Sperm competition promotes asymmetries in reproductive barriers between closely related species

Reproductive barriers between closely related species are often incomplete and asymmetric, but the evolutionary significance of these well-known phenomena remains unsolved. We test the hypothesis that the degree of gametic incompatibility in reciprocal crosses is associated to levels of sperm competition because this selective force favors both increased sperm competitiveness and ovum defensiveness. Using three species of Mus with high, intermediate, and low levels of sperm competition, we examined fertilization rates in competitive and noncompetitive contexts. We found that the influence of sperm competition upon sperm competitiveness is as strong as it is upon ovum defensiveness, revealing an effect upon female gametes so far overlooked. As a result, fertilization success was strongly related to differences in sperm competition levels between species providing sperm and ova, thus generating major asymmetries in reciprocal crosses. When placed in competition, conspecific sperm maintained levels of fertilization success similar to those found in noncompetitive contexts, at the expense of the success of heterospecific sperm. When only heterospecific sperm competed, species with highest levels of sperm competition outcompeted others and asymmetries were exacerbated. We conclude that sperm competition explains both the degree of gametic isolation and the degree of asymmetries between closely related species.