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MBE Advance Access published online on June 14, 2006

Molecular Biology and Evolution, doi:10.1093/molbev/msl038
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© The Author 2006. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org
Accepted June 1, 2006

Research Article

A Mitogenomics Timescale for Birds Detects Variable Phylogenetic Rates of Molecular Evolution and Refutes the Standard Molecular Clock

Sergio L. Pereira 1 * and Allan J. Baker 2

1 Department of Natural History, Royal Ontario Museum, 100 Queen's Park Crescent, Toronto, ON, Canada, M5S 2C6
2 Department of Natural History, Royal Ontario Museum, 100 Queen's Park Crescent, Toronto, ON, Canada, M5S 2C6; Department of Zoology, University of Toronto, Toronto, ON, Canada, M5S 1A1

* To whom correspondence should be addressed.
Sergio L. Pereira, E-mail: sergio.pereira{at}utoronto.ca


   Abstract

Current understanding of the diversification of birds is hindered by their incomplete fossil record, and uncertainty in phylogenetic relationships and phylogenetic rates of molecular evolution. Here we performed the first comprehensive analysis of mitogenomic data of 48 vertebrates, including 35 birds, to derive a Bayesian timescale for avian evolution and to estimate rates of DNA evolution. Our approach used multiple fossil time constraints scattered throughout the phylogenetic tree and accounts for uncertainties in time constraints, branch lengths and heterogeneity of rates of DNA evolution. We estimated that the major vertebrate lineages originated in the Permian; the 95% credible intervals of our estimated ages of the origin of archosaurs (258 Mya), the amniote-amphibian split (356 Mya), and the archosaur-lizard divergence (278 Mya) bracket estimates from the fossil record. The origin of modern orders of birds was estimated to have occurred throughout the Cretaceous beginning about 139 Mya, arguing against a cataclysmic extinction of lineages at the K-T boundary. We identified fossils that are useful as time constraints within vertebrates. Our timescale reveals that rates of molecular evolution vary across genes and among taxa through time, thereby refuting the widely used mitogenomic or cytochrome b molecular clock in birds. Moreover, the 5 million years (Myr) divergence time assumed between two genera of geese (Branta and Anser) to originally calibrate the standard mitochondrial clock rate of 0.01 substitutions/site/lineage/Myr in birds was shown to be underestimated by about 9.5 Myr. Phylogenetic rates in birds vary between 0.0009 and 0.012 substitution/site/lineage/myr, indicating that many phylogenetic splits among avian taxa also have been underestimated and need to be revised. We found no support for the hypothesis that the molecular clock in birds "ticks" according to a constant rate of substitution per unit of mass-specific metabolic energy rather than per unit of time, as recently suggested. Our analysis advances knowledge of rates of DNA evolution across birds and other vertebrates, and will therefore aid comparative biology studies that seek to infer the origin and timing of major adaptive shifts in vertebrates.

Keywords: divergence times; Aves; vertebrates; fossil; rate of DNA evolution; molecular clock.
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