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Females increase offspring heterozygosity and fitness through extra-pair matings

Nature volume 425, pages 714–717 (2003)Cite this article

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.

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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.

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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.

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Authors and Affiliations

  1. Max Planck Research Centre for Ornithology, PO Box 1564, D-82305, Starnberg (Seewiesen), Germany

    Katharina Foerster, Kaspar Delhey, Arild Johnsen & Bart Kempenaers

  2. Zoological Museum, University of Oslo, PO Box 1172, Blindern, N-0318, Oslo, Norway

    Jan T. Lifjeld

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  1. Katharina Foerster
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Correspondence to Bart Kempenaers.

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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

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