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In many species, the physical act of mating and exposure to accessory gland proteins (Acps) in male seminal fluid reduces female survival and offspring production. It is not clear what males gain from harming their sexual partners or why females mate frequently despite being harmed. Using sterile strains of Drosophila melanogaster that differ in their production of Acps, we found that both the physical act of mating and exposure to male seminal fluid in mothers increase the fitness of daughters. We show that the changes in daughter fitness are mediated by parental effects, not by sexual selection involving good genes or owing to variation in maternal egg production. These results support the idea that male harm of females might partly evolve through cross-generational fitness benefits.

In many species, increased mating frequency reduces maternal survival and reproduction. In order to understand the evolution of mating frequency, we need to determine the consequences of increased mating frequency for offspring. We conducted an experiment in Drosophila melanogaster in which we manipulated the mating frequency of mothers and examined the survival and fecundity of the mothers and their daughters. We found that mothers with the highest mating frequency had accelerated mortality and more rapid reproductive senescence. On average, they had 50% shorter lives and 30% lower lifetime reproductive success (LRS) than did mothers with the lowest mating frequency. However, mothers with the highest mating frequency produced daughters with 28% greater LRS. This finding implies that frequent mating stimulates cross-generational fitness trade-offs such that maternal fitness is reduced while offspring fitness is enhanced. We evaluate these results using a demographic metric of inclusive fitness. We show that the costs and benefits of mating frequency depend on the growth rate of the population. In an inclusive fitness context, there was no evidence that increased mating frequency results in fitness costs for mothers. These results indicate that cross-generational fitness trade-offs have an important role in sexual selection and life-history evolution.

In traditional deterministic models the conditions for the evolution of sex and sexual behavior are limited because their benefits are context dependent. In novel and adverse environments both multiple mating and recombination can help generate gene combinations that allow for rapid adaptation. Mating frequency often increases in conditions in which recombination might be beneficial; therefore, increased sexual behavior might evolve to act as a cue that stimulates recombination. We conducted two experiments in the fruit fly, Drosophila melanogaster, using linked phenotypic markers to determine how recent bouts of additional mating affect female recombination rate. The first experiment examined the effect of additional mating, mating history, and age on female recombination rate. The second experiment assessed the effect of recent mating events on recombination rate. Together, the experiments suggest that each additional bout of mating temporarily increases female recombination rate. These findings imply that the conditions favoring the evolution of sexual reproduction and multiple mating behaviors are broader than currently appreciated.