Abstract
Female birds frequently copulate with extra-pair males1,2, but the adaptive value of this behaviour is poorly understood2. Some studies have suggested that ‘good genes’ may be involved, where females seek to have their eggs fertilized by high-quality males without receiving any material benefits from them3,4. Nevertheless, it remains to be shown that a genetic benefit is passed on to offspring5,6. Here we report that nestling bluethroats, Luscinia svecica , sired by extra-pair males had a higher T-cell-mediated immune response than their maternal half-siblings raised in the same nest. The difference could not be attributed to nestling body mass, sex or hatching order, but may be an effect of paternal genotype. Extra-pair young were also more immunocompetent than their paternal half-sibs raised in the genetic father's own nest, which indicates an additional effect of maternal genotype. Our results are consistent with the idea that females engage in extra-pair copulations to obtain compatible viability genes, rather than ‘good genes’ per se.
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Westneat, D. F. & Sherman, P. W. Density and extra-pair fertilizations in birds: a comparative analysis. Behav. Ecol. Sociobiol. 41, 205–215 (1997).
Birkhead, T. R. in Sperm Competition and Sexual Selection (eds Birkhead, T. R. & Møller, A. P.) 579–622 (Academic, London, 1998).
Kempenaers, B. et al. Extra-pair paternity results from female preference for high-quality males in the blue tit. Nature 357, 494– 496 (1992).
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).
Petrie, M. Improved growth and survival of offspring of peacocks with more elaborate trains. Nature 327, 598– 599 (1994).
Sheldon, B. C., Merilä, J., Qvarnström, A., Gustafsson, L. & Ellegren, H. Paternal genetic contribution to offspring condition predicted by size of male secondary sexual character. Proc. R. Soc. Lond. B 264, 297– 302 (1997).
Johnsen, A., Lifjeld, J. T., Rohde, P. A., Primmer, C. R. & Ellegren, H. Sexual conflict over fertilizations: female bluethroats escape male paternity guards. Behav. Ecol. Sociobiol. 43, 401–408 ( 1998).
Johnsen, A., Andersson, S., Örnborg, J. & Lifjeld, J. T. Ultraviolet plumage ornamentation affects social mate choice and sperm competition in bluethroats (Aves: Luscinia s. svecica): a field experiment. Proc. R. Soc. Lond. B 265, 1313–1318 (1998).
McCorkle, F. Jr, Olah, I. & Glick, B. The morphology of the phytohemagglutinin-induced cell response in the chicken wattle. Poultry Sci. 59, 616– 623 (1980).
Saino, N., Calza, S. & Møller, A. P. Immunocompetence of nestling barn swallows in relation to brood size and parental effort. J. Anim. Ecol. 66 , 827–836 (1997).
Brinkhof, M. W. G., Heeb, P., Kölliker, M. & Richner, H. Immunocompetence of nestling great tits in relation to rearing environment and parentage. Proc. R. Soc. Lond. B 266, 2315–2322 (1999).
Christe, P., Møller, A. P. & de Lope, F. Immunocompetence and nestling survival in the house martin: the tasty chick hypothesis. Oikos 83, 175–179 (1998).
Birkhead, T. R., Fletcher, F. & Pellatt, E. J. Nestling diet, secondary sexual traits and fitness in the zebra finch. Proc. R. Soc. Lond. B 266, 385–390 (1999).
Anthonisen, K., Krokene, C. & Lifjeld, J. T. Brood division is associated with fledgling dispersion in the bluethroat (Luscinia s. svecica). Auk 114, 553–561 (1997).
Kempenaers, B. & Sheldon, B. C. Why do male birds not discriminate between their own and extra-pair offspring? Anim. Behav. 51, 1165–1173 (1996).
Sheldon, B. C., Andersson, S., Griffith, S. C., Örnborg, J. & Sendecka, J. Ultraviolet colour variation influences blue tit sex ratios. Nature 402 , 874–877 (1999).
Gil, D., Graves, J., Hazon, N. & Wells, A. Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286, 126–128 ( 1999).
Cunningham, E. J. A. & Russell, A. F. Egg investment is influenced by male attractiveness in the mallard. Nature 404, 74–77 (2000).
Andersson, M. Sexual Selection (Princeton Univ. Press, Princeton, 1994).
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).
Jeffreys, A. J., Allen, M. J., Hagelberg, E. & Sonnberg, A. Identification of the skeletal remains of Josef Mengele by DNA analysis. Forensic Sci. Int. 56, 65–76 (1992).
Griffiths, R., Double, M. C., Orr, K. & Dawson, R. J. G. A DNA test to sex most birds. Mol. Ecol. 7, 1071– 1075 (1998).
Acknowledgements
We thank B.-A. Bjerke and C. K. Aas for assistance, and T. Amundsen, M. Andersson, T. R. Birkhead, D. Blomqvist, L. T. T. Hansen, B. Kempenaers, F. Mehlum, M. Petrie and T. Slagsvold, for comments. This work was supported by a post-doc fellowship from the Norwegian Research Council (A.J.) and a grant from the Nansen Endowment (J.T.L.). Permission to carry out the immune experiment on nestling bluethroats was given by the Norwegian Animal Research Authority.
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Zoological Museum, University of Oslo, Sars gate 1 , N-0562 Oslo, Norway
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Johnsen, A., Andersen, V., Sunding, C. et al. Female bluethroats enhance offspring immunocompetence through extra-pair copulations. Nature 406, 296–299 (2000). https://doi.org/10.1038/35018556
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DOI: https://doi.org/10.1038/35018556
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