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.
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Jennions, M. D. & Petrie, M. Why do females mate multiply? A review of the genetic benefits. Biol. Rev. 75, 21–64 (2000)
Tregenza, T. & Wedell, N. Genetic compatibility, mate choice and patterns of parentage: invited review. Mol. Ecol. 9, 1013–1027 (2000)
Zeh, J. A. & Zeh, D. W. Reproductive mode and the genetic benefits of polyandry. Anim. Behav. 61, 1051–1063 (2001)
Brown, J. L. A theory of mate choice based on heterozygosity. Behav. Ecol. 8, 60–65 (1997)
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)
Tregenza, T. & Wedell, N. Polyandrous females avoid costs of inbreeding. Nature 415, 71–73 (2002)
Thornhill, N. W. The Natural History of Inbreeding and Outbreeding: Theoretical and Empirical Perspectives (Univ. Chicago Press, Chicago, 1993)
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)
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)
Amos, W. et al. The influence of parental relatedness on reproductive success. Proc. R. Soc. Lond. B 268, 2021–2027 (2001)
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)
Höglund, J. et al. Inbreeding depression and male fitness in black grouse. Proc. R. Soc. Lond. B 269, 711–715 (2002)
Hansson, B. & Westerberg, L. On the correlation between heterozygosity and fitness in natural populations. Mol. Ecol. 11, 2467–2474 (2002)
Pusey, A. & Wolf, M. Inbreeding avoidance in animals. Trends Ecol. Evol. 11, 201–206 (1996)
Petrie, M. & Kempenaers, B. Extra-pair paternity in birds: explaining variation between species and populations. Trends Ecol. Evol. 13, 52–58 (1998)
Blomqvist, D. et al. Genetic similarity between mates and extra-pair parentage in three species of shorebirds. Nature 419, 613–615 (2002)
Kempenaers, B. et al. Extra-pair paternity results from female preference for high-quality males in the blue tit. Nature 357, 494–496 (1992)
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)
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)
Andersson, S., Örnborg, J. & Andersson, M. Ultraviolet sexual dimorphism and assortative mating in blue tits. Proc. R. Soc. Lond. B 265, 445–450 (1998)
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)
Sheldon, B., Andersson, S., Griffith, S. C., Örnborg, J. & Sendecka, J. Ultraviolet colour variation influences blue tit sex ratios. Nature 402, 874–877 (1999)
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)
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)
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)
Bensch, S., Price, T. & Kohn, J. Isolation and characterization of microsatellite loci in a Phylloscopus warbler. Mol. Ecol. 6, 91–92 (1997)
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)
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)
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)
Turelli, M. & Ginzburg, L. R. Should individual fitness increase with heterozygosity? Genetics 104, 191–209 (1983)
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.
The authors declare that they have no competing financial interests.
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
Behavioral Ecology and Sociobiology (2021)
Scientific Reports (2020)
Genome-wide analysis indicates association between heterozygote advantage and healthy aging in humans
BMC Genetics (2019)
Inbreeding load and inbreeding depression estimated from lifetime reproductive success in a small, dispersal-limited population
Extra-pair paternity patterns in European barn swallows Hirundo rustica are best explained by male and female age rather than male ornamentation
Behavioral Ecology and Sociobiology (2019)