Abstract
Recent studies question the importance of indirect genetic effects in explaining female benefits of extra-pair matings in socially monogamous species. Compiling data on 14 wild bird species, Arnqvist and Kirkpatrick (Am Nat 165:S26–S37, 2005) estimated the average direct cost in terms or reduced parental care to be an order of magnitude larger than the potential effect of genetic benefits. This study has sparked a debate regarding potential confounding factors but no consensus appears to have been reached. Here we focus on the implicit assumption that all individuals face the same selective pressures and argue that this assumption is probably too strong in most cases. Using a theoretical model we show that when the amount of resources that a male provides depends on territory quality, his physical condition or prospects for alternative breeding opportunities, a female may respond to such differences by altering her mating behaviour. Such confounding factors may lead to direct fitness effects that result in negative correlations between paternal care and paternity even if females that produce extra-pair young experience a net benefit. Negative correlations can also result when males forcefully seek copulations and females resist them. We discuss the studies included in the analysis in this light, and conclude that current analyses on the net selective pressures remain uninformative. In addition to considering average effects across individuals and species we suggest giving attention to individual differences and the influence of ecological factors such as territory quality and predation pressures on female mating behaviour.
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References
Akçay E, Roughgarden J (2007) Extra-pair paternity in birds: review of the genetic benefits. Evol Ecol Res 9:855–868
Albrecht T, Kreisinger J, Pialek J (2006) The strength of direct selection against female promiscuity is associated with rates of extrapair fertilizations in socially monogamous songbirds. Am Nat 167:739–744
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–S37
Arnqvist G, Kirkpatrick M (2007) The evolution of infidelity in socially monogamous passerines revisited: a reply to Griffith. Am Nat 169:282–283
Blomqvist DD (2005) High frequency of extra-pair fertilisations in the moustached warbler, a songbird with a variable breeding system. Behaviour 142:1133–1148
Brommer JE, Korsten P, Bouwman KM, Berg ML, Komdeur J (2007) Is extrapair mating random? On the probability distribution of extrapair young in avian broods. Behav Ecol 18:895–904
Buchanan KL, Catchpole CK (2000) Song as an indicator of male parental effort in the sedge warbler. Proc R Soc Lond B 267:321–326
Burke T, Davies NB, Bruford MW, Hatchwell BJ (1989) Parental care and mating-behaviour of polyandrous dunnocks Prunella modularis related to paternity by DNA fingerprinting. Nature 338:249–251
Burley N (1986) Sexual selection for aesthetic traits in species with biparental care. Am Nat 127:415–445
Burley N (1988) The differential-allocation hypothesis—an experimental test. Am Nat 132:611–628
Charmantier A, Sheldon BC (2006) Testing genetic models of mate choice evolution in the wild. Trends Ecol Evol 21:417–419
Chuang-Dobbs HC, Webster MS, Holmes RT (2001) Paternity and parental care in the black-throated blue warbler, Dendroica caerulescens. Anim Behav 62:83–92
Cockburn A (2004) Mating systems and sexual conflict. In: Koenig WD, Dickinson J (eds) Ecology and Evolution of cooperative breeding in birds. Cambridge University Press, Cambridge, pp 81–101
Davies NB (1992) Dunnock behaviour and social evolution. Oxford University Press, Oxford
Dickinson JL (2001) Extrapair copulations in western bluebirds (Sialia mexicana): female receptivity favors older males. Behav Ecol Sociobiol 50:423–429
Dickinson JL (2003) Male share of provisioning is not influenced by actual or apparent loss of paternity in western bluebirds. Behav Ecol 14:360–366
Fedorka KM, Mousseau TA (2004) Female mating bias results in conflicting sex-specific offspring fitness. Nature 429:65–67
Freeman-Gallant CR (1996) DNA fingerprinting reveals female preference for male parental care in savannah sparrows. Proc R Soc Lond B 263:157–160
Gill SA, Stutchbury BJM (2006) Long-term mate and territory fidelity in neotropical buff-breasted wrens (Thryothorus leucotis). Behav Ecol Sociobiol 61:245–253
Gray EM (1997) Female red-winged blackbirds accrue material benefits from copulating with extra-pair males. Anim Behav 53:625–639
Griffith SC (2007) The evolution of infidelity in socially monogamous passerines: neglected components of direct and indirect selection. Am Nat 169:274–281
Griffith SC, Owens IPF, Thuman KA (2002) Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 11:2195–2212
Hadfield JD, Burgess MD, Lord A, Phillimore AB, Clegg SM, Owens IPF (2006) Direct versus indirect sexual selection: genetic basis of colour, size and recruitment in a wild bird. Proc R Soc Lond B 273:1347–1353
Hartley IR, Davies NB, Hatchwell BJ, Desrochers A, Nebel D, Burke T (1995) The ploygynandrous mating system of the alpine accentor, Prunella collaris. 2. Multiple paternity and parental effort. Anim Behav 49:789–803
Head ML, Hunt J, Jennions MD, Brooks R (2005) The indirect benefits of mating with attractive males outweigh the direct costs. PLOS Biology 3:e33
Hill GE (1991) Plumage coloration is a sexually selected indicator of male quality. Nature 350:337–339
Hoelzer GAD (1989) The good parent process of sexual selection. Anim Behav 38:1067–1078
Holen ØH, Johnstone RA (2007) Parental investment with a superior alien in the brood. J Evol Biol 20:2165–2172
Houston AI, McNamara JM (2002) A self-consistent approach to paternity and parental effort. Philos Trans R Soc Lond B Biol Sci 357:351–362
Houston AI, Szekely T, McNamara JM (2005) Conflict between parents over care. Trends Ecol Evol 20:33–38
Jennions MD, Petrie M (1997) Variation in mate choice and mating preferences: a review of causes and consequences. Biol Rev 72:283–232
Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64
Jennions MD, Møller AP, Petrie M (2001) Sexually selected traits and adult survival: a meta-analysis. Q Rev Biol 76:3–36
Kempenaers B (2007) Mate choice and genetic quality: a review of the heterozygosity theory. Adv Study Behav 37:189–278
Kempenaers B, Sheldon BC (1996) Why do male birds not discriminate between their own and extra-pair offspring? Anim Behav 51:1165–1173
Kempenaers B, Sheldon BC (1997) Studying paternity and paternal care: pitfalls and problems. Anim Behav 53:423–427
Kokko H (1998) Should advertising parental care be honest? Proc R Soc Lond B 265:1871–1878
Kokko H (1999a) Competition for early arrival in migratory birds. J Anim Ecol 68:940–950
Kokko H (1999b) Cuckoldry and the stability of biparental care. Ecol Lett 2:247–255
Kokko H, Heubel K (2008) Condition-dependence, genotype-by-environment interactions, and the lek paradox. Genetica 132:209–216
Kokko H, Jennions MD, Brooks R (2006) Unifying and testing models of sexual selection. Annu Rev Ecol Evol Syst 37:43–66
Krebs EA, Hunte W, Green DJ (2004) Plume variation, breeding performance and extra-pair copulations in the cattle egret. Behaviour 141:479–499
Kvarnemo C (2006) Evolution and maintenance of male care: is increased paternity a neglected benefit of care? Behav Ecol 17:144–148
Lifjeld JT, Dunn PO, Robertson RJ, Boag PT (1993) Extra-pair paternity in monogamous tree swallows. Anim Behav 45:213–229
Linville SU, Breitwisch R, Schilling AJ (1998) Plumage brightness as an indicator of parental care in northern cardinals. Anim Behav 55:119–127
Lubjuhn T, Curio S, Muth SC, Brün J, Epplen JT (1993) Influence of extra-pair paternity on parental care in great tit (Parus major). In: Pena SDJ, Chakraborty R, Epplen JT, Jeffreys AJ (eds) DNA fingerprinting: state of the science. Birkhäusen, Basel, pp 379–385
Magrath MJL, Komdeur J (2003) Is male care compromised by additional mating opportunity? Trends Ecol Evol 18:424–430
Marra PP, Hobson KA, Holmes RT (1998) Linking winter and summer events in a migratory bird by using stable-carbon isotopes. Science 282:1884–1886
Mitchell DP, Dunn PO, Whittingham LA, Freeman-Gallant CR (2007) Attractive males provide less parental care in two populations of the common yellowthroat. Anim Behav 73:165–170
Møller AP (2001) Heritability of arrival date in a migratory bird. Proc R Soc Lond B 268:203–206
Møller AP, Tegelstrom H (1997) Extra-pair paternity and tail ornamentation in the barn swallow Hirundo rustica. Behav Ecol Sociobiol 41:353–360
Nakagawa SD, Gillespie DOS, Hatchwell BJ, Burke T (2007) Does the badge of status influence parental care and investment in house sparrows? An experimental test. Oecologia 153:749–760
Oneal E, Connallon T, Knowles LL (2007) Conflict between direct and indirect benefits of female choice in desert Drosophila. Biol Lett 3:29–32
Petrie M, Kempenaers B (1998) Extra-pair paternity in birds: explaining variation between species and populations. Trends Ecol Evol 13:52–58
Pullin AS, Stewart GB (2006) Guidelines for systematic review in conservation and environmental management. Conserv Biol 20:1647–1656
Qvarnström A (1997) Experimentally increased badge size increases male competition and reduces male parental care in the collared flycatcher. Proc R Soc Lond B 264:1225–1231
Qvarnström A, Brommer JE, Gustafsson L (2006) Testing the genetics underlying the co-evolution of mate choice and ornament in the wild. Nature 441:84–86
Rowe KMC, Weatherhead PJ (2007) Social and ecological factors affecting paternity allocation in American robins with overlapping broods. Behav Ecol Sociobiol 61:1283–1291
Rubenstein DR (2007) Female extrapair mate choice in a cooperative breeder: trading sex for help and increasing offspring heterozygosity. Proc R Soc Lond B 274:1895–1903
Rundle HD, Ödeen A, Mooers AØ (2007) An experimental test for indirect benefits in Drosophila melanogaster. BMC Evol Biol 7:36
Schwagmeyer PL (1999) Species differences in male parental care in birds: a reexamination of correlates with paternity. The Auk 116:487–503
Sheldon BC (2000) Differential allocation: tests, mechanisms and implications. Trends Ecol Evol 15:397–402
Sheldon BC (2002) Relating paternity to paternal care. Philos Trans R Soc Lond B Biol Sci 357:341–350
Smiseth PT, Ornborg J, Andersson S, Amundsen T (2001) Is male plumage reflectance correlated with paternal care in bluethroats? Behav Ecol 12:164–170
Smith HG, Montgomerie R (1992) Male incubation in barn swallows—the influence of nest temperature and sexual selection. Condor 94:750–759
Stutchbury BJ, Rhymer JM, Morton ES (1994) Extrapair paternity in hooded warblers. Behav Ecol 5:384–392
Taylor ML, Wedell N, Hosken DJ (2007) The heritability of attractiveness. Curr Biol 17:R959–R960
Wagner RH, Schug MD, Morton ES (1996) Confidence of paternity, actual paternity and parental effort by purple martins. Anim Behav 52:123–132
West SA, Sheldon BC (2002) Constraints in the evolution of sex ratio adjustment. Science 295:1685–1688
Westneat DF (1995) Paternity and paternal behaviour in the red-winged blackbird, Agelaius phoeniceus. Anim Behav 49:21–35
Westneat DF, Sherman PW (1993) Parentage and the evolution of parental behaviour. Behav Ecol 4:66–77
Westneat DF, Stewart IRK (2003) Extra-pair paternity in birds: causes, correlates, and conflict. Annu Rev Ecol Evol Syst 34:365–396
Whittingham LA, Lifjeld JT (1995) High paternal investment in unrelated young—extra-pair paternity and male paternal care in house martins. Behav Ecol Sociobiol 37:103–108
Yezerinac SM, Weatherhead PJ, Boag PT (1996) Cuckoldry and lack of parentage-dependent paternal care in yellow warblers: a cost-benefit approach. Anim Behav 52:821–883
Acknowledgements
We thank Göran Arnqvist, Oren Hasson, Michael Jennions, Bart Kempenaers, Naomi Langmore, Dustin Rubenstein and two anonymous reviewers for their many very helpful comments and suggestions. Funding was provided by the Academy of Finland (HK) and the University of Bergen (SE).
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Communicated by S. Pruett-Jones
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Eliassen, S., Kokko, H. Current analyses do not resolve whether extra-pair paternity is male or female driven. Behav Ecol Sociobiol 62, 1795–1804 (2008). https://doi.org/10.1007/s00265-008-0608-2
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DOI: https://doi.org/10.1007/s00265-008-0608-2