Fitness consequences of female multiple mating: A direct test of indirect benefits

BACKGROUND: The observation that females mate multiply when males provide nothing but sperm - which sexual selection theory suggests is unlikely to be limiting - continues to puzzle evolutionary biologists. Here we test the hypothesis that multiple mating is prevalent under such circumstances because it enhances female fitness. We do this by allowing female Trinidadian guppies to mate with either a single male or with multiple males, and then tracking the consequences of these matings across two generations. RESULTS: Overall, multiply mated females produced 67% more F2 grand-offspring than singly mated females. These offspring, however, did not grow or mature faster, nor were they larger at birth, than F2 grand-offspring of singly mated females. Our results, however, show that multiple mating yields benefits to females in the form of an increase in the production of F1. The higher fecundity among multiply mated mothers was driven by greater production of sons but not daughters. However, contrary to expectation, individually, the offspring of multiply mated females do not grow at different rates than offspring of singly mated females, nor do any indirect fitness benefits or costs accrue to second-generation offspring. CONCLUSIONS: The study provides strong evidence that multiple mating is advantageous to females, even when males contribute only sperm. This benefit is achieved through an increase in fecundity in the first generation, rather than through other fitness correlates such as size at birth, growth rate, time to sexual maturation and survival. Considered alongside previous work that female guppies can choose to mate with multiple partners, our results provide compelling evidence that direct fitness benefits underpin these mating decisions.