Genetic drift promotes and recombination hinders speciation on holey fitness landscapes

Abstract

Dobzhansky and Muller proposed a general mechanism through which microevolution, the substitution of alleles within populations, can cause the evolution of reproductive isolation between populations and, therefore, macroevolution. As allopatric populations diverge, many combinations of alleles differing between them have not been tested by natural selection and may thus be incompatible. Such genetic incompatibilities often cause low fitness in hybrids between species. Furthermore, the number of incompatibilities grows with the genetic distance between diverging populations. However, what determines the rate and pattern of accumulation of incompatibilities remains unclear. We investigate this question by simulating evolution on holey fitness landscapes on which genetic incompatibilities can be identified unambiguously. We find that genetic incompatibilities accumulate more slowly among genetically robust populations and identify two determinants of the accumulation rate: recombination rate and population size. In large populations with abundant genetic variation, recombination selects for increased genetic robustness and, consequently, incompatibilities accumulate more slowly. In small populations, genetic drift interferes with this process and promotes the accumulation of genetic incompatibilities. Our results suggest a novel mechanism by which genetic drift promotes and recombination hinders speciation. Author summaryAs geographically isolated populations evolve, genetic incompatibilities accumulate between them. Eventually, these incompatibilities may cause the populations to become different species. What determines how quickly species are formed in this way remains unclear. We investigate this question using computer simulations and find that genetic incompatibilities accumulate more slowly among populations with individuals that are robust to genetic perturbations. We identify two factors that influence the accumulation rate via their effects on genetic robustness: the size of the populations and how much recombination takes place in them. Small populations with rare recombination accumulate incompatibilities more quickly.