Post-mating sexual selection increases lifetime fitness of polyandrous females in the wild

Females often mate with several males before producing offspring(1). Field studies of vertebrates suggest, and laboratory experiments on invertebrates confirm, that even when males provide no material benefits, polyandry can enhance offspring survival(2,3). This enhancement is widely attributed to genetic benefits that arise whenever paternity is biased towards males that sire more viable offspring(1,4,5). Field studies suggest that post-mating sexual selection biases fertilization towards genetically more compatible males(6,7) and one controlled experiment has shown that, when females mate with close kin, polyandry reduces the relative number of inbred offspring(8). Another potential genetic benefit of polyandry is that it increases offspring survival because males with more competitive ejaculates sire more viable offspring(9). Surprisingly, however, there is no unequivocal evidence for this process(10). Here, by experimentally assigning mates to females, we show that polyandry greatly increases offspring survival in the Australian marsupial Antechinus stuartii. DNA profiling shows that males that gain high paternity under sperm competition sire offspring that are more viable. This beneficial effect occurs in both the laboratory and the wild. Crucially, there are no confounding non-genetic maternal effects that could arise if polyandry increases female investment in a particular reproductive event(10) because A. stuartii is effectively semelparous. Our results therefore show that polyandry improves female lifetime fitness in nature. The threefold increase in offspring survival is not negated by a decline in maternal lifespan and is too large to be offset by an equivalent decline in the reproductive performance of surviving offspring.