Rapid divergence of the male reproductive proteins in theDrosophila dunnigroup and implications for postmating incompatibilities between species

Proteins involved in post-copulatory interactions between males and females are among the fastest evolving genes in many species, usually attributed to their involvement in reproductive conflict. As a result, these proteins are thought to often be involved in the formation of postmating-prezygotic incompatibilities between species. The Drosophila dunni subgroup consists of a dozen recently diverged species found across the Caribbean islands with varying levels of hybrid incompatibility. We performed experimental crosses between species in the dunni group and see some evidence of hybrid incompatibilities. We also find evidence of reduced survival following hybrid mating, likely due to postmating-prezygotic incompatibilities. We assessed rates of evolution between these species genomes and find evidence of rapid evolution and divergence of some reproductive proteins, specifically the seminal fluid proteins. This work suggests the rapid evolution of seminal fluid proteins may be associated with postmating-prezygotic isolation, which acts as a barrier for gene flow between even the most closely related species.

Conflict over fertilization underlies the transient evolution of reinforcement

ABSTRACTWhen two populations or species hybridize, their offspring often experience reductions in fitness relative to either parental population. The production of low fitness hybrids may be prevented by the evolution of increased prezygotic isolation; a process known as reinforcement. Theoretical challenges to the evolution of reinforcement are generally cast as a coordination problem — e.g., linkage disequilibrium between trait and preference loci is difficult to maintain in the face of recombination. However, the evolution of reinforcement also poses a potential conflict between mates. For example, the opportunity costs to hybridization may differ between the sexes or species. This is particularly likely for postmating prezygotic isolation, as the ability to fertilize both conspecific and heterospecific eggs is beneficial to male gametes, but heterospecific mating may incur a cost for female gametes. Motivated by this problem, we develop a population genetic model of interspecific conflict over reinforcement, inspired by ‘gametophytic factors’, which act as postmating prezygotic barriers among Zea mays subspecies. We demonstrate that this conflict results in the transient evolution of reinforcement – after female preference for a conspecific gamete trait rises to high frequency, male traits adaptively introgress into the other population. Ultimately the male gamete trait fixes in both species, and prezygotic isolation returns to pre-reinforcement levels. We interpret geographic patterns of isolation among Z. mays subspecies in light of these findings, and suggest when and how this conflict can be mediated. Our results suggest that sexual conflict may pose an understudied obstacle to the evolution of reinforcement via postmating prezygotic isolation.

Within-population sperm competition intensity does not predict asymmetry in conpopulation sperm precedence

ABSTRACTPostcopulatory sexual selection can generate coevolutionary arms races between the sexes resulting in the rapid coevolution of reproductive phenotypes. As traits affecting fertilisation success diverge between populations postmating prezygotic barriers to gene flow may evolve. Conspecific sperm precedence is a form of such isolation thought to evolve early during speciation yet has mostly been studied between species. Here we show conpopulation sperm precedence between Drosophila montana populations. Using genomic data to estimate divergence times and patterns of gene flow between populations, we show gene flow has played a considerable role during divergence. We find conpopulation sperm precedence is asymmetric and is concordant with asymmetry in non-competitive postmating prezygotic reproductive isolation. These results suggest these phenomena have a shared mechanism, but we show that this asymmetry is unrelated to the strength of postcopulatory sexual selection acting within populations. We tested whether overlapping foreign and coevolved ejaculates within the female reproductive tract altered fertilisation success but found no effect. Our results show that neither time since divergence nor sperm competitiveness predicts the strength of postmating prezygotic reproductive isolation. We suggest that divergence of postcopulatory phenotypes resulting in postmating prezygotic isolation is potentially driven by cryptic female choice, or mutation order divergence.

Reproductive Isolation through Experimental Manipulation of Sexually Antagonistic Coevolution in Drosophila melanogaster

Promiscuity can drive the evolution of sexual conflict before and after mating occurs. Post-mating, the male ejaculate can selfishly manipulate female physiology leading to a chemical arms race between the sexes. Theory suggests that drift and sexually antagonistic coevolution can cause allopatric populations to evolve different chemical interactions between the sexes, thereby leading to postmating reproductive barriers and speciation. There is, however, little empirical evidence supporting this form of speciation. We tested this theory by creating an experimental evolutionary model of Drosophila melanogaster populations undergoing different levels of interlocus sexual conflict. We found that allopatric populations under elevated sexual conflict show assortative mating indicating premating reproductive isolation. Further, these allopatric populations also show reduced copulation duration and sperm defense ability when mating happens between individuals between individuals across populations compared to that within the same population, indicating postmating prezygotic isolation. Sexual conflict can cause reproductive isolation in allopatric populations through the coevolution of chemical (postmating prezygotic) as well as behavioural (premating) interaction between the sexes. Thus, to our knowledge, we provide the first comprehensive evidence of postmating (as well as premating) reproductive isolation due to sexual conflict.