How does the mode of evolutionary divergence affect reproductive isolation?

When divergent populations interbreed, the outcome will be affected by the genomic and phenotypic differences that they have accumulated. In this way, the mode of evolutionary divergence between populations may have predictable consequences for the fitness of their hybrids, and so for the progress of speciation. To investigate these connections, we present a new analysis of hybridization under Fisher’s geometric model, making few assumptions about the allelic effects that differentiate the hybridizing populations. Results show that the strength and form of postzygotic reproductive isolation (RI) depend on just two properties of the evolutionary changes, which we call the “total amount” and “net effect” of change, and whose difference quantifies the similarity of the changes at different loci, or their tendency to act in the same phenotypic direction. It follows from our results that identical patterns of RI can arise in different ways, since different evolutionary histories can lead to the same total amount and net effect of change. Nevertheless, we show how these estimable quantities do contain some information about the history of divergence, and that – thanks to Haldane’s Sieve – the dominance and additive effects contain complementary information. Impact Summary When populations of animals or plants evolve differences in their genomes or traits, the nature of the differences will help to determine whether they can continue to interbreed. For example, the hybrid offspring may be infertile, or unlikely to survive to reproductive age, meaning that the two populations remain distinct from one another even after mating. However, in some cases the hybrids may be more fertile than their parents or have some other reproductive advantage. In this study, we use a mathematical model to relate hybrid fitness to the evolved differences separating the parents. We find that the outcome depends on just two properties of these differences, which capture the “total amount” and the “net effect” of evolutionary change. We then show that different evolutionary divergence scenarios or modes can lead to the exact same hybrid fitness. On the other hand, we can still make some inferences about the history of divergence by observing certain properties of hybrid fitness. Determining the relationship between hybrid fitness and the mode of evolutionary divergence will help to understand how new species form, to plan conservation interventions such as moving individuals between isolated populations to increase their adaptive potential, and to understand how existing species might interact when their habitats overlap, for example due to climate change or other human impacts.