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Female fur seals show active choice for males that are heterozygous and unrelated

Abstract

Much debate surrounds the exact rules that influence mating behaviour, and in particular the selective forces that explain the evolution of female preferences. A key example is the lek paradox, in which female choice is expected rapidly to become ineffective owing to loss of additive genetic variability for the preferred traits1,2,3. Here we exploit a remarkable system in which female fur seals exert choice by moving across a crowded breeding colony to visit largely static males. We show that females move further to maximize the balance between male high multilocus heterozygosity and low relatedness. Such a system shows that female choice can be important even in a strongly polygynous species, and at the same time may help to resolve the lek paradox because heterozygosity has low heritability and inbreeding avoidance means there is no single ‘best’ male for all females.

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Figure 1: Distances between male and female seals on the estimated day of conception.
Figure 2: Relationship between distance moved by female and father’s internal relatedness (IR, filled circles).

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References

  1. Borgia, G. in Sexual selection and reproductive competition in insects (eds Blum, M. S. & Blum, N. A.) 19–80 (Academic Press, New York, 1979)

    Google Scholar 

  2. Taylor, P. D. & Williams, G. C. The lek paradox is not resolved. Theor. Popul. Biol. 22, 392–409 (1982)

    Article  Google Scholar 

  3. Kirkpatrick, M. & Ryan, M. The evolution of mating preferences and the paradox of the lek. Nature 350, 33–38 (1991)

    Article  ADS  Google Scholar 

  4. Trivers, R. L. in Sexual selection and the descent of man, 1871–1971 (ed. Campbell, B.) 136–179 (Aldine-Atherton, Chicago, 1972)

    Google Scholar 

  5. Andersson, M. & Iwasa, Y. Sexual selection. Trends Ecol. Evol. 11, A53–A58 (1996)

    Article  Google Scholar 

  6. Birkhead, T. & Moller, A. Female control of paternity. Trends Ecol. Evol. 8, 100–104 (1993)

    Article  CAS  Google Scholar 

  7. Tomkins, J. L., Radwan, J., Kotiaho, J. S. & Tregenza, T. Genic capture and resolving the lek paradox. Trends Ecol. Evol. 19, 323–328 (2004)

    Article  Google Scholar 

  8. Qvarnström, A., Brommer, J. E. & Gustafsson, L. Testing the genetics underlying the co-evolution of mate choice and ornament in the wild. Nature 441, 84–86 (2006)

    Article  ADS  Google Scholar 

  9. Worthington Wilmer, J., Allen, P. J., Pomeroy, P. P., Twiss, S. D. & Amos, W. Where have all the fathers gone? An extensive microsatellite analysis of paternity in the grey seal (Halichoerus grypus). Mol. Ecol. 8, 1417–1429 (1999)

    Article  CAS  Google Scholar 

  10. Lidgard, D. C., Boness, D. J., Bowen, W. D., McMillan, J. I. & Fleischer, R. C. The rate of fertilization in male mating tactics of the polygynous grey seal. Mol. Ecol. 13, 3543–3548 (2004)

    Article  CAS  Google Scholar 

  11. Goldsworthy, S. D., Boness, D. J. & Fleischer, R. C. Mate choice among sympatric fur seals: female preference for conphenotypic males. Behav. Ecol. Sociobiol. 45, 253–267 (1999)

    Article  Google Scholar 

  12. Hoffman, J. I., Boyd, I. L. & Amos, W. Male reproductive strategy and the importance of maternal status in the Antarctic fur seal Arctocephalus gazella. Evolution Int. J. Org. Evolution 57, 1917–1930 (2003)

    Article  Google Scholar 

  13. Hoffman, J. I., Trathan, P. N. & Amos, W. Genetic tracking reveals extreme site fidelity in territorial male Antarctic fur seals Arctocephalus gazella. Mol. Ecol. 15, 3841–3847 (2006)

    Article  CAS  Google Scholar 

  14. Hoffman, J. I., Boyd, I. L. & Amos, W. Exploring the relationship between parental relatedness and male reproductive success in the Antarctic fur seal Arctocephalus gazella. Evolution Int. J. Org. Evolution 58, 2087–2099 (2004)

    Article  Google Scholar 

  15. Amos, W. et al. The influence of parental relatedness on reproductive success. Proc. R. Soc. Lond. B 268, 2021–2027 (2001)

    Article  CAS  Google Scholar 

  16. Hansson, B. & Westerberg, L. On the correlation between heterozygosity and fitness in natural populations. Mol. Ecol. 11, 2467–2474 (2002)

    Article  Google Scholar 

  17. Hoffman, J. I., Forcada, J. & Amos, W. No relationship between microsatellite variation and neonatal fitness in Antarctic fur seals, Arctocephalus gazella. Mol. Ecol. 15, 1995–2005 (2006)

    Article  CAS  Google Scholar 

  18. Acevedo-Whitehouse, K., Gulland, F., Grieg, D. & Amos, W. Inbreeding: Disease susceptibility in California sea lions. Nature 422, 35 (2003)

    Article  ADS  CAS  Google Scholar 

  19. Rowe, L. & Houle, D. The lek paradox and the capture of genetic variance by condition dependent traits. Proc. R. Soc. Lond. B 263, 1415–1421 (1996)

    Article  ADS  Google Scholar 

  20. 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)

    Article  CAS  Google Scholar 

  21. Brown, J. L. & Eklund, A. Kin recognition and the major histocompatibility complex: an integrative review. Am. Nat. 143, 435–461 (1994)

    Article  Google Scholar 

  22. Bernatchez, L. & Landry, C. MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? J. Evol. Biol. 16, 363–377 (2003)

    Article  CAS  Google Scholar 

  23. Partridge, L. in Mate Choice (ed. Bateson, P.) 227–256 (Cambridge University Press, Cambridge, 1983)

    Google Scholar 

  24. Irwin, A. J. & Taylor, P. D. Heterozygous advantage and the evolution of female choice. Evol. Ecol. Res. 2, 119–128 (2000)

    Google Scholar 

  25. Pujolar, J. M., Maes, G. E., Vancoillie, C. & Volckaert, F. A. M. Growth rate correlates to individual heterozygosity in the european eel, Anguilla anguilla L. Evolution Int. J. Org. Evolution 59, 189–199 (2005)

    CAS  Google Scholar 

  26. Tiira, K. et al. Do dominants have higher heterozygosity? Social status and genetic variation in brown trout, Salmo trutta. Behav. Ecol. Sociobiol. 59, 657–665 (2006)

    Article  Google Scholar 

  27. Seddon, N., Amos, W., Mulder, R. A. & Tobias, J. A. Male heterozygosity predicts territory size, song structure and reproductive success in a cooperatively breeding bird. Proc. R. Soc. Lond. B 271, 1823–1829 (2004)

    Article  Google Scholar 

  28. Arnould, J. P. Y. & Duck, C. D. The cost and benefits of territorial tenure, and factors affecting mating success in male Antarctic fur seals. J. Zool. 241, 649–664 (1997)

    Article  Google Scholar 

  29. Hoffman, J. I. & Amos, W. Microsatellite genotyping errors: detection approaches, common sources and consequences for paternal exclusion. Mol. Ecol. 14, 599–612 (2005)

    Article  CAS  Google Scholar 

  30. Queller, D. C. & Goodnight, K. F. Estimating relatedness using genetic markers. Evolution 43, 258–275 (1989)

    Article  Google Scholar 

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Acknowledgements

We thank D. Briggs, S. Robinson, M. Jessop, K. Reid, R. Taylor, T. Walker and N. Warren for help with logistics and fieldwork. We are also grateful to T. Clutton-Brock, S. Hodge and K. Isvaran for helpful comments on the manuscript. This work was funded by the Natural Environment Research Council (NERC) and the Antarctic Funding Initiative (AFI), and contributes to the BAS DISCOVERY 2010 science programme. J.I.H. was also funded by the Isaac Newton Trust, Balfour fund and Cambridge University VIP scheme. Fieldwork was approved by BAS and the University of Cambridge Animal Ethics Board. Samples were collected and retained under permits issued by the Department for Environment, Food and Rural Affairs (DEFRA), and in accordance with the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES).

Author Contributions J.I.H. contributed to the concept, genotyping, data analysis, and writing; W.A. to the concept, data analysis and writing; and J.F. and P.N.T. to field project coordination and the collection of tissue samples and observational data.

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Correspondence to J. I. Hoffman.

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Hoffman, J., Forcada, J., Trathan, P. et al. Female fur seals show active choice for males that are heterozygous and unrelated. Nature 445, 912–914 (2007). https://doi.org/10.1038/nature05558

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