Reinforcement and selection against migrants maintain sperm competitive and genetic differences among populations of Drosophila pseudoobscura

Sexual interactions among closely related species can select for divergence in reproductive traits as a mechanism to avoid the costs of hybridization. This selection, termed ‘reinforcement’, produces a canonical pattern of stronger isolation in populations that are sympatric with congeners, versus in allopatric populations. While reinforcement has been observed in many systems, the resulting pattern might be transient. There must be selection against migrants between allopatry and sympatry—akin to local reproductive adaptation—for a pattern of stronger sympatric isolation to be maintained. We tested for evidence of this selection against migrants in the context of sperm competition, in Drosophila pseudoobscura . Previously we showed an advantage of sympatric genotypes in sympatric contexts, via their elevated reproductive isolation (conspecific sperm precedence) against congeneric D. persimilis . Here, using experimental crosses that simulated migration between populations that are naturally sympatric and allopatric with D. persimilis, we show that sympatric genotypes are at a sperm-competitive disadvantage against allopatric male genotypes. This selection against sympatric males in allopatry, combined with the advantage of sympatric genotypes in sympatry, produce a scenario for strong selection against migrants between these two geographic contexts. This is accompanied by population differentiation in reproductive gene expression and allele frequency variation between allopatry and sympatry, including genes with known roles in sperm competition. While some of these changes are parallel among sympatric or allopatric contexts, most are unique to individual populations and might reflect the unique ways that selection has acted on sperm competition genes in different sympatric populations.