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

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Abstract

Females often mate with several males before producing offspring1. Field studies of vertebrates suggest, and laboratory experiments on invertebrates confirm, that even when males provide no material benefits, polyandry can enhance offspring survival2,3. This enhancement is widely attributed to genetic benefits that arise whenever paternity is biased towards males that sire more viable offspring1,4,5. Field studies suggest that post-mating sexual selection biases fertilization towards genetically more compatible males6,7 and one controlled experiment has shown that, when females mate with close kin, polyandry reduces the relative number of inbred offspring8. Another potential genetic benefit of polyandry is that it increases offspring survival because males with more competitive ejaculates sire more viable offspring9. Surprisingly, however, there is no unequivocal evidence for this process10. 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 event10 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.

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Acknowledgements

We thank P. Backwell, S. Griffith and M. Olsson for discussions and comments; numerous field and lab assistants for their hard work; P. Marsack, S. and R. Berkhout, and O. and C. Carriage for help at Kioloa. This work was supported by an Australian Research Council fellowship (to D.O.F.). Author Contributions D.O.F. designed the main study, carried out the experiments, performed animal husbandry and drafted the manuscript. M.C.D. performed the molecular analysis. S.P.B. performed statistical analyses and contributed to fieldwork. A.C. carried out additional statistical analyses; M.D.J. designed the sperm competition experiment. All authors discussed the results and analysis and contributed to the writing.

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Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.

Correspondence to Diana O. Fisher.

Supplementary information

  1. Supplementary Methods and Supplementary Discussion

    This file contains details of the methods for genotyping, statistical analysis and discussion of the effect of treatment on offspring sex ratio and survival, and offspring growth. This file also contains an elaboration of the combined effects of mating treatment across years, our choice of methods to analyse the number of young attached at birth, and of the effect of ejaculate competitiveness on offspring survival, and an explanation of the evidence concerning relatedness between mates, and of the extraordinary life history and sexual behaviour of male antechinuses. (DOC 43 kb)

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Further reading

Figure 1: Effect of mating treatment and rearing environment on the proportion of offspring surviving to weaning.
Figure 2: Effect of mating treatment and male ejaculate competitiveness on survival of offspring in captivity from birth to release (2004).
Figure 3: Total number of offspring sired by males when mated to three polyandrous females.

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