*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;
Edited by Wen-Hsiung Li, University of Chicago, Chicago, IL, and approved September 13, 2004 (received for review June 7, 2004) 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
Evolution
The timing of eukaryotic evolution: Does a relaxed molecular clock reconcile proteins and fossils?
,
,
, 
¶
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
100 million years more ancient than the Cambrian boundary.
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.
To whom correspondence may be addressed.
www.pnas.org/cgi/doi/10.1073/pnas.0403984101
![]()
CiteULike
Complore
Connotea
Del.icio.us
Digg What's this?
This article has been cited by other articles in HighWire Press-hosted journals:
![]() |
V. Krauss, C. Thummler, F. Georgi, J. Lehmann, P. F. Stadler, and C. Eisenhardt Near Intron Positions Are Reliable Phylogenetic Markers: An Application to Holometabolous Insects Mol. Biol. Evol., May 1, 2008; 25(5): 821 - 830. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Stafflinger, K. K. Hansen, F. Hauser, M. Schneider, G. Cazzamali, M. Williamson, and C. J. P. Grimmelikhuijzen Cloning and identification of an oxytocin/vasopressin-like receptor and its ligand from insects PNAS, March 4, 2008; 105(9): 3262 - 3267. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. Lepage, D. Bryant, H. Philippe, and N. Lartillot A General Comparison of Relaxed Molecular Clock Models Mol. Biol. Evol., December 1, 2007; 24(12): 2669 - 2680. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. E. Pimanda, K. Ottersbach, K. Knezevic, S. Kinston, W. Y. I. Chan, N. K. Wilson, J.-R. Landry, A. D. Wood, A. Kolb-Kokocinski, A. R. Green, et al. Gata2, Fli1, and Scl form a recursively wired gene-regulatory circuit during early hematopoietic development PNAS, November 6, 2007; 104(45): 17692 - 17697. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. C. Slot, K. N. Hallstrom, P. B. Matheny, and D. S. Hibbett Diversification of NRT2 and the Origin of Its Fungal Homolog Mol. Biol. Evol., August 1, 2007; 24(8): 1731 - 1743. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. A. Hug and A. J. Roger The Impact of Fossils and Taxon Sampling on Ancient Molecular Dating Analyses Mol. Biol. Evol., August 1, 2007; 24(8): 1889 - 1897. [Abstract] [Full Text] [PDF] |
||||
![]() |
N. H. Putnam, M. Srivastava, U. Hellsten, B. Dirks, J. Chapman, A. Salamov, A. Terry, H. Shapiro, E. Lindquist, V. V. Kapitonov, et al. Sea Anemone Genome Reveals Ancestral Eumetazoan Gene Repertoire and Genomic Organization Science, July 6, 2007; 317(5834): 86 - 94. [Abstract] [Full Text] [PDF] |
||||
![]() |
W. Iwasaki and T. Takagi Reconstruction of highly heterogeneous gene-content evolution across the three domains of life Bioinformatics, July 1, 2007; 23(13): i230 - i239. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Bengtson, B. Rasmussen, and B. Krapez The Paleoproterozoic megascopic Stirling biota Paleobiology, June 1, 2007; 33(3): 351 - 381. [Abstract] [Full Text] [PDF] |
||||
![]() |
Y. Yang, E. Yang, Z. An, and X. Liu Evolution of nematode-trapping cells of predatory fungi of the Orbiliaceae based on evidence from rRNA-encoding DNA and multiprotein sequences PNAS, May 15, 2007; 104(20): 8379 - 8384. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. D. Nguyen, M. Yoshihama, and N. Kenmochi The Evolution of Spliceosomal Introns in Alveolates Mol. Biol. Evol., May 1, 2007; 24(5): 1093 - 1096. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. N. Khachane, K. N. Timmis, and V. A. P. Martins dos Santos Dynamics of Reductive Genome Evolution in Mitochondria and Obligate Intracellular Microbes Mol. Biol. Evol., February 1, 2007; 24(2): 449 - 456. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. E. Baker Evolution of metamorphosis: role of environment on expression of mutant nuclear receptors and other signal-transduction proteins Integr. Comp. Biol., December 1, 2006; 46(6): 808 - 814. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. L. Dupont, S. Yang, B. Palenik, and P. E. Bourne Modern proteomes contain putative imprints of ancient shifts in trace metal geochemistry PNAS, November 21, 2006; 103(47): 17822 - 17827. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. W. Taylor and M. L. Berbee Dating divergences in the Fungal Tree of Life: review and new analyses Mycologia, November 1, 2006; 98(6): 838 - 849. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. Grasberger and S. Refetoff Identification of the Maturation Factor for Dual Oxidase: EVOLUTION OF AN EUKARYOTIC OPERON EQUIVALENT J. Biol. Chem., July 7, 2006; 281(27): 18269 - 18272. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Freeling and B. C. Thomas Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity Genome Res., July 1, 2006; 16(7): 805 - 814. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. Gadelha, B. Wickstead, P. G. McKean, and K. Gull Basal body and flagellum mutants reveal a rotational constraint of the central pair microtubules in the axonemes of trypanosomes J. Cell Sci., June 15, 2006; 119(12): 2405 - 2413. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Petersen, R. Teich, B. Becker, R. Cerff, and H. Brinkmann The GapA/B Gene Duplication Marks the Origin of Streptophyta (Charophytes and Land Plants) Mol. Biol. Evol., June 1, 2006; 23(6): 1109 - 1118. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. E. Stajich and F. S. Dietrich Evidence of mRNA-Mediated Intron Loss in the Human-Pathogenic Fungus Cryptococcus neoformans Eukaryot. Cell, May 1, 2006; 5(5): 789 - 793. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. Wickstead and K. Gull A "Holistic" Kinesin Phylogeny Reveals New Kinesin Families and Predicts Protein Functions Mol. Biol. Cell, April 1, 2006; 17(4): 1734 - 1743. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. P. M. Weber, M. Linka, and D. Bhattacharya Single, Ancient Origin of a Plastid Metabolite Translocator Family in Plantae from an Endomembrane-Derived Ancestor Eukaryot. Cell, March 1, 2006; 5(3): 609 - 612. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. H. Davidson and D. H. Erwin Gene Regulatory Networks and the Evolution of Animal Body Plans Science, February 10, 2006; 311(5762): 796 - 800. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Rokas, D. Kruger, and S. B. Carroll Animal Evolution and the Molecular Signature of Radiations Compressed in Time Science, December 23, 2005; 310(5756): 1933 - 1938. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. E. Blair and S. B. Hedges Molecular Phylogeny and Divergence Times of Deuterostome Animals Mol. Biol. Evol., November 1, 2005; 22(11): 2275 - 2284. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Saranak and K. W. Foster Photoreceptor for Curling Behavior in Peranema trichophorum and Evolution of Eukaryotic Rhodopsins Eukaryot. Cell, October 1, 2005; 4(10): 1605 - 1612. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. Martinelli and J.-M. Reichhart Evolution and integration of innate immune systems from fruit flies to man: lessons and questions Innate Immunity, August 1, 2005; 11(4): 243 - 248. [Abstract] [PDF] |
||||
![]() |
N. M. El-Sayed, P. J. Myler, G. Blandin, M. Berriman, J. Crabtree, G. Aggarwal, E. Caler, H. Renauld, E. A. Worthey, C. Hertz-Fowler, et al. Comparative Genomics of Trypanosomatid Parasitic Protozoa Science, July 15, 2005; 309(5733): 404 - 409. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. J. Peterson and N. J. Butterfield From The Cover: Origin of the Eumetazoa: Testing ecological predictions of molecular clocks against the Proterozoic fossil record PNAS, July 5, 2005; 102(27): 9547 - 9552. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. Philippe, N. Lartillot, and H. Brinkmann Multigene Analyses of Bilaterian Animals Corroborate the Monophyly of Ecdysozoa, Lophotrochozoa, and Protostomia Mol. Biol. Evol., May 1, 2005; 22(5): 1246 - 1253. [Abstract] [Full Text] [PDF] |
||||
![]() |
G. K. Philip, C. J. Creevey, and J. O. McInerney 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 Mol. Biol. Evol., May 1, 2005; 22(5): 1175 - 1184. [Abstract] [Full Text] [PDF] |
||||