Explaining Darwin’s Corollary to Haldane’s Rule: The Role of Mitonuclear Interactions in Asymmetric Postzygotic Isolation Among Toads

Abstract

We examine the basis of Darwin's corollary to Haldane's rule, which describes viability and fertility differences between F 1 produced from reciprocal crosses. We analyzed asymmetries in hybrid viability from .100 reciprocal crosses involving 36 toad species to test whether relatively high rates of mitochondrial vs. nuclear evolution produce dams with systematically less viable F 1 hybrid progeny. We find no such effect, suggesting a predominant role for stochastic accumulation of asymmetric epistatic incompatibilities.A S Darwin (1859, Chap. 8) noted, interspecific reciprocal crosses often differ in whether fertilization occurs and in the viability and fecundity of F 1 hybrids. Even under optimal laboratory conditions, reciprocal F 1 s often show viability or fecundity differences. This pattern of asymmetric intrinsic postzygotic isolation has been dubbed "Darwin's corollary to Haldane's rule" (Turelli and Moyle 2007). While asymmetric fertilization success can be produced under autosomal genetic control, Darwin's corollary requires deleterious epistatic interactions (i.e., Dobzhansky-Muller incompatibilities, DMIs) involving uniparentally inherited factors such as mitochondria, sex chromosomes, epigenetic programming, or maternal effects (Turelli and Moyle 2007), because only uniparentally inherited factors will differentially affect F 1 produced from reciprocal crosses.Turelli and Moyle (2007) contrasted deterministic vs. stochastic explanations for Darwin's corollary, depending on whether the cross that produces less fit hybrids is predictable from relative rates of evolution for uniparentally vs. biparentally inherited factors. Differences in the relative rates of evolution can lead to different expected fitnesses from reciprocal crosses. Consider the species pair A-B. If the proportion of mitochondrial to nuclear substitutions in lineage A exceeds that in lineage B, we expect more mitonuclear DMIs in AB F 1 hybrids with A mothers vs. BA hybrids with B mothers, simply because there are more potential incompatibilities in the AB cross than in the BA cross. Thus, if mitonuclear DMIs contribute significantly to lowered interpopulation (Burton et al. 2006;Ellison and Burton 2008;Montooth et al. 2010; Meiklejohn et al. 2013) or interspecific (e.g., Fishman andWillis 2006;Lee et al. 2008; Rieseberg and Blackman 2010) fitness, as often argued (e.g., Rand et al. 2004;Gershoni et al. 2009;Lane 2011;Burton and Barreto 2012), directional asymmetry may be predictable from relative rates of mitochondrial vs. nuclear evolution. Turelli and Moyle (2007) conjectured that the deterministic signal associated with directional effects produced by a particular class of DMIs (e.g., mitonuclear incompatibilities) was likely to be overwhelmed by both stochastic effects and other classes of asymmetric incompatibilities. The theoretical analyses pioneered by Orr (1993) describe the accumulation of DMIs as rare--independent and inherently stochastic--events associated with molecular differences between diverging taxa. Diff...

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