Genetic hitchhiking and the dynamic buildup of genomic divergence during speciation with gene flow.

A major issue in evolutionary biology is explaining patterns of differentiation observed in population genomic data, as divergence can be due to both direct selection on a locus and genetic hitchhiking. "Divergence hitchhiking" (DH) theory postulates that divergent selection on a locus reduces gene flow at physically linked sites, facilitating the formation of localized clusters of tightly linked, diverged loci. "Genome hitchhiking" (GH) theory emphasizes genome-wide effects of divergent selection. Past theoretical investigations of DH and GH focused on static snapshots of divergence. Here, we used simulations assessing a variety of strengths of selection, migration rates, population sizes, and mutation rates to investigate the relative importance of direct selection, GH, and DH in facilitating the dynamic buildup of genomic divergence as speciation proceeds through time. When divergently selected mutations were limiting, GH promoted divergence, but DH had little measurable effect. When populations were small and divergently selected mutations were common, DH enhanced the accumulation of weakly selected mutations, but this contributed little to reproductive isolation. In general, GH promoted reproductive isolation by reducing effective migration rates below that due to direct selection alone, and was important for genome-wide "congealing" or "coupling" of differentiation (F(ST)) across loci as speciation progressed.
(© 2013 The Author(s). Evolution © 2013 The Society for the Study of Evolution.)