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MBE Advance Access originally published online on November 12, 2007
Molecular Biology and Evolution 2008 25(1):120-130; 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 Articles

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, Centre National de la Recherche Scientifique—Université Montpellier 2, Montpellier, France

E-mail: bnabholz{at}univ-montp2.fr.

Accepted for publication October 24, 2007.

Mitochondrial DNA (mtDNA) 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 mtDNA 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 nonsynonymous substitutions, we measure the lineage-specific mitochondrial mutation rate across 1,696 mammalian species and compare it with the nuclear rate. We report an unexpected 2 orders of magnitude mitochondrial mutation rate variation between lineages: cytochrome b third codon positions are renewed every 1–2 Myr, in average, in the fastest evolving mammals, whereas it takes >100 Myr 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 aging.

Key Words: mutation rate • mitochondrial DNA • theory of aging • mammals

Ziheng Yang, Associate Editor


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