Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

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

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.

Your institute does not have access to this article

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

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.

References

  1. Jennions, M. D. & Petrie, M. Why do females mate multiply? A review of the genetic benefits. Biol. Rev. Camb. Phil. Soc. 75, 21–64 (2000)

    CAS  Article  Google Scholar 

  2. Madsen, T., Shine, R., Loman, J. & Hakansson, T. Why do female adders copulate so frequently?. Nature 335, 440–441 (1992)

    ADS  Article  Google Scholar 

  3. Tregenza, T. & Wedell, N. Benefits of multiple mates in the cricket Gryllus bimaculatus. Evolution Int. J. Org. Evolution 52, 1726–1730 (1998)

    Article  Google Scholar 

  4. Tregenza, T. & Weddell, N. Genetic compatibility, mate choice and patterns of parentage. Mol. Ecol. 9, 1013–1027 (2000)

    CAS  Article  Google Scholar 

  5. Zeh, J. A. & Zeh, D. W. Reproductive mode and the genetic benefits of polyandry. Anim. Behav. 61, 1051–1063 (2001)

    Article  Google Scholar 

  6. Olsson, M., Shine, R., Madsen, T., Gullberg, A. & Tegelstrom, H. Sperm selection by females. Nature 383, 585 (1996)

    ADS  CAS  Article  Google Scholar 

  7. Thuman, K. A. & Griffith, S. C. Genetic similarity and the non-random distribution of paternity in a genetically highly polyandrous shorebird. Anim. Behav. 69, 765–770 (2005)

    Article  Google Scholar 

  8. Tregenza, T. & Wedell, N. Polyandrous females avoid costs of inbreeding. Nature 415, 71–73 (2002)

    ADS  CAS  Article  Google Scholar 

  9. Yasui, Y. A ‘good sperm’ model can explain the evolution of costly multiple mating by females. Am. Nat. 149, 573–584 (1997)

    Article  Google Scholar 

  10. Simmons, L. W. The evolution of polyandry: sperm competition, sperm selection, and offspring viability. Annu. Rev. Ecol. Evol. Syst. 36, 125–146 (2005)

    Article  Google Scholar 

  11. Tregenza, T., Wedell, N., Hosken, D. J. & Ward, P. I. Maternal effects on offspring depend on female mating pattern and offspring environment in yellow dung flies. Evolution Int. J. Org. Evolution 57, 297–304 (2003)

    Article  Google Scholar 

  12. Sheldon, B. C. Differential allocation: tests, mechanisms and implications. Trends Ecol. Evol. 15, 397–402 (2000)

    CAS  Article  Google Scholar 

  13. Kozielska, M., Krzeminska, A. & Radwan, J. Good genes and the maternal effects of polyandry on offspring reproductive success in the bulb mite. Proc. R. Soc. Lond. B 271, 165–170 (2004)

    Article  Google Scholar 

  14. Weigensberg, I., Carriére, Y. & Roff, D. A. Effects of male genetic contribution and paternal investment to egg and hatchling size in the cricket Gryllus firmus. J. Evol. Biol. 11, 135–146 (1998)

    Article  Google Scholar 

  15. Zeh, J. A. & Zeh, D. W. Outbred embryos rescue inbred half-siblings in mixed-paternity broods of live-bearing females. Nature 439, 201–203 (2006)

    ADS  CAS  Article  Google Scholar 

  16. Evans, J. P., Zane, L., Francescato, S. & Pilastro, A. Directional postcopulatory sexual selection revealed by artificial insemination. Nature 421, 360–363 (2003)

    ADS  CAS  Article  Google Scholar 

  17. Hosken, D. J., Garner, T. W. J., Tregenza, T., Wedell, N. & Ward, P. I. Superior sperm competitors sire higher-quality young. Proc. R. Soc. Lond. B 2270, 1933–1938 (2003)

    Article  Google Scholar 

  18. Holleley, C. E., Dickman, C. R., Crowther, M. S. & Oldroyd, B. P. Size breeds success: multiple paternity, multivariate selection and male semelparity in a small marsupial, Antechinus stuartii. Mol. Ecol. 15, 3439–3448 (2006)

    CAS  Article  Google Scholar 

  19. Selwood, L. A timetable of embryonic development of the dasyurid marsupial Antechinus stuartii (Macleay). Aust. J. Zool. 28, 649–668 (1980)

    Google Scholar 

  20. Fisher, D. O. Population density and presence of the mother are related to natal dispersal decisions in male and female Antechinus stuartii. Aust. J. Zool. 53, 103–110 (2005)

    Article  Google Scholar 

  21. Fisher, D. O. & Cockburn, A. The large male advantage in brown antechinuses: female choice, male dominance and delayed male death. Behav. Ecol. 17, 164–171 (2005)

    Article  Google Scholar 

  22. Kraaijeveld-Smit, F. J. L., Ward, S. J. & Temple-Smith, P. D. Paternity success and the direction of sexual selection in a field population of a semelparous marsupial, Antechinus agilis. Mol. Ecol. 12, 475–484 (2003)

    CAS  Article  Google Scholar 

  23. Fisher, D. O., Double, M. C. & Moore, B. D. Number of mates and timing of mating affect offspring growth in the small marsupial, Antechinus agilis. Anim. Behav. 71, 289–297 (2006)

    Article  Google Scholar 

  24. Neff, B. D. & Pitcher, T. E. Genetic quality and sexual selection: an integrated framework for good genes and compatible genes. Mol. Ecol. 14, 19–38 (2005)

    CAS  Article  Google Scholar 

  25. Evans, J. P. & Marshall, D. J. Male-by-female interactions influence fertilization success and mediate the benefits of polyandry in the sea urchin Heliocidaris erythrogramma. Evolution Int. J. Org. Evolution 59, 106–112 (2005)

    Article  Google Scholar 

  26. Nicholls, J. A., Double, M. C., Rowell, D. & Magrath, R. D. The evolution of cooperative and pair breeding in thornbills Acanthiza (Aves: Pardalotidae). J. Avian Biol. 31, 165–176 (2000)

    Article  Google Scholar 

  27. Bates, D. & Maechler, M. Matrix: a matrix package for R (R Foundation for Statistical Computing, Vienna, 2006)

  28. R Core Development Team. R: a language and environment for statistical computing (R Foundation for Statistical Computing, Vienna, 2006)

  29. Genstat Committee. Genstat Manual, version 8 (Clarendon, Oxford, UK, 2005)

  30. Pollock, K. H., Nichols, J. D., Brownie, C. & Hines, J. E. Statistical inference for capture-recapture experiments. Wildlife Monogr. 107, 1–97 (1990)

    Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Diana O. Fisher.

Ethics declarations

Competing interests

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

Supplementary information

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)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Fisher, D., Double, M., Blomberg, S. et al. Post-mating sexual selection increases lifetime fitness of polyandrous females in the wild. Nature 444, 89–92 (2006). https://doi.org/10.1038/nature05206

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature05206

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing