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.

Genetic similarity between mates and extra-pair parentage in three species of shorebirds

Abstract

Matings between close relatives often reduce the fitness of offspring, probably because homozygosity leads to the expression of recessive deleterious alleles1,2,3,4,5. Studies of several animals have shown that reproductive success is lower when genetic similarity between parents is high4,5,6,7, and that survival and other measures of fitness increase with individual levels of genetic diversity8,9,10,11. These studies indicate that natural selection may favour the avoidance of matings with genetically similar individuals. But constraints on social mate choice, such as a lack of alternatives, can lead to pairing with genetically similar mates. In such cases, it has been suggested that females may seek extra-pair copulations with less related males4, but the evidence is weak or lacking4,5. Here we report a strong positive relationship between the genetic similarity of social pair members and the occurrence of extra-pair paternity and maternity (‘quasi-parasitism’) in three species of shorebirds. We propose that extra-pair parentage may represent adaptive behavioural strategies to avoid the negative effects of pairing with a genetically similar mate.

This is a preview of subscription content, access via your institution

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: Band-sharing between mates and occurrence of extra-pair fertilizations (EPFs) in three species of shorebirds: a, Kentish plover; b, western sandpiper; and c, common sandpiper.

References

  1. van Noordwijk, A. J. & Scharloo, W. Inbreeding in an island population of the great tit. Evolution 35, 674–688 (1981)

    Article  CAS  Google Scholar 

  2. Thornhill, N. W. (ed.) The Natural History of Inbreeding and Outbreeding (Univ. Chicago Press, Chicago, 1993)

  3. Jiménez, J. A., Hughes, K. A., Alaks, G., Graham, L. & Lacy, R. C. An experimental study of inbreeding depression in a natural habitat. Science 266, 271–273 (1994)

    Article  ADS  Google Scholar 

  4. Bensch, S., Hasselquist, D. & von Schantz, T. Genetic similarity between parents predicts hatching failure: non-incestuous inbreeding in the great reed warbler? Evolution 48, 317–326 (1994)

    Article  Google Scholar 

  5. Kempenaers, B., Adriaensen, F., van Noordwijk, A. J. & Dhondt, A. A. Genetic similarity, inbreeding and hatching failure in blue tits: are unhatched eggs infertile? Proc. R. Soc. Lond. B 263, 179–185 (1996)

    Article  ADS  Google Scholar 

  6. Olsson, M. & Madsen, T. Promiscuity in sand lizards (Lacerta agilis) and adder snakes (Vipera berus): Causes and consequences. J. Hered. 92, 190–197 (2001)

    Article  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  8. Amos, W. et al. The influence of parental relatedness on reproductive success. Proc. R. Soc. Lond. B 268, 2021–2028 (2001)

    Article  CAS  Google Scholar 

  9. Coltman, D. W., Bowen, W. D. & Wright, J. M. Birth weight and neonatal survival of harbour seal pups are positively correlated with genetic variation measured by microsatellites. Proc. R. Soc. Lond. B 265, 803–809 (1998)

    Article  CAS  Google Scholar 

  10. Coulson, T. N. et al. Microsatellites reveal heterosis in red deer. Proc. R. Soc. Lond. B 265, 489–495 (1998)

    Article  CAS  Google Scholar 

  11. Hansson, B., Bensch, S., Hasselquist, D. & Åkesson, M. Microsatellite diversity predicts recruitment of sibling great reed warblers. Proc. R. Soc. Lond. B 268, 1287–1291 (2001)

    Article  CAS  Google Scholar 

  12. Petrie, M. & Kempenaers, B. Extra-pair paternity in birds: explaining variation between species and populations. Trends Ecol. Evol. 13, 52–58 (1998)

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  14. Westneat, D. F. & Sherman, P. W. Density and extra-pair fertilizations in birds: a comparative analysis. Behav. Ecol. Sociobiol. 41, 205–215 (1997)

    Article  Google Scholar 

  15. Alves, M. A. S. & Bryant, D. M. Brood parasitism in the sand martin, Riparia riparia: evidence for two parasitic strategies in a colonial passerine. Anim. Behav. 56, 1323–1331 (1998)

    Article  CAS  Google Scholar 

  16. Wallander, J., Blomqvist, D. & Lifjeld, J. T. Genetic and social monogamy—does it occur without mate guarding in the ringed plover? Ethology 107, 561–572 (2001)

    Article  Google Scholar 

  17. Brooker, M. G., Rowley, I., Adams, M. & Baverstock, P. R. Promiscuity: an inbreeding avoidance mechanism in a socially monogamous species? Behav. Ecol. Sociobiol. 26, 191–199 (1990)

    Google Scholar 

  18. Stockley, P., Searle, J. B., Macdonald, D. W. & Jones, C. S. Female multiple mating behaviour in the common shrew as a strategy to reduce inbreeding. Proc. R. Soc. Lond. B 254, 173–179 (1993)

    Article  ADS  CAS  Google Scholar 

  19. Brown, J. L. A theory of mate choice based on heterozygosity. Behav. Ecol. 8, 60–65 (1997)

    Article  Google Scholar 

  20. Hasselquist, D., Bensch, S. & von Schantz, T. Correlation between male song repertoire, extra-pair paternity and offspring survival in the great reed warbler. Nature 381, 229–232 (1996)

    Article  ADS  CAS  Google Scholar 

  21. Kempenaers, B. et al. Extra-pair paternity results from female preference for high-quality males in the blue tit. Nature 357, 494–496 (1992)

    Article  ADS  Google Scholar 

  22. Petrie, M., Krupa, A. & Burke, T. Peacocks lek with relatives even in the absence of social and environmental cues. Nature 401, 155–157 (1999)

    Article  ADS  CAS  Google Scholar 

  23. Höglund, J., Alatalo, R. V., Lundberg, A., Rintamäki, P. T. & Lindell, J. Microsatellite markers reveal the potential for kin selection on black grouse leks. Proc. R. Soc. Lond. B 266, 813–816 (1999)

    Article  Google Scholar 

  24. Shorey, L., Piertney, S., Stone, J. & Höglund, J. Fine-scale genetic structuring on Manacus manacus leks. Nature 408, 352–353 (2000)

    Article  ADS  CAS  Google Scholar 

  25. del Hoyo, J., Elliott, A. & Sargatal, J. (eds) Handbook of the Birds of the World, Vol. 3. Hoatzin to Auks (Lynx Edicions, Barcelona, 1996)

  26. Carter, R. E. Molecular Methods in Ecology (ed. Baker, A. J.) 113–135 (Blackwell Science, Oxford, 2000)

    Google Scholar 

  27. Shin, H.-S., Bargiello, T. A., Clark, B. T., Jackson, F. R. & Young, M. W. An unusual coding sequence from a Drosophila clock gene is conserved in vertebrates. Nature 317, 445–448 (1985)

    Article  ADS  CAS  Google Scholar 

  28. Westneat, D. F. Polygyny and extrapair fertilizations in eastern red-winged blackbirds (Agelaius phoeniceus). Behav. Ecol. 4, 49–60 (1993)

    Article  Google Scholar 

  29. Griffiths, R., Double, M. C., Orr, K. & Dawson, R. J. G. A DNA test to sex most birds. Mol. Ecol. 7, 1071–1075 (1998)

    Article  CAS  Google Scholar 

  30. Ellegren, H. & Fridolfsson, A.-K. Male-driven evolution of DNA sequences in birds. Nature Genet. 17, 182–184 (1997)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank J. Lifjeld for scoring fingerprints; D. Hasselquist, A. Johnsen, K. Lessells, B. Sheldon and R. Wagner for comments on the manuscript; and U. Bläsi, I. Moll and K. Carter for logistic support. The study was supported by the Konrad Lorenz Institute for Comparative Ethology, Vienna, and by grants from the Natural Environment Research Council UK, the Hungarian Scientific Research Fund and the Swedish Research Council.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bart Kempenaers.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Blomqvist, D., Andersson, M., Küpper, C. et al. Genetic similarity between mates and extra-pair parentage in three species of shorebirds. Nature 419, 613–615 (2002). https://doi.org/10.1038/nature01104

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature01104

This article is cited by

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