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MBE Advance Access published online on November 12, 2007
Molecular Biology and Evolution, doi:10.1093/molbev/msm248
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© The Author 2007. 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

Research Article

Strong Variations of Mitochondrial Mutation Rate across Mammals – the Longevity Hypothesis

Benoit Nabholz*, Sylvain Glémin and Nicolas Galtier

Institut des Sciences de l'Evolution – CC64, CNRS – Université Montpellier 2, 34095 Montpellier Cedex 5, France, phone: (+33) 467 14 48 18, fax: (+33) 467 14 46 10, bnabholz{at}univ-montp2.fr

* corresponding author

Received for publication July 6, 2007. Revision received October 15, 2007. Accepted for publication October 24, 2007.

Mitochondrial DNA is the most popular marker of molecular diversity in animals, primarily because of its elevated mutation rate. After >20 years of intensive usage, the extent of mitochondrial evolutionary rate variations across species, their practical consequences on sequence analysis methods, and the ultimate reasons for mitochondrial DNA hypermutability are still largely unresolved issues. Using an extensive cytochrome b data set, fossil data, and taking advantage of the decoupled dynamics of synonymous and non-synonymous substitutions, we measure the lineage-specific mitochondrial mutation rate across 1696 mammalian species, and compare it to the nuclear rate. We report an unexpected two-orders of magnitude mitochondrial mutation rate variation between lineages: cytochrome b third-codon positions are renewed every 1-2 million year, in average, in the fastest evolving mammals, while it takes >100 million years in slow-evolving lineages. This result has obvious implications in the fields of molecular phylogeny, molecular dating and population genetics. Variations of mitochondrial substitution rate across species are partly explained by body mass, longevity, and age of female sexual maturity. The classical metabolic rate and generation time hypothesis, however, do not fully explain the observed patterns, especially a stronger effect of longevity in long-lived than in short-lived species. We propose that natural selection tends to decrease the mitochondrial mutation rate in long-lived species, in agreement with the mitochondrial theory of ageing.

Key Words: Mutation rate • mitochondrial DNA • theory of ageing • mammals


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