Estimating the timing of early eukaryotic diversification with multigene molecular clocks

Contributed by Andrew H. Knoll, July 1, 2011 (sent for review February 9, 2011)
August 2, 2011
108 (33) 13624-13629

Abstract

Although macroscopic plants, animals, and fungi are the most familiar eukaryotes, the bulk of eukaryotic diversity is microbial. Elucidating the timing of diversification among the more than 70 lineages is key to understanding the evolution of eukaryotes. Here, we use taxon-rich multigene data combined with diverse fossils and a relaxed molecular clock framework to estimate the timing of the last common ancestor of extant eukaryotes and the divergence of major clades. Overall, these analyses suggest that the last common ancestor lived between 1866 and 1679 Ma, consistent with the earliest microfossils interpreted with confidence as eukaryotic. During this interval, the Earth's surface differed markedly from today; for example, the oceans were incompletely ventilated, with ferruginous and, after about 1800 Ma, sulfidic water masses commonly lying beneath moderately oxygenated surface waters. Our time estimates also indicate that the major clades of eukaryotes diverged before 1000 Ma, with most or all probably diverging before 1200 Ma. Fossils, however, suggest that diversity within major extant clades expanded later, beginning about 800 Ma, when the oceans began their transition to a more modern chemical state. In combination, paleontological and molecular approaches indicate that long stems preceded diversification in the major eukaryotic lineages.

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Acknowledgments

We thank Ben Normark, Rob Dorit, and Sam Bowser for useful discussions, and Jeff Thorne and Bengt Sennblad for helpful discussions about molecular clock models. This manuscript has been improved following the comments of Emmanuelle Javaux, Andrew Roger, and Heroen Verbruggen. We thank Jessica Grant and Tony Caldanaro for technical help. This research was supported by the National Aeronautics and Space Administration Astrobiology Institute (A.H.K.) and by National Science Foundation Assembling the Tree of Life Grant 043115 and National Science Foundation Systematics Grant 0919152 (to L.A.K). D.J.G.L. is supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico-Brazil Doutorado no Exterior Fellowship 200853/2007-4.

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Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 108 | No. 33
August 16, 2011
PubMed: 21810989

Classifications

Submission history

Published online: August 2, 2011
Published in issue: August 16, 2011

Keywords

  1. microbial eukaryotes
  2. Proterozoic oceans
  3. taxon sampling
  4. origin of eukaryotes

Acknowledgments

We thank Ben Normark, Rob Dorit, and Sam Bowser for useful discussions, and Jeff Thorne and Bengt Sennblad for helpful discussions about molecular clock models. This manuscript has been improved following the comments of Emmanuelle Javaux, Andrew Roger, and Heroen Verbruggen. We thank Jessica Grant and Tony Caldanaro for technical help. This research was supported by the National Aeronautics and Space Administration Astrobiology Institute (A.H.K.) and by National Science Foundation Assembling the Tree of Life Grant 043115 and National Science Foundation Systematics Grant 0919152 (to L.A.K). D.J.G.L. is supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico-Brazil Doutorado no Exterior Fellowship 200853/2007-4.

Authors

Affiliations

Laura Wegener Parfrey
Program in Organismic and Evolutionary Biology, University of Massachusetts, Amherst, MA 01003;
Department of Biological Sciences, Smith College, Northampton, MA 01063; and
Present address: Department of Chemistry and Biochemistry, University of Colorado, Boulder, CO 80309.
Daniel J. G. Lahr
Program in Organismic and Evolutionary Biology, University of Massachusetts, Amherst, MA 01003;
Department of Biological Sciences, Smith College, Northampton, MA 01063; and
Andrew H. Knoll1 [email protected]
Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138
Laura A. Katz1 [email protected]
Program in Organismic and Evolutionary Biology, University of Massachusetts, Amherst, MA 01003;
Department of Biological Sciences, Smith College, Northampton, MA 01063; and

Notes

1
To whom correspondence may be addressed. E-mail: [email protected] or [email protected]
Author contributions: L.W.P. and L.A.K. designed research; L.W.P. and D.J.G.L. performed research; L.W.P., D.J.G.L., A.H.K., and L.A.K. analyzed data; and L.W.P., D.J.G.L., A.H.K., and L.A.K. wrote the paper.

Competing Interests

The authors declare no conflict of interest.

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    Estimating the timing of early eukaryotic diversification with multigene molecular clocks
    Proceedings of the National Academy of Sciences
    • Vol. 108
    • No. 33
    • pp. 13359-13878

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