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.

Females increase offspring heterozygosity and fitness through extra-pair matings

Abstract

Females in a variety of species commonly mate with multiple males, and there is evidence that they benefit by producing offspring of higher genetic quality1,2,3; however, the nature of these genetic benefits is debated1,2,3,4. Enhanced offspring survival or quality can result from intrinsic effects of paternal genes—‘good genes’—or from interactions between the maternal and paternal genomes—‘compatible genes’1,2,3,4,5. Evidence for the latter process is accumulating2,6: matings between relatives lead to decreased reproductive success, and the individual level of inbreeding—measured as average heterozygosity—is a strong fitness predictor7,8,9,10,11,12,13. Females should thus benefit from mating with genetically dissimilar males2,14. In many birds, social monogamy restricts mate choice, but females may circumvent this by pursuing extra-pair copulations15,16. Here we show that female blue tits, Parus caeruleus, increase the heterozygosity of their progeny through extra-pair matings. Females thereby produce offspring of higher reproductive value, because less inbred individuals have increased survival chances, a more elaborate male secondary sexual trait (crown colour) and higher reproductive success. The cost of inbreeding may therefore be an important factor driving the evolution of female extra-pair mating.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Mean difference (±s.e.m.) in standardized heterozygosity between extra-pair young and their within-pair nestmates.
Figure 2: Correlation between standardized heterozygosity and crown coloration in 49 male blue tits.

References

  1. 1

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

    CAS  Article  Google Scholar 

  2. 2

    Tregenza, T. & Wedell, N. Genetic compatibility, mate choice and patterns of parentage: invited review. Mol. Ecol. 9, 1013–1027 (2000)

    CAS  Article  Google Scholar 

  3. 3

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

    Article  Google Scholar 

  4. 4

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

    MathSciNet  Article  Google Scholar 

  5. 5

    Zeh, J. A. & Zeh, D. W. The evolution of polyandry I: intragenomic conflict and genetic incompatibility. Proc. R. Soc. Lond. B 263, 1711–1717 (1996)

    Article  Google Scholar 

  6. 6

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

    CAS  Article  Google Scholar 

  7. 7

    Thornhill, N. W. The Natural History of Inbreeding and Outbreeding: Theoretical and Empirical Perspectives (Univ. Chicago Press, Chicago, 1993)

    Google Scholar 

  8. 8

    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  Google Scholar 

  9. 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)

    CAS  Article  Google Scholar 

  10. 10

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

    CAS  Article  Google Scholar 

  11. 11

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

    CAS  Article  Google Scholar 

  12. 12

    Höglund, J. et al. Inbreeding depression and male fitness in black grouse. Proc. R. Soc. Lond. B 269, 711–715 (2002)

    Article  Google Scholar 

  13. 13

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

    Article  Google Scholar 

  14. 14

    Pusey, A. & Wolf, M. Inbreeding avoidance in animals. Trends Ecol. Evol. 11, 201–206 (1996)

    CAS  Article  Google Scholar 

  15. 15

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

    CAS  Article  Google Scholar 

  16. 16

    Blomqvist, D. et al. Genetic similarity between mates and extra-pair parentage in three species of shorebirds. Nature 419, 613–615 (2002)

    CAS  Article  Google Scholar 

  17. 17

    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  Google Scholar 

  18. 18

    Kempenaers, B., Verheyen, G. R. & Dhondt, A. A. Extrapair paternity in the blue tit (Parus caeruleus): female choice, male characteristics, and offspring performance. Behav. Ecol. 8, 481–492 (1997)

    Article  Google Scholar 

  19. 19

    Aparicio, J. M., Cordero, P. J. & Veiga, J. P. A test of the hypothesis of mate choice based on heterozygosity in the spotless starling. Anim. Behav. 62, 1001–1006 (2001)

    Article  Google Scholar 

  20. 20

    Andersson, S., Örnborg, J. & Andersson, M. Ultraviolet sexual dimorphism and assortative mating in blue tits. Proc. R. Soc. Lond. B 265, 445–450 (1998)

    Article  Google Scholar 

  21. 21

    Hunt, S., Cuthill, I. C., Bennett, A. T. D. & Griffiths, R. Preferences for ultraviolet partners in the blue tit. Anim. Behav. 58, 809–815 (1999)

    CAS  Article  Google Scholar 

  22. 22

    Sheldon, B., Andersson, S., Griffith, S. C., Örnborg, J. & Sendecka, J. Ultraviolet colour variation influences blue tit sex ratios. Nature 402, 874–877 (1999)

    CAS  Article  Google Scholar 

  23. 23

    Mitton, J. B., Schuster, W. S. F., Cothran, E. G. & De Fries, J. C. Correlation between the individual heterozygosity of parents and their offspring. Heredity 71, 59–63 (1993)

    Article  Google Scholar 

  24. 24

    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)

    CAS  Article  Google Scholar 

  25. 25

    Dawson, D. A., Hanotte, O., Greig, C., Stewart, I. R. K. & Burke, T. Polymorphic microsatellites in the blue tit Parus caeruleus and their cross-species utility in 20 songbird families. Mol. Ecol. 9, 1941–1944 (2000)

    CAS  Article  Google Scholar 

  26. 26

    Bensch, S., Price, T. & Kohn, J. Isolation and characterization of microsatellite loci in a Phylloscopus warbler. Mol. Ecol. 6, 91–92 (1997)

    CAS  Article  Google Scholar 

  27. 27

    Fridolfsson, A. K., Gyllensten, U. B. & Jakobsson, S. Microsatellite markers for paternity testing in the willow warbler Phylloscopus trochilus: high frequency of extra-pair young in an island population. Hereditas 126, 127–132 (1997)

    Article  Google Scholar 

  28. 28

    Jamieson, A. The effectiveness of using co-dominant polymorphic allelic series for (1) checking pedigrees and (2) distinguishing full-sib pair members. Anim. Genet. 25, 37–44 (1994)

    Article  Google Scholar 

  29. 29

    Pemberton, J. M., Coltman, D. W., Coulson, T. N. & Slate, J. in Microsatellites, Evolution and Applications (eds Goldstein, D. B. & Schlötterer, C.) 151–164 (Oxford Univ. Press, Oxford, 1999)

    Google Scholar 

  30. 30

    Turelli, M. & Ginzburg, L. R. Should individual fitness increase with heterozygosity? Genetics 104, 191–209 (1983)

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank D. Blomqvist, S. Griffith, D. Hasselquist, L. Keller, M. Milinski, A. Peters, B. Sheldon, C. Wedekind and D. Zeh for comments on the manuscript; K. Carter, D. Kaulfuss, H. Kunc, K. Peer, A. Pösel and A. Türk for help with field and laboratory work; S. Andersson for computing the colour variables; and H. Winkler (Konrad Lorenz Institute for Comparative Ethology) and R.-T. Klumpp and A. Fojt (Institute of Silviculture, University of Agricultural Sciences, Vienna) for logistic support.

Author information

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

Foerster, K., Delhey, K., Johnsen, A. et al. Females increase offspring heterozygosity and fitness through extra-pair matings. Nature 425, 714–717 (2003). https://doi.org/10.1038/nature01969

Download citation

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