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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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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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
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“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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“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.
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Eukaryotic organisms in Proterozoic oceans
Knoll, A. H., Javaux, E. J., Hewitt, D., & Cohen, P. (2006) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2006.1843 · Cited by 701
“…2002a), but molecular clock estimates commonly suggest an earlier Proterozoic origin and later Proterozoic diversification of the clade (Doolittle et al. 1996; Douzery et al. 2004; tribution of 14 to a Discussion Meeting Issue ‘Major steps in ution’. r for correspondence (aknoll@oeb.harvard.edu).”
Background
Phylogenomics: The beginning of incongruence?
JEFFROY, O., BRINKMANN, H., DELSUC, F., & PHILIPPE, H. (2006) · Trends in Genetics · doi:10.1016/j.tig.2006.02.003 · Cited by 698
“[1] ,a nd alternatively by probabilistic methods – Bayesian inference (BI) [8] or maximum likelihood (ML) [9–11] – because these methods are generally considered the most accurate [12,13] .I n addition, because the diversification of these yeasts is ancient (O250 Mya [ 14 ]) and amino acid sequences evolve more slowly…”
MethodSelf-citation
Babesia: A world emerging
Schnittger, L., Rodríguez, A. E., Florin‐Christensen, M., & Morrison, D. A. (2012) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2012.07.004 · Cited by 629
A general comparison of relaxed molecular clock models
Lepage, T., Bryant, D., Philippe, H., & Lartillot, N. (2007) · Molecular Biology and Evolution · doi:10.1093/molbev/msm193 · Cited by 546
Self-citation
The tree of eukaryotes
Keeling, P. J., Burger, G., Durnford, D. G., Lang, B. F., Lee, R. W., Pearlman, R. E., Roger, A. J., & Gray, M. W. (2005) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2005.09.005 · Cited by 579
“aimed at dating the earliest divergences in the tree of eukaryotes using fossil-calibrated ‘molecular dating’ methods [77, 78 ].”
MethodInfluential
Monophyly of Primary Photosynthetic Eukaryotes: Green Plants, Red Algae, and Glaucophytes
Rodríguez‐Ezpeleta, N., Brinkmann, H., Burey, S. C., Roure, B., Burger, G., Löffelhardt, W., Bohnert, H. J., Philippe, H., & Lang, B. F. (2005) · Current Biology · doi:10.1016/j.cub.2005.06.040 · Cited by 559
“5 billion years ago [1, 2], eukaryotic organisms acquired the ability to convert light into chemical energy through endosymbiosis with a Cyanobacterium (e.”
BackgroundSelf-citation
Multigene Analyses of Bilaterian Animals Corroborate the Monophyly of Ecdysozoa, Lophotrochozoa, and Protostomia
Philippe, H., Lartillot, N., & Brinkmann, H. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msi111 · Cited by 551
“However, this generally implies allowing for missing or partial sequences of some genes from some species (e.g., the amount of missing data is of 12.5% [Murphy et al. 2001], 20% [Qiu et al. 1999], or 25% [Douzery et al. 2004]).”
BackgroundInfluentialSelf-citation
RAG1 Core and V(D)J Recombination Signal Sequences Were Derived from Transib Transposons
Kapitonov, V. V., & Jurka, J. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030181 · Cited by 521
“The basic timescale of the evolutionary tree is based on published literature [49–51].”
Method
The Origin and Establishment of the Plastid in Algae and Plants
Reyes-Prieto, A., Weber, A. P. M., & Bhattacharya, D. (2007) · Annual Review of Genetics · doi:10.1146/annurev.genet.41.110306.130134 · Cited by 453
“Although still controversial (23), recent analyses suggest that the primary plastid was established ca.”
Background
Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexityPreprint
Freeling, M., & Thomas, B. C. (2006) · Genome Research · doi:10.1101/gr.3681406 · Cited by 463
Molecular Phylogeny and Divergence Times of Deuterostome Animals
Blair, J. E., & Hedges, S. B. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msi225 · Cited by 451
“Some studies have produced considerably younger divergence times among deuterostomes (Aris-Brosou and Yang 2002, 2003; Douzery et al. 2004) but suffer from methodological biases, causing their results to conflict with other well-supported aspects of the eukaryote fossil record (Blair and Hedges…”
Systematic humanization of yeast genes reveals conserved functions and genetic modularity
Kachroo, A. H., Laurent, J. M., Yellman, C. M., Meyer, A. G., Wilke, C. O., & Marcotte, E. M. (2015) · Science · doi:10.1126/science.aaa0769 · Cited by 447
A phylostratigraphy approach to uncover the genomic history of major adaptations in metazoan lineages
Domazet‐Lošo, T., Brajković, J., & Tautz, D. (2007) · Trends in Genetics · doi:10.1016/j.tig.2007.08.014 · Cited by 421
Dating divergences in the Fungal Tree of Life: review and new analyses
Taylor, J. W., & Berbee, M. L. (2006) · Mycologia · doi:10.3852/mycologia.98.6.838 · Cited by 430
“…(Blagoderov et al 2002, Peterson et al 2004) and a maximum of 417 000 000 y, the age of the first primitive hexapod fossils (Gaunt and Miles 2002, Douzery et al 2004); and the divergence of eudicots within the angiosperms, with a minimum age of 144 000 000 and maximum of 206 000 000 y (Sanderson…”
BackgroundMethodInfluential
Genomic adaptation to polyphagy and insecticides in a major East Asian noctuid pest
Cheng, T., Wu, J., Wu, Y., Chilukuri, R. V. E., Huang, L., Yamamoto, K., Feng, L., Li, W., Chen, Z., Guo, H., et al. (2017) · Nature Ecology & Evolution · doi:10.1038/s41559-017-0314-4 · Cited by 412
Paleobiological Perspectives on Early Eukaryotic Evolution
Knoll, A. H. (2014) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a016121 · Cited by 394
“…with some positing a long interval of eukaryotic evolution before Neoproterozoic radiation (e.g., Yoon et al. 2004; Hedges et al. 2004; Parfrey et al 2011), while others suggest a shorter fuse (e.g., Douzery et al. 2004, Berney and Pawlowski 2006; Chernikova et al. 2011; Shih and Matzke 2013).”
Background
Unexpected complexity of the Aquaporin gene family in the moss Physcomitrella patens
Danielson, J. Å., & Johanson, U. (2008) · BMC Plant Biology · doi:10.1186/1471-2229-8-45 · Cited by 409
“patens is a moss (bryophyte) and as such diverged from the lineage leading to higher plants approximately 443– 490 million years ago, before the evolution of vascular plants [34].”
Animal Evolution and the Molecular Signature of Radiations Compressed in Time
Rokas, A., Krüger, D., & Carroll, S. B. (2005) · Science · doi:10.1126/science.1116759 · Cited by 374
Origin of the Eumetazoa: Testing ecological predictions of molecular clocks against the Proterozoic fossil record
Peterson, K. J., & Butterfield, N. J. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503660102 · Cited by 361
The origin and evolution of mycorrhizal symbioses: from palaeomycology to phylogenomics
Strullu‐Derrien, C., Selosse, M., Kenrick, P., & Martin, F. M. (2018) · New Phytologist · doi:10.1111/nph.15076 · Cited by 355
Identification of the Maturation Factor for Dual Oxidase
Grasberger, H., & Refetoff, S. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.c600095200 · Cited by 340
Molecular Phylogenetics, Temporal Diversification, and Principles of Evolution in the Mustard Family (Brassicaceae)
Couvreur, T. L. P., Franzke, A., Al-Shehbaz, I. A., Bakker, F. T., Koch, М. A., & Mummenhoff, K. (2009) · Molecular Biology and Evolution · doi:10.1093/molbev/msp202 · Cited by 333
Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes
Nowack, E. C. M., Melkonian, M., & Glöckner, G. (2008) · Current Biology · doi:10.1016/j.cub.2008.02.051 · Cited by 329
“Yet the reasons for the apparent singularity of plastid acquisition through endosymbiosis, which is thought to have taken place more than a billion years ago [6], have remained enigmatic.”
Background
Beyond the Whole-Genome Duplication: Phylogenetic Evidence for an Ancient Interspecies Hybridization in the Baker's Yeast Lineage
Marcet‐Houben, M., & Gabaldón, T. (2015) · PLoS Biology · doi:10.1371/journal.pbio.1002220 · Cited by 334
“[65]) was used as calibration point.”
Origin of land plants: Do conjugating green algae hold the key?
Wodniok, S., Brinkmann, H., Glöckner, G., Heidel, A. J., Philippe, H., Melkonian, M., & Becker, B. (2011) · BMC Evolutionary Biology · doi:10.1186/1471-2148-11-104 · Cited by 333
“Streptophyte algae and embryophytes together constitute the division Streptophyta, which likely split from the Chlorophyta (all other green algae) about 725-1200 MY ago [10-12].”
BackgroundSelf-citation
Early photosynthetic eukaryotes inhabited low-salinity habitats
Sánchez‐Baracaldo, P., Raven, J. A., Pisani, D., & Knoll, A. H. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1620089114 · Cited by 332
“9 Bya (56); others based on the α and β subunits of ATP synthase and the elongation factor thermo unstable (45, 67) propose ∼1.”
Background
The Ediacaran emergence of bilaterians: congruence between the genetic and the geological fossil records
Peterson, K. J., Cotton, J. A., Gehling, J. G., & Pisani, D. (2008) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2007.2233 · Cited by 313
Estimating the Phanerozoic history of the Ascomycota lineages: Combining fossil and molecular data
Beimforde, C., Feldberg, K., Nylinder, S., Rikkinen, J. K., Tuovila, H., Dörfelt, H., Gube, M., Jackson, D. J., Joachim Reitner, A., Seyfullah, L. J., et al. (2014) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2014.04.024 · Cited by 311
“…a metacapnodiaceous fossil and Palaeocurvularia for the split of Dothideomycetes and Arthoniomycetes, together with several non-ascomycotan (Taylor et al., 1994; Redecker et al., 2000; Hibbett et al., 1995, 1997), and non-fungal (Crane et al., 1995; Douzery et al., 2004) calibration constraints.”
Background
The Origins of Multicellularity and the Early History of the Genetic Toolkit For Animal Development
Rokas, A. (2008) · Annual Review of Genetics · doi:10.1146/annurev.genet.42.110807.091513 · Cited by 312
“75 bya (82, 97), a date strikingly contemporaneous with the emergence of the first ancestors of fungi and animals (30, 82).”
Background
The evolution, metabolism and functions of the apicoplast
Lim, L., & McFadden, G. I. (2010) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2009.0273 · Cited by 356
“There are no fossil records for apicomplexa but molecular dating estimates the apicomplexan protists to have evolved between 600–800 Ma ago (Douzery et al. 2004) and there are fossils of the sister group dinoflagellates that are in excess of 400 million years old.”
Background
A review of neurohormone GPCRs present in the fruitfly Drosophila melanogaster and the honey bee Apis mellifera
Hauser, F., Cazzamali, G., Williamson, M. P., Blenau, W., & Grimmelikhuijzen, C. J. P. (2006) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2006.07.005 · Cited by 302
“3), these ‘‘ligand-hops’’ have occurred before the split of the ancestors of the present-day flies (Diptera) and honey bees (Hymenoptera), which is about 350 million years ago (Douzery et al., 2004).”
Background
Origin and diversification of the basic helix-loop-helix gene family in metazoans: insights from comparative genomics
Simionato, E., Ledent, V., Richards, G. S., Thomas‐Chollier, M., Kerner, P., Coornaert, D., Degnan, B. M., & Vervoort, M. (2007) · BMC Evolutionary Biology · doi:10.1186/1471-2148-7-33 · Cited by 292
“Since this ancestor which is estimated to have lived some 600–700 millions years ago [24,25], the bHLH complement in bilaterians is remarkably stable.”
Background
On the Age of Eukaryotes: Evaluating Evidence from Fossils and Molecular Clocks
Eme, L., Sharpe, S. C., Brown, M. W., & Roger, A. J. (2014) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a016139 · Cited by 287
“Douzery et al. (2004) estimated the age of LECA and other major groups using a Bayesian RMC approach calibrated with, for the first time, six paleontological constraints from the Phanerozoic.”
BackgroundMethodResultInfluential
Dating the molecular clock in fungi – how close are we?
Berbee, M. L., & Taylor, J. W. (2010) · Fungal Biology Reviews · doi:10.1016/j.fbr.2010.03.001 · Cited by 285
“If, however, it could be considered a Pezizomycotina, it would push the divergence of Ascomycota and Basidiomycota back to 843 Ma, and if it were considered a Sordariomycete, back to 1.489 Ba (Taylor and Berbee, 2006) (Fig.”
BackgroundInfluential
An Empirical Assessment of Long-Branch Attraction Artefacts in Deep Eukaryotic Phylogenomics
Brinkmann, H., van der Giezen, M., Zhou, Y., de Raucourt, G. P., & Philippe, H. (2005) · Systematic Biology · doi:10.1080/10635150500234609 · Cited by 286
Self-citation
Three-dimensional preservation of cellular and subcellular structures suggests 1.6 billion-year-old crown-group red algae
Bengtson, S., Sallstedt, T., Belivanova, V., & Whitehouse, M. (2017) · PLOS Biology · doi:10.1371/journal.pbio.2000735 · Cited by 284
Cell evolution and Earth history: stasis and revolution
Cavalier‐Smith, T. (2006) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2006.1842 · Cited by 282
“…of the eukaryote tree and strong evidence that extant anaerobic eukaryotes probably all have organelles (hydrogenosomes or mitosomes) evolutionarily derived from aerobic mitochondria (Embley 2006) is that the last common ancestor of all eukaryotes was an aerobic amoeboflagellate with mitochondria.”
Background
The origin of eukaryotes: a reappraisal
Duve, C. D. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2071 · Cited by 273
Gene family innovation, conservation and loss on the animal stem lineage
(2018) · doi:10.7554/elife.34226 · Cited by 226
The sea cucumber genome provides insights into morphological evolution and visceral regeneration
Zhang, X., Sun, L., Yuan, J., Sun, Y., Gao, Y., Zhang, L., Li, S., Dai, H., Hamel, J., Liu, C., et al. (2017) · PLoS Biology · doi:10.1371/journal.pbio.2003790 · Cited by 267
The making of a chloroplast
Waters, M. T., & Langdale, J. A. (2009) · The EMBO Journal · doi:10.1038/emboj.2009.264 · Cited by 261
“EMBO openEMBO Member‘s Review”
BackgroundInfluential
Distinct Dynamics of HISTONE3 Variants between the Two Fertilization Products in Plants
Ingouff, M., Hamamura, Y., Gourgues, M., Higashiyama, T., & Berger, F. (2007) · Current Biology · doi:10.1016/j.cub.2007.05.019 · Cited by 258
The Evolution of Invertebrate Gene Body Methylation
Sarda, S., Zeng, J., Hunt, B. G., & Yi, S. V. (2012) · Molecular Biology and Evolution · doi:10.1093/molbev/mss062 · Cited by 258
The Geological Succession of Primary Producers in the Oceans
KNOLL, A. H., SUMMONS, R. E., WALDBAUER, J. R., & ZUMBERGE, J. E. (2007) · Evolution of Primary Producers in the Sea · doi:10.1016/b978-012370518-1/50009-6 · Cited by 249
“On the other hand, some molecular clock analyses suggest divergence times for the plastids in photosynthetic chromoalveolates well back into the Proterozoic (Douzery et al. 2004; Yoon et al. 2004).”
Background
Deciphering deuterostome phylogeny: molecular, morphological and palaeontological perspectives
Swalla, B. J., & Smith, A. B. (2008) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2007.2246 · Cited by 253
“2005) and other analyses that apply potentially more appropriate models (Douzery et al. 2004) have continued to find somewhat deeper divergence dates for the Bilateria.”
GATA2 haploinsufficiency caused by mutations in a conserved intronic element leads to MonoMAC syndrome
Hsu, A. P., Johnson, K. D., Falcone, E. L., Sanalkumar, R., Sanchez, L. A., Hickstein, D. D., Cuellar‐Rodríguez, J., Lemieux, J. E., Zerbe, C. S., Bresnick, E. H., et al. (2013) · Blood · doi:10.1182/blood-2012-08-452763 · Cited by 251
Initial Diversification of Living Amphibians Predated the Breakup of Pangaea
Mauro, D. S., Vences, M., Alcobendas, M., Zardoya, R., & Meyer, A. (2005) · The American Naturalist · doi:10.1086/429523 · Cited by 255
“Limited taxon sampling or calibration points can seriously affect molecular dating estimates (Douzery et al. 2004).”
Relaxed molecular clocks for dating historical plant dispersal events
Renner, S. S. (2005) · Trends in Plant Science · doi:10.1016/j.tplants.2005.09.010 · Cited by 241
Modern proteomes contain putative imprints of ancient shifts in trace metal geochemistry
Dupont, C. L., Yang, S., Palenik, B., & Bourne, P. E. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605798103 · Cited by 236
A genome-wide inventory of neurohormone GPCRs in the red flour beetle Tribolium castaneum
Hauser, F., Cazzamali, G., Williamson, M. P., Park, Y., Li, B., Tanaka, Y., Predel, R., Neupert, S., Schachtner, J., Verleyen, P., et al. (2007) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2007.10.003 · Cited by 239
Evolution and pathology in Chagas disease: a review
Teixeira, A. R., Nascimento, R. J., & Sturm, N. R. (2006) · Memórias do Instituto Oswaldo Cruz · doi:10.1590/s0074-02762006000500001 · Cited by 237
“The constant accumulation of mutations affecting aminoacid change in proteins during evolution is thus accountable (Douzery et al. 2004).”
Background
Gata2, Fli1, and Scl form a recursively wired gene-regulatory circuit during early hematopoietic development
Pimanda, J. E., Ottersbach, K., Knezevic, K., Kinston, S., Chan, W. Y. I., Wilson, N. K., Landry, J.-R., Wood, A. D., Kolb-Kokocinski, A., Green, A. R., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0707045104 · Cited by 228
Fungi evolved right on track
Lücking, R., Huhndorf, S. M., Pfister, D. H., Plata, E. R., & Lumbsch, H. T. (2009) · Mycologia · doi:10.3852/09-016 · Cited by 232
“It was even suggested that it could fall outside the euascomycetes (Pezizomycotina), and possible links with the enigmatic taphrinomycete Neolecta (Landvik et al 2003) were discussed (Eriksson 2005, Taylor and Berbee 2006, Berbee and Taylor 2007).”
BackgroundInfluential
Molecular dating of phylogenetic trees: A brief review of current methods that estimate divergence times
Rutschmann, F. (2005) · Diversity and Distributions · doi:10.1111/j.1366-9516.2006.00210.x · Cited by 228
Molecular dating when rates vary
Welch, J. J., & Bromham, L. D. (2005) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2005.02.007 · Cited by 228
“The influence of the prior diminishes, however, with the amount of sequence data used [33,34, 42 ].”
MethodResult
Rooting the tree of life by transition analyses.
Cavalier‐Smith, T. (2006) · Biology Direct · doi:10.1186/1745-6150-1-19 · Cited by 224
“Roger and Hug [35] indeed reanalyzed those very data by a technically superior method estimating parameters for each gene separately, not concatenating them all; this yields an even younger date of ~900 My (not 1100 My as in [34]) for the eukaryote cenancestor – strictly speaking the divergence between Amoebozoa (the…”
BackgroundMethodInfluential
Early Diverging Fungi: Diversity and Impact at the Dawn of Terrestrial Life
Berbee, M. L., James, T. Y., & Strullu‐Derrien, C. (2017) · Annual Review of Microbiology · doi:10.1146/annurev-micro-030117-020324 · Cited by 232
“Somewhere between 1,481 and 900 Mya (26, 93) that common ancestor had a single flagellum that beat to propel it forward (92, 131).”
Background
Early evolution of the Eukaryota
Butterfield, N. J. F. (2014) · Palaeontology · doi:10.1111/pala.12139 · Cited by 225
“…billion-year extrapolation error have precluded any consensus on the timing of LECA (Roger and Hug 2006; Eme et al. 2014): estimates range from less than 1200 Ma (Douzery et al. 2004; Berney and Pawlowski 2006; Chernikova et al. 2011; Shih and Matzke 2013) to more than 2300 Ma (Hedges et al. 2004).”
Background
The Genomic and Cellular Foundations of Animal Origins
Richter, D. J., & King, N. (2013) · Annual Review of Genetics · doi:10.1146/annurev-genet-111212-133456 · Cited by 196
Decimetre-scale multicellular eukaryotes from the 1.56-billion-year-old Gaoyuzhuang Formation in North China
Zhu, S., Zhu, M., Knoll, A. H., Yin, Z., Zhao, F., Sun, S., Qu, Y., Shi, M., & Liu, H. (2016) · Nature Communications · doi:10.1038/ncomms11500 · Cited by 199
Combined micro-Fourier transform infrared (FTIR) spectroscopy and micro-Raman spectroscopy of Proterozoic acritarchs: A new approach to Palaeobiology
Marshall, C. P., Javaux, E., Knoll, A. H., & Walter, M. R. (2005) · Precambrian Research · doi:10.1016/j.precamres.2005.05.006 · Cited by 197
Phylogenetic modeling of lateral gene transfer reconstructs the pattern and relative timing of speciations
Szöllősi, G. J., Boussau, B., Abby, S. S., Tannier, É., & Daubin, V. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1202997109 · Cited by 202
Evolutionary mysteries in meiosis
Lenormand, T., Engelstädter, J., Johnston, S. E., Wijnker, T. G., & Haag, C. R. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0001 · Cited by 188
“Meiosis is one of the ‘major innovations’ of eukaryotic life that evolved before their subsequent radiation over one billion years ago [3–5].”
Evolution of nematode-trapping cells of predatory fungi of the Orbiliaceae based on evidence from rRNA-encoding DNA and multiprotein sequences
Yang, Y., Yang, E., An, Z., & Liu, X. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0702770104 · Cited by 192
Evolutionary conservation of early mesoderm specification by mechanotransduction in Bilateria
Brunet, T., Bouclet, A., Ahmadi, P., Mitrossilis, D., Driquez, B., Brunet, A., Henry, L., Serman, F., Béalle, G., Ménager, C., et al. (2013) · Nature Communications · doi:10.1038/ncomms3821 · Cited by 199
Central and storage carbon metabolism of the brown alga Ectocarpus siliculosus : insights into the origin and evolution of storage carbohydrates in Eukaryotes
Michel, G., Tonon, T., Scornet, D., Cock, J. M., & Kloareg, B. (2010) · New Phytologist · doi:10.1111/j.1469-8137.2010.03345.x · Cited by 188
“…clock analyses calibrated by 5 paleontological constraints, Stramenopiles are thought to have diverged from other major 6 eukaryotic groups about 1 billion years ago and it is also thought that the secondary 7 endosymbiosis happened shortly after the primary endosymbiosis (Douzery et al., 2004).”
Background
Dating the Diversification of the Major Lineages of Ascomycota (Fungi)
Prieto, M., & Wedin, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0065576 · Cited by 189
“Most of the existing dating studies provide hypotheses on divergence times for major events in fungal evolution (e.g., the time for the origin of Fungi, Basidiomycota or Ascomycota), but not on the details of the radiation within a major group [26– 27,32,46–47].”
Background
Did an ancient chlamydial endosymbiosis facilitate the establishment of primary plastids?
Huang, J., & Gogarten, J. P. (2007) · Genome biology · doi:10.1186/gb-2007-8-6-r99 · Cited by 189
“Such an insect-to-plant transfer scenario would also push the emergence of insects to before the split of primary photosynthetic eukaryotes, which contradicts all available molecular and fossil evidence [47,48].”
Identification of novel conserved peptide uORF homology groups in Arabidopsis and rice reveals ancient eukaryotic origin of select groups and preferential association with transcription factor-encoding genes
Hayden, C. A., & Jorgensen, R. A. (2007) · BMC Biology · doi:10.1186/1741-7007-5-32 · Cited by 181
“netic relationships among these species [58], the most”
Background
Ecomorphological diversification among South American spiny rats (Rodentia; Echimyidae): a phylogenetic and chronological approach
Galewski, T., Mauffrey, J.-F., Leite, Y. L. R., Patton, J. L., & Douzery, E. (2005) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2004.11.015 · Cited by 182
“This approach has already permitted to highlight unsuspected biogeographical patterns within frogs (Bossuyt and Milinkovitch, 2001) and gave compatible results with the fossil record at various taxonomic levels (Douzery et al., 2004; Hassanin and Douzery, 2003).”
ResultSelf-citation
Phylogenomic Analyses Indicate that Early Fungi Evolved Digesting Cell Walls of Algal Ancestors of Land Plants
Chang, Y., Wang, S., Sekimoto, S., Aerts, A. L., Choi, C., Clum, A., LaButti, K. M., Lindquist, E. A., Ngan, C. Y., Ohm, R. A., et al. (2015) · Genome Biology and Evolution · doi:10.1093/gbe/evv090 · Cited by 185
Cloning and identification of an oxytocin/vasopressin-like receptor and its ligand from insects
Stafflinger, E., Hansen, K. K., Hauser, F., Schneider, M., Cazzamali, G., Williamson, M. P., & Grimmelikhuijzen, C. J. P. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0710897105 · Cited by 180
“A comparison with the mouse vasopressin and oxytocin and the Lymnaea stagnalis (mollusk) conopressin preprohormones shows that these proteins have conserved their structural organizations since the split of Proto- and Deuterostomia, 700 million years ago (18).”
Background
The origin and diversification of eukaryotes: problems with molecular phylogenetics and molecular clock estimation
Roger, A. J., & Hug, L. A. (2006) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2006.1845 · Cited by 180
“However, currently neither phylogenetics, discussed below, nor comparisons of cellular and genomic properties across eukaryotic diversity (see Embley 2006, this volume) provide compelling evidence for an early-branching status of these or any other eukaryote lineages.”
Background
The relative ages of ectomycorrhizal mushrooms and their plant hosts estimated using Bayesian relaxed molecular clock analyses
Hibbett, D. S., & Matheny, P. B. (2009) · BMC Biology · doi:10.1186/1741-7007-7-13 · Cited by 191
“Three other molecular clock studies that analyzed datasets with 37 to 129 genes have estimated the Dikarya to be 727 to 1208 million years old [16-18].”
Independent HHsearch, Needleman-Wunsch-Based, and Motif Analyses Reveal the Overall Hierarchy for Most of the G Protein-Coupled Receptor Families
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14 Agaricomycetes
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“with the most closely related believed to be the 2 kinetoplastids, T. brucei and L. major, which diverged ~250 Mya ( Douzery et al., 2004 ).”
Background
An exceptional horizontal gene transfer in plastids: gene replacement by a distant bacterial paralog and evidence that haptophyte and cryptophyte plastids are sisters
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“This rpl36 transfer and the rbcLS transfer described years ago [16] and revisited above share several features: (i) they both involve bacterial donors; (ii) they are both relatively ancient [56-58], having occurred in the common ancestor of red algae (rbcLS), perhaps 1.”
The Opisthokonta and the Ecdysozoa May Not Be Clades: Stronger Support for the Grouping of Plant and Animal than for Animal and Fungi and Stronger Support for the Coelomata than Ecdysozoa
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“In view of the emergence of winged insects (380-325 Mya [70]), these LTR retroelements most probably emerged simultaneously with those of Retroviridae classes 2 and 3 in amniotes (again consistent with the three kings hypothesis).”
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“In spite of recent criticisms (Blair & Hedges 2005), the maximum age limits used by Douzery et al. (2004) were apparently not too constraining, as the dates inferred in our time-scale are largely congruent with their estimations.”
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Diversity and evolution of marine phytoplankton
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“A secondary endosymbiosis event (0.8–1.2 Gy, [21,22]) with a primitive red algae gave rise to the cryptophytes, haptophytes, photosynthetic stramenopiles (or heterokontophytes) and peridinin-containing dinoflagellates.”
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Hidden levels of phylodiversity in Antarctic green algae: further evidence for the existence of glacial refugia
Wever, A. D., Leliaert, F., Verleyen, E., Vanormelingen, P., der Gucht, K. V., Hodgson, D. A., Sabbe, K., & Vyverman, W. (2009) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2009.0994 · Cited by 151
“Owing to the lack of reliable green algal fossils, our phylogenetic tree is only calibrated at a single node, using a minimum and maximum age of the Chlorophyta– Streptophyta split at 700 and 1500 Ma, respectively (Douzery et al. 2004; Hedges et al. 2004; Yoon et al. 2004; Berney & Pawlowski 2006; Cavalier-Smith 2006;…”
Method

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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