Female-driven mechanisms, ejaculate size and quality contribute to the lower fertility of sex-ratio distorter males in Drosophila simulans

Background: Sex-ratio meiotic drive refers to the preferential transmission of the X chromosome by XY males. The loss of Y-bearing sperm is caused by an X-linked distorter and results in female-biased progeny. The fertility of sex-ratio (SR) males expressing the distorter is usually strongly reduced compared to wild-type males, especially when they are in competition. The aim of this study was to identify the post-copulatory mechanisms that lower the fertility of SR males in Drosophila simulans. Parameters contributing to male fertility were measured in single and double mating conditions. Results: The most detrimental effect on SR males fertility is due to the size of their ejaculate which is half that of wild-type males. Sperm viability and sperm use by the females are also reduced. Sex-ratio males are poor sperm competitors in both offence and defence. We found evidence for sperm release from the female reproductive tract that specifically affects SR males. It results in the removal of stored sperm from a first SR mate without the action of the sperm of the second male. In addition, females mated once with an SR male remate more frequently with wild-type males. Conclusion: The paternity reduction of SR males in competitive conditions is greater than that attributable to their low sperm production and could prevent the spread of distorter X chromosomes in populations when multiple mating occur. The female-driven mechanisms are shown to play a major role both throughout the post-copulatory selective process and increased polyandry. The variation in male reproductive performance may drive the evolution of sexual learning capability of females.