wright and Lynn, 1997).”
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Molecular aspects of calcium signalling at the crossroads of unikont and bikont eukaryote evolution – The ciliated protozoan Paramecium in focus
Plattner, H. (2014) · Cell Calcium · doi:10.1016/j.ceca.2014.12.002 · Cited by 34
Stability-based sorting: The forgotten process behind (not only) biological evolution
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Radiation of Meso-Neoproterozoic and Early Cambrian protists inferred from the microfossil record of China
Leiming, Y., & Xunlai, Y. (2007) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2007.03.028 · Cited by 34
BODY MASS AND TEMPERATURE INFLUENCE RATES OF MITOCHONDRIAL DNA EVOLUTION IN NORTH AMERICAN CYPRINID FISH
Estabrook, G. F., Smith, G. R., & Dowling, T. E. (2007) · Evolution · doi:10.1111/j.1558-5646.2007.00089.x · Cited by 34
“…different molecular rates and evolution of rate changes, based on nucleotide distributions among branches (e.g., Sanderson 1997, 2002; Rambaut and Bromham 1998; Thorne et al. 1998; Huelsenbeck et al. 2000; Yoder and Yang 2000; Kishino et al. 2001; Thorne and Kishino 2002; Douzery et al. 2004).”
Background
Pericentrin-mediated SAS-6 recruitment promotes centriole assembly
Ito, D., Zitouni, S., Jana, S. C., Duarte, P., Surkont, J., Carvalho-Santos, Z., Pereira‐Leal, J. B., Ferreira, M. G., & Bettencourt‐Dias, M. (2019) · eLife · doi:10.7554/elife.41418 · Cited by 38
“Despite the one billion years separating yeasts from animals (Douzery et al., 2004; Parfrey et al., 2011), SAS-6-GFP, Bld10-GFP and YFP-SAS-4 co-localized with fission yeast Sid4 to the SPB (Figure 2A and B).”
Background
A timeframe for mint evolution: towards a better understanding of trait evolution and historical biogeography in Lamiaceae
Rose, J. P., Xiang, C., Sytsma, K. J., & Drew, B. T. (2021) · Botanical Journal of the Linnean Society · doi:10.1093/botlinnean/boab104 · Cited by 33
Diversification of NRT2 and the Origin of Its Fungal Homolog
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“Molecular clock analysesofnuclearproteins and ribosomalgenes suggest that the divergence of Dikarya from other fungi occurred during (Douzery et al. 2004; Berney and Pawlowski 2006) or before (Heckman et al. 2001; Hedges et al. 2004; Padovan et al. 2005) this period of massive oxygen accumulation…”
Background
Late Proterozoic Transitions in Climate, Oxygen, and Tectonics, and the Rise of Complex Life
Planavsky, N. J., Tarhan, L. G., Bellefroid, E. J., Evans, D. A. D., Reinhard, C. T., Love, G. D., & Lyons, T. W. (2015) · The Paleontological Society Papers · doi:10.1017/s1089332600002965 · Cited by 32
“Historically, molecular-clock estimates for the origin of eukaryotes range widely from the A r c h e a n t o t h e P a l e o p r o t e r o z o i c , Mesoproterozoic, or even the Neoproterozoic (e.g., Cavalier-Smith, 2002; Douzery et al., 2004; Hedges et al., 2004; Yoon et al., 2004).”
BackgroundInfluential
Of early animals, anaerobic mitochondria, and a modern sponge
Mentel, M., Roettger, M., Leys, S. P., Tielens, A. G. M., & Martin, W. F. (2014) · BioEssays · doi:10.1002/bies.201400060 · Cited by 32
“5 Gy ago, as fossils clearly representing eukaryotic protists are found in rocks of that age [29, 30], and molecular estimates for the timing of eukaryotic evolution are consistent with that view [8, 31, 32].”
Background
Reconstruction of highly heterogeneous gene-content evolution across the three domains of life
Iwasaki, W., & Takagi, T. (2007) · Bioinformatics · doi:10.1093/bioinformatics/btm165 · Cited by 30
The genome, transcriptome, and proteome of the nematode Steinernema carpocapsae: evolutionary signatures of a pathogenic lifestyle
Rougon‐Cardoso, A., Flores-Ponce, M., Ramos-Aboites, H. E., Martínez-Guerrero, C. E., Hao, Y., Cunha, L. F. N., Rodríguez-Martínez, J. A., Ovando‐Vázquez, C., Bermúdez‐Barrientos, J. R., Abreu‐Goodger, C., et al. (2016) · Scientific Reports · doi:10.1038/srep37536 · Cited by 31
Saccharomyces genome database informs human biology
Skrzypek, M. S., Nash, R. S., Wong, E. D., MacPherson, K. A., Hellerstedt, S. T., Engel, S. R., Karra, K., Weng, S., Sheppard, T. K., Binkley, G., et al. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx1112 · Cited by 31
“Yeast and humans are separated by a billion years of evolution (3), yet there are thousands of recognizable orthologs between the two species (4).”
Background
Essential Genes of the Parasitic Apicomplexa
Oberstaller, J., Otto, T. D., Rayner, J. C., & Adams, J. H. (2021) · Trends in Parasitology · doi:10.1016/j.pt.2020.11.007 · Cited by 31
Centromere-associated topoisomerase activity in bloodstream form Trypanosoma brucei
Obado, S. O., Bot, C., Echeverry, M. C., Bayona, J. C., Álvarez, V. E., Taylor, M. C., & Kelly, J. M. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq839 · Cited by 31
“These parasites diverged between 100 and 200 million years ago (44) and there are distinct differences in the organization and composition of centromeric DNA in the two species (28,29).”
Background
Geobiology of the Proterozoic Eon
Lyons, T. W., Reinhard, C. T., Love, G. D., & Xiao, S. (2012) · Wiley eBooks · doi:10.1002/9781118280874.ch20 · Cited by 31
“Molecular clock estimates, although complicated by calibration issues, imply that major eukaryotic clades diverged prior to and survived the snowball Earth events (Douzery et al., 2004).”
Background
Enigmatic chambered structures in Cryogenian reefs: The oldest sponge-grade organisms?
Wallace, M. W., Hood, A. V. S., Woon, E. M. S., Hoffmann, K.-H., & Reed, C. P. (2014) · Precambrian Research · doi:10.1016/j.precamres.2014.09.020 · Cited by 30

Authors: Douzery, E. J. P., Snell, E. A., Bapteste, E., Delsuc, F., & Philippe, H.
Affiliations: Centre National de la Recherche Scientifique (FR)
ORCID: Douzery, Emmanuel J. P.
Bapteste, Eric
Delsuc, Frédéric
Philippe, Hervé
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
DOI: 10.1073/pnas.0403984101
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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The timing of eukaryotic evolution: Does a relaxed molecular clock reconcile proteins and fossils?

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