The evolution of hybrid fitness during speciation

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.Author summary: As populations diverge and ultimately evolve into distinct species, hybrids between them gradually become inviable and infertile. Before this happens, there can be a brief period in which hybrids are actually 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. Simulations of the model, using state-of-the-art experimental data on gene interactions, show evolutionary trajectories that mirror patterns seen in nature. The model suggests how the process by which populations diverge affects the rate of speciation.