Abstract
The evolution of postzygotic reproductive isolation is an important component of speciation. But before isolation is complete there is sometimes a phase of heterosis in which hybrid fitness exceeds that of the two parental species. The genetics and evolution of heterosis and postzygotic isolation have typically been studied in isolation, precluding the development of a unified theory of speciation. Here, we develop a model that incorporates both positive and negative gene interactions, and accounts for the evolution of both heterosis and postzygotic isolation. We parameterize the model with recent data on the fitness effects of 10,000 mutations in yeast, singly and in pairwise epistatic combinations. The model makes novel predictions about the types of interactions that contribute to declining hybrid fitness. We reproduce patterns familiar from earlier models of speciation (e.g. Haldane’s Rule and Darwin’s Corollary) and identify new mechanisms that may underlie these patterns. Our approach provides a general framework for integrating experimental data from gene interaction networks into speciation theory and makes new predictions about the genetic mechanisms of speciation.
Highlights
There can be a brief period in which hybrids are more fit than their parents, a condition called heterosis or hybrid vigor
This paper describes a model of how hybrid fitness changes as two populations diverge that can explain both hybrid vigor and hybrid inviability in a single framework
These results show that interactions between alleles within a population can often be more important to hybrid fitness than new interactions first seen in hybrids
Summary
Mathematical models of DMIs [16, 17] have generated testable predictions about the evolution of hybrid inviability [16, 18], the asymmetric inviability of reciprocal crosses [19], and sex differences in hybrid fitness [20] (reviewed in [21]) These predictions have generally been supported by empirical studies [2], the majority of these models share four limitations. Substitutions are typically assumed to occur randomly through time, with no explicit consideration of the roles played by selection and drift How these mutations become fixed could have important consequences for how they affect hybrid fitness. We develop a more general model that relaxes all four assumptions
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