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

  1. Emmanuel J. P. Douzery*,,
  2. Elizabeth A. Snell,
  3. Eric Bapteste§,
  4. Frédéric Delsuc*,, and
  5. Hervé Philippe,§,
  1. *Departments of Paleontology, Phylogeny, and Paleobiology, CC064, Institut des Sciences de l'Evolution (Unité Mixte de Recherche 5554, Centre National de la Recherche Scientifique), Université Montpellier II, Place E. Bataillon, 34 095 Montpellier Cedex 5, France; School of Animal and Microbial Sciences, University of Reading, Whiteknights, P.O. Box 228, Reading RG6 6AJ, United Kingdom; §Departments of Phylogeny, Bioinformatics, and Genomics, Unité Mixte de Recherche 7622, Centre National de la Recherche Scientifique, Université Pierre et Marie Curie, 9 Quai St. Bernard, Bâtiment C, 75005 Paris, France; and Canadian Institute for Advanced Research. Département de Biochimie, Université de Montréal, Succursale Centre-Ville, Montréal, QC, Canada H3C 3J7
  1. Edited by Wen-Hsiung Li, University of Chicago, Chicago, IL (received for review June 7, 2004)

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.

Footnotes

  • To whom correspondence may be addressed. E-mail: douzery{at}isem.univ-montp2.fr or herve.philippe{at}umontreal.ca.

  • Author contributions: E.J.P.D. and H.P. designed research; E.J.P.D. and H.P. performed research; E.A.S. and E.B. contributed new reagents/analytic tools; E.J.P.D., F.D., and H.P. analyzed data; E.J.P.D., F.D., and H.P. wrote the paper.

  • This paper was submitted directly (Track II) to the PNAS office.

  • Abbreviations: Mya, million years ago; Myr, million years; MCMC, Markov chain Monte Carlo.

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