Originally published as Genetics Published Articles Ahead of Print on February 1, 2008.

Genetics, Vol. 178, 1037-1048, February 2008, Copyright © 2008
doi:10.1534/genetics.107.081364

Accelerated Mitochondrial Evolution and "Darwin's Corollary": Asymmetric Viability of Reciprocal F₁ Hybrids in Centrarchid Fishes

Daniel I. Bolnick^*,1, Michael Turelli, Hernán López-Fernández, Peter C. Wainwright and Thomas J. Near

^* Section of Integrative Biology, University of Texas, Austin, Texas 78712, Section of Evolution and Ecology, University of California, Davis, California 95616, Department of Wildlife and Fisheries Sciences, Texas A&M University, College Station, Texas 77843-2258 and Department of Ecology and Evolution and Peabody Museum of Natural History, Yale University, New Haven, Connecticut 06520

¹ Corresponding author: Section of Integrative Biology, One University Station C0930, University of Texas, Austin, TX 78712.
E-mail: danbolnick{at}mail.utexas.edu

Reciprocal crosses between species can yield hybrids with different viabilities. The high frequency of this asymmetric hybrid viability ("Darwin's corollary") places it alongside Haldane's rule and the "large-X effect" as a general feature of postmating reproductive isolation. Recent theory suggests that reciprocal cross asymmetries can arise from stochastic substitutions in uniparentally inherited loci such as mitochondrial genomes, although large systematic differences in mitochondrial substitution rates can also contribute to asymmetries. Although the magnitude of asymmetry will be relatively insensitive to unequal rates of mitochondrial evolution in diverging species, we show here that rate asymmetries can have a large effect on the direction of viability asymmetries. In reciprocal crosses between species, the maternal parent with faster mitochondrial evolution will tend to produce less viable F₁ hybrids owing to an increased probability of mito-nuclear incompatibilities. We test this prediction using data on reciprocal hybrid viability and molecular evolution rates from a clade of freshwater fishes, Centrarchidae. As predicted, species with accelerated mitochondrial evolution tend to be the worse maternal parent for F₁ hybrids, providing the first comparative evidence for a systematic basis to Darwin's corollary. This result is consistent with the hypothesis that mito-nuclear incompatibilities can play an important role in reproductive isolation. Such asymmetrical reproductive isolation may help explain the asymmetrical mitochondrial introgression observed between many hybridizing species. However, as with any comparative study, we cannot rule out the possibility that our results arise from a mutual correlation with a third variable such as body size.

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