Non-random paternity of offspring in a highly promiscuous marine snail suggests postcopulatory sexual selection

Abstract

In the marine snail Littorina saxatilis females are highly polyandrous, resulting in simultaneous broods of offspring sired by ∼20 males. Such high polyandry, in combination with female sperm storage, is likely to promote postcopulatory sexual selection among males. In addition, females may gain direct reproductive benefits from multiple mating. Investigating sexual selection in males and female benefits in relation to the number of sires, we put single virgin females in aquaria with one, two, five or ten males for 80 days, during which each female mated a majority of available males. After removal of the males, females continued to produce offspring during >1 year. Offspring genotypes of 27 families showed multiple paternity with 76 % of males contributing to juveniles, but paternity deviated from random with one or a few males siring the majority of the offspring. Larger males tended to be overrepresented among the sires. Female reproductive output (newborn or juvenile stage) did, however, not increase with number of sires, and females seemed not limited by the number of available males. Because previous studies have shown that females are seemingly indiscriminative in their mate choice, and given that they mate many hundreds of times in their lifespan, this suggests there is comparatively limited scope for premating sexual selection in this species. Hence, we interpret these results mainly in the light of postcopulatory sexual selection. Sexual selection is a main component of evolution. In that context, mating behaviour is central, although it sometimes appears puzzling, even maladaptive. For example, matings are costly; still, in some species, females mate multiple times and with numerous males. Why this behaviour has evolved is intriguing. Extensive numbers of matings suggest less efficient precopulatory mate choice, opening for postcopulatory sexual selection through cryptic female choice and sperm competition. Using a highly promiscuous snail species with internal fertilisation and long-term sperm storage, we identified the fathers of 549 offspring. We found that while females mated most males available, the offspring were non-randomly distributed among mated males and large males were overrepresented among the sires. This suggests that sexual selection predominantly occurs after mating and that males benefit from size-related effects. Yet, we could not find any female benefits from mating multiple males.