Emergent Speciation by Multiple Dobzhansky–Muller Incompatibilities

Abstract The Dobzhansky–Muller model posits that incompatibilities between alleles at different loci cause speciation. However, it is known that if the alleles involved in a Dobzhansky–Muller incompatibility (DMI) between two loci are neutral, the resulting reproductive isolation cannot be maintained in the presence of either mutation or gene flow. Here we show that speciation can emerge through the collective effects of multiple neutral DMIs that cannot, individually, cause speciation—a mechanism we call emergent speciation. We investigate emergent speciation using models of haploid holey adaptive landscapes—neutral networks—with recombination. We find that certain combinations of multiple neutral DMIs can lead to speciation. Furthermore, emergent speciation is a robust mechanism that can occur in the presence of migration, and of deviations from the assumptions of the neutral network model. Strong recombination and complex interactions between the DMI loci facilitate emergent speciation. These conditions are likely to occur in nature. We conclude that the interaction between DMIs may cause speciation. Author Summary Most species are kept distinct by incompatibilities between the genes they carry. These genetic incompatibilities cause hybrids between the species to have low fitness. Here we propose that combinations of several incompatibilities can collectively cause the origin of species, although they cannot do so acting alone—a mechanism we call emergent speciation. We use flat fitness landscapes with many holes in them to extend the classic Dobzhansky–Muller model, and capture the essence of the phenomenon. We find that emergent speciation can, indeed, occur through the combined effects of multiple genetic incompatibilities. Furthermore, the conditions that facilitate emergent speciation are likely to occur in nature. We conclude that the interaction between genetic incompatibilities may be a root cause of the origin of species.