Genetics. Published Articles Ahead of Print: February 1, 2008, Copyright © 2008
doi:10.1534/genetics.107.081364


A more recent version of this article appeared on February 1, 2008.


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Accelerated mitochondrial evolution and "Darwin's corollary": Asymmetric viability of reciprocal F1 hybrids in centrarchid fishes

1 University of Texas at Austin
2 University of California
3 Texas A&M University
4 University of California at Davis
5 Yale University

* To whom correspondence should be addressed. E-mail: danbolnick{at}mail.utexas.edu.

Submitted on August 29, 2007
Revised on October 26, 2007
Accepted on 26 November 2007


Abstract

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, though 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.

Key Words: Dobzhansky-Muller incompatibilities, mitochondria, reproductive isolation, speciation, sunfish




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