Female Callosobruchus maculatus can maximize long-term fitness through polyandry

Females often mate with multiple males even when a single mating is sufficient to fertilize their eggs. Remating can lead to direct and indirect benefits for females, but these benefits trade-off against the potential costs associated with polyandry. There is a growing understanding that not all males are equal in their ability to deliver sperm to the site of fertilization. Such differences can arise both from environmental (e.g., mating history) and intrinsic (genetic) sources of variation. Most studies that investigate female fitness control male mating history to overcome such effects, but this control may bias interpretations of the benefits of polyandry. Here, we tried to avoid overestimating the benefits of polyandry that might accrue from mating repeatedly with virgin males. To do this, we quantified 6 components of fitness in female bruchid beetles, Callosobruchus maculatus, that were mated between 1 and 4 times to males with unknown mating histories, either in isolation or with rival males present. As copulation number increased, fecundity, offspring production, and egg-to-adult survival declined. In contrast to these short-term costs, the probability that a female remained completely infertile was highest at 1 copulation, and geometric mean fitness peaked after 3 copulations. Pericopulatory harassment by males did not affect female productivity. There was a significant interaction between this harassment and copulation number on longevity such that harassed females mating 2 or 3 times, and females mating twice in isolation, died soonest. Our results suggest that females may be selected to mate multiply despite short-term costs to fitness.