Behavioral Ecology and Sociobiology

, Volume 65, Issue 3, pp 513–523

Why do females have so few extra-pair offspring?

Original Paper

Abstract

It is generally accepted that if a female can improve her offspring’s genetics via extra-pair copulations (EPC), it is by copulating with extra-pair males whose phenotypes are more superior or whose genes are more compatible to hers than those of her bonded male. Here, we present a model that puts together uncertainties about the male genetic quality, a postcopulatory sperm bias in favor of the better or the more compatible genes, and costs that females pay by being choosy about extra-pair male quality. The model’s conclusions challenge traditional views of good genes explanations of EPC. When phenotypes give incomplete information about genotypes, a female choosing a phenotypically superior extra-pair male, may nevertheless find herself trading good genes of a bonded male for poor genes of an extra-pair male. Such “unfortunate sperm replacements” can limit the female involvement in EPC even when EPC are otherwise cost-free. The model also shows that even a female bonded to a phenotypically superior male may benefit by EPC, provided that sperm competition is biased toward sperm with more fit or more compatible genes. Furthermore, if choosiness is sufficiently costly, a female may even do best by copulating with a random extra-pair male.

Keywords

Extra-pair copulations EPC Female strategies Costs Mathematical model Sperm bias Old males Good genes Compatible genes 

References

  1. Akçay E, Roughgarden J (2007) Extra-pair paternity in birds: review of the genetic benefits. Evol Ecol Res 9:855–868Google Scholar
  2. Arnqvist G, Kirkpatrick M (2005) The evolution of infidelity in socially monogamous passerines: the strength of direct and indirect selection on extrapair copulation behaviour in females. Am Nat 165:S26–S37PubMedCrossRefGoogle Scholar
  3. Ball MA, Parker GA (2003) Sperm competition games: sperm selection by females. J Theor Biol 224:27–42PubMedCrossRefGoogle Scholar
  4. Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368PubMedCrossRefGoogle Scholar
  5. Brommer JE, Korsten P, Bouwman KM, Berg ML, Domdeur J (2007) Is extrapair mating random? On the probability distribution of extrapair young in avian broods. Behav Ecol 18:895–904CrossRefGoogle Scholar
  6. Brooks R, Kemp DJ (2001) Can older males deliver the good genes? TREE 16:308–313PubMedGoogle Scholar
  7. Dominey WR (1984) Altarnative mating tactics and evolutionarily stable strategies. Am Zool 24:385–396Google Scholar
  8. Evans JP, Zane L, Francescato S, Pilastro A (2003) Directional postcopulatory sexual selection revealed by artificial insemination. Nature 421:360–363PubMedCrossRefGoogle Scholar
  9. Eliassen S, Kokko H (2008) Current analyses do not resolve whether extra-pair paternity is male or female driven. Behav Ecol Sociobiol 62:1795–1804CrossRefGoogle Scholar
  10. Fisher RA (1930) The genetical theory of natural selection. Oxford University Press, OxfordGoogle Scholar
  11. Foerster K, Valcu M, Johnsen A (2006) A spatial genetic structure and effects of relatedness on mate choice in a wild bird population. Mol Ecol 15:4555–4567PubMedCrossRefGoogle Scholar
  12. Fromhage L, Kokko H, Reid JM (2009) Evolution of mate choice for genome-wide heterzygosity. Evolution 63:684–694PubMedCrossRefGoogle Scholar
  13. Gowaty PA (1996) Battles of the sexes and origins of monogamy. In: Black JM (ed) Partnerships in birds: the study of monogamy. Oxford University Press, Oxford, pp 21–52Google Scholar
  14. Griffith SC (2007) The evolution of infidelity in socially monogamous passerines: neglected components of direct and indirect selection. Am Nat 169:274–281PubMedCrossRefGoogle Scholar
  15. Griffith SC, Owens IPF, Thuman KA (2002) Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 11:2195–2212PubMedCrossRefGoogle Scholar
  16. Hansen TF, Price DK (1995) Good genes and old age: do old mates provide superior genes? J Evol Biol 8:759–778CrossRefGoogle Scholar
  17. Hasson O, Stone L (2009) Male infertility, female fertility and extrapair copulations. Biol Rev 84:225–244PubMedCrossRefGoogle Scholar
  18. Hardy OJ (2003) Estimation of pairwise relatedness between individuals and characterization of isolation-by-distance process using dominant genetic markers. Mol Ecol 12:1577–1588PubMedCrossRefGoogle Scholar
  19. Higginson AD, Reader T (2009) Environmental heterogeneity, genotype-environment interactions and the reliability of sexual traits as indicators of mate quality. Proc R Soc B 276:1153–1159PubMedCrossRefGoogle Scholar
  20. Howard DJ (1999) Conspecific sperm and pollen precedence and speciation. Ann Rev Ecol Syst 30:109–132CrossRefGoogle Scholar
  21. Kirkpatrick M (1986) The handicap mechanism of sexual selection does not work. Am Nat 127:222–240CrossRefGoogle Scholar
  22. Kokko H (1998) Good genes, old age and lifehistory trade-offs. Evol Ecol 12:739–750CrossRefGoogle Scholar
  23. Kokko H (1999) Kuckoldry and the stability of biparental care. Ecol Lett 2:247–255CrossRefGoogle Scholar
  24. Kokko H, Heubel K (2008) Condition-dependence, genotype-by-environment interactions and the lek paradox. Genetica 132:209–216PubMedCrossRefGoogle Scholar
  25. Lehmann L, Keller LF, Kokko H (2007) Mate choice evolution, dominance effects, and the maintenance of genetic variations. J Theor Biol 244:282–295PubMedCrossRefGoogle Scholar
  26. Locatello L, Rasotto MB, Evans JP, Pilastro A (2006) Colourful male guppies produce faster and more viable sperm. J Evol Biol 19:1595–1602PubMedCrossRefGoogle Scholar
  27. Marshall J, McNamara J, Houston A (2010) The state of Darwinian theory. Behav Ecol Soc. doi:10.1007/s00265-010-1121-y
  28. Maynard Smith J, Harper DGC (1995) Animal signals: models and terminology. J Theor Biol 177:305–311CrossRefGoogle Scholar
  29. Mays HL Jr, Albrecht T, Liu M, Hill GE (2008) Female choice for genetic complementary in birds: a review. Genetica 134:147–158PubMedCrossRefGoogle Scholar
  30. Neff BD, Pitcher TE (2005) Genetic quality and sexual selection: an integrated framework for good genes and compatible genes. Mol Ecol 14:19–38PubMedCrossRefGoogle Scholar
  31. Penn DJ (2009) The scent of genetic compatibility: sexual selection and the major histocompatibility complex. Ethology 108:1–21CrossRefGoogle Scholar
  32. Petrie M, Kempenaers B (1998) Extra-pair paternity in birds: explaining variation between species and populations. Trends Ecol Evol 13:52–58PubMedCrossRefGoogle Scholar
  33. Pitcher TE, Rodd FH, Rowe L (2007) Sexual colouration and sperm traits in guppies. J Fish Biol 70:165–177CrossRefGoogle Scholar
  34. Puurtinen M, Ketola T, Kotiaho JS (2005) Genetic compatibility and sexual selection. Trends Ecol Evol 20:157–158PubMedCrossRefGoogle Scholar
  35. Puurtinen M, Ketola T, Kotiaho JS (2009) The good-genes and compatible genes benefits of female choice. Am Nat 174:741–752PubMedCrossRefGoogle Scholar
  36. Radwan J (2003) Male age, germline mutations and the benefits of polyandry. Ecol Lett 6:581–586CrossRefGoogle Scholar
  37. Reid JM (2007) Secondary sexual ornaments and non-additive genetic benefits of female mate choice. Proc R Soc B 274:1395–1402PubMedCrossRefGoogle Scholar
  38. Slagsvold T, Lifjeld J (1997) Incomplete knowledge of male quality may explain variation in extra-pair paternity in birds. Behaviour 134:353–371CrossRefGoogle Scholar
  39. Schmoll T, Schurr FM, Winkel W, Epplen JT, Lubjun T (2009) Lifespan, lifetime reproductive performance and the paternity loss of within-pair and extra-pair offspring in the coal tit Periparus ater. Proc Roy Soc B 276:337–345CrossRefGoogle Scholar
  40. Westneat DF, Stewart IRK (2003) Extra-pair paternity in birds: causes, correlates, and conflict. Ann Rev Ecol Syst 34:365–396CrossRefGoogle Scholar
  41. Whittingham LA, Dunn PO (2001) Male parental care and paternity in birds. Curr Ornithol 16:257–298Google Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Biomathematics Unit, Department of Zoology, Faculty of Life SciencesTel Aviv UniversityRamat AvivIsrael

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