Journal of Ornithology

, Volume 152, Supplement 1, pp 265–277 | Cite as

A review and perspective on context-dependent genetic effects of extra-pair mating in birds

  • Tim SchmollEmail author


The evolutionary origin and the maintenance of extra-pair mating in birds has been a major field of study in the last decades, but no consensus has been reached on the adaptive significance of this behaviour for female birds. The genetic benefit hypothesis proposes that extra-pair sires provide alleles of superior quality and/or better compatibility compared to the social mate, resulting in offspring of higher reproductive value. One frequently adopted approach to test this idea compares the performance of maternal half-siblings in broods with multiple paternity. However, results from such comparisons are inconsistent. Here I discuss the concept that the magnitude of genetic fitness benefits from extra-pair mating depends on the environmental context. To date, context-dependent genetic effects in maternal half-sibling comparisons have been demonstrated for only five passerine bird species. In none of the studies were the crucial environmental conditions experimentally manipulated, and the potentially confounding effects of differential maternal investment in relation to paternity were also largely not accounted for. A number of high-quality data sets on fitness consequences of extra-pair mating behaviour are available that could be (re-) analysed for context-dependence given that relevant gradients of the environment have been recorded and their use is well justified a priori. Such relevant variation may include, for example, the time of breeding in temperate regions, hatching order, but also offspring sex. Primarily, however, experimental approaches are required that systematically and gradually vary fitness-relevant environmental gradients, such as food availability or parasite abundance, and analyse the resulting differential fitness effects while controlling for differential investment. The context dependency of the genetic effects of extra-pair mating behaviour may offer an opportunity for reconciling conflicting results from different extra-pair paternity studies within and across species. More generally, it could allow a better understanding of under which environmental conditions will selection act to maintain a female mating bias towards extra-pair males with potentially far-reaching implications for the ecology and evolution of mating preferences and the maintenance of genetic variation in (sexually) selected traits.


Compatible genes Context-dependence Differential investment Extra-pair paternity Genotype-by-environment interaction Good genes Fitness consequences Half-sibling comparison Multiple mating 


Der evolutionäre Ursprung und die Aufrechterhaltung von außerpaarlichem Kopulationsverhalten bei Vögeln sind in den letzten Jahrzehnten intensiv untersucht worden. Allerdings konnte bisher kein Konsens bezüglich des adaptiven Nutzens dieses Verhaltens für Vogelweibchen erzielt werden. Die genetische Vorteile-Hypothese postuliert, dass Fremdkopulationspartner Genvarianten von höherer Qualität oder besserer Kompatibilität im Vergleich zum sozialen Paarpartner aufweisen, was zu Nachkommen von höherem Reproduktionswert führen würde. Ein häufig genutzter Ansatz zur Überprüfung dieser Hypothese besteht darin, mütterliche Halbgeschwister in Bruten mit multiplen Vaterschaften bezüglich fitness-relevanter Merkmale zu vergleichen. Die Ergebnisse solcher Vergleiche sind allerdings nicht konsistent. In diesem Beitrag diskutiere ich die Idee, dass das Ausmaß genetischer Fitnessvorteile aus Fremdkopulationen vom Umweltkontext abhängt. Kontext-abhängige genetische Effekte wurden bisher nur bei fünf Singvogelarten nachgewiesen. In keiner der betreffenden Studien wurden jedoch die entscheidenden Umweltvariablen experimentell manipuliert. Auch wurden die potentiell konfundierenden Effekte von differentiellem mütterlichen Investment in Abhängigkeit der Vaterschaft zumeist nicht kontrolliert. Eine Reihe von hochqualitativen Datensätzen zu den Fitnesskonsequenzen von Fremdkopulationsverhalten ist verfügbar, die bezüglich ihrer Umweltabhängigkeit (re-) analysiert werden könnten. Dies gilt, sofern relevante Umweltgradienten erfasst wurden und ihre Berücksichtigung a priori plausibel gemacht werden kann. Relevante Variation könnte zum Beispiel den Zeitpunkt des Brütens in gemäßigten Breiten, die Reihenfolge des Schlupfes, aber auch das Geschlecht der Nachkommen umfassen. In erster Linie sind jedoch experimentelle Ansätze nötig, die fitnessrelevante Gradienten der Umwelt wie Futterverfügbarkeit oder Parasitenbelastung systematisch und graduell variieren. Die Kontextabhängigkeit genetischer Effekte von Fremdkopulationen könnte möglicherweise erlauben, widersprüchliche Resultate verschiedener Studien innerhalb und zwischen Arten zu integrieren. Eine solche Kontextabhängigkeit könnte aber auch ganz allgemein helfen zu verstehen, unter welchen Umweltbedingungen Selektion eine weibliche Paarungspräferenz für Fremdkopulationspartner aufrechterhält. Dies hätte potenziell weit reichende Folgen für die Ökologie und Evolution von Paarungspräferenzen und die Aufrechterhaltung genetischer Variation von (sexuell) selektierten Merkmalen.



Thanks to Klaus Reinhold, Peter Korsten and Verena Dietrich-Bischoff who commented on earlier drafts of this manuscript. Thomas Friedl and an anonymous reviewer also provided helpful comments.


  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 behavior in females. Am Nat 165:S26–S37PubMedCrossRefGoogle Scholar
  3. Barber I, Arnott SA, Braithwaite VA, Andrew J, Huntingford FA (2001) Indirect fitness consequences of mate choice in sticklebacks: offspring of brighter males grow slowly but resist parasitic infections. Proc R Soc Lond B Biol Sci 268:71–76CrossRefGoogle Scholar
  4. Birkhead TR, Møller AP (1992) Sperm competition in birds: evolutionary causes and consequences. Academic Press, New YorkGoogle Scholar
  5. Bonduriansky R, Chenoweth SF (2009) Intralocus sexual conflict. Trends Ecol Evol 24:280–288PubMedCrossRefGoogle Scholar
  6. Burley N (1986) Sexual selection for aesthetic traits in species with biparental care. Am Nat 127:415–445CrossRefGoogle Scholar
  7. Bussière LF, Hunt J, Stolting KN, Jennions MD, Brooks R (2008) Mate choice for genetic quality when environments vary: suggestions for empirical progress. Genetica 134:69–78PubMedCrossRefGoogle Scholar
  8. Butler MW, Garvin JC, Wheelwright NT, Freeman-Gallant CR (2009) Ambient temperature, but not paternity, is associated with immune response in Savannah Sparrows (Passerculus sandwichensis). Auk 126:536–542CrossRefGoogle Scholar
  9. Chaine AS, Lyon BE (2008) Adaptive plasticity in female mate choice dampens sexual selection on male ornaments in the lark bunting. Science 319:459–462PubMedCrossRefGoogle Scholar
  10. Chapman JR, Nakagawa S, Coltman DW, Slate J, Sheldon BC (2009) A quantitative review of heterozygosity-fitness correlations in animal populations. Mol Ecol 18:2746–2765PubMedCrossRefGoogle Scholar
  11. Charmantier A, Garant D (2005) Environmental quality and evolutionary potential: lessons from wild populations. Proc R Soc Lond B Biol Sci 272:1415–1425CrossRefGoogle Scholar
  12. Danielson-François AM, Kelly JK, Greenfield MD (2006) Genotype × environment interaction for male attractiveness in an acoustic moth: evidence for plasticity and canalization. J Evol Biol 19:532–542PubMedCrossRefGoogle Scholar
  13. David P, Bjorksten T, Fowler K, Pomiankowski A (2000) Condition-dependent signalling of genetic variation in stalk-eyed flies. Nature 406:186–188PubMedCrossRefGoogle Scholar
  14. Dietrich V, Schmoll T, Winkel W, Epplen JT, Lubjuhn T (2004) Pair identity: an important factor concerning variation in extra-pair paternity in the coal tit (Parus ater). Behaviour 141:817–835CrossRefGoogle Scholar
  15. Dietrich-Bischoff V, Schmoll T, Winkel W, Krackow S, Lubjuhn T (2006) Extra-pair paternity, offspring mortality and offspring sex ratio in the socially monogamous coal tit (Parus ater). Behav Ecol Sociobiol 60:563–571CrossRefGoogle Scholar
  16. Dunn PO, Lifjeld JT, Whittingham LA (2009) Multiple paternity and offspring quality in tree swallows. Behav Ecol Sociobiol 63:911–922CrossRefGoogle Scholar
  17. Edler R, Friedl TWP (2008) Within-pair young are more immunocompetent than extrapair young in mixed-paternity broods of the red bishop. Anim Behav 75:391–401CrossRefGoogle Scholar
  18. Edly-Wright C, Schwagmeyer PL, Parker PG, Mock DW (2007) Genetic similarity of mates, offspring health and extrapair fertilization in house sparrows. Anim Behav 73:367–378CrossRefGoogle Scholar
  19. Ellegren H, Gustafsson L, Sheldon BC (1996) Sex ratio adjustment in relation to paternal attractiveness in a wild bird population. Proc Natl Acad Sci USA 93:11723–11728PubMedCrossRefGoogle Scholar
  20. Ferree ED, Dickinson J, Rendell W, Stern C, Porter S (2010) Hatching order explains an extrapair chick advantage in western bluebirds. Behav Ecol 21:802–807CrossRefGoogle Scholar
  21. Foerster K, Delhey K, Johnsen A, Lifjeld JT, Kempenaers B (2003) Females increase offspring heterozygosity and fitness through extra-pair matings. Nature 425:714–717PubMedCrossRefGoogle Scholar
  22. Forsman AM, Vogel LA, Sakaluk SK, Johnson BG, Masters BS, Johnson LS, Thompson CF (2008) Female house wrens (Troglodytes aedon) increase the size, but not immunocompetence, of their offspring through extra-pair mating. Mol Ecol 17:3697–3706PubMedCrossRefGoogle Scholar
  23. Fossøy F, Johnsen A, Lifjeld JT (2008) Multiple genetic benefits of female promiscuity in a socially monogamous passerine. Evolution 62:145–156PubMedCrossRefGoogle Scholar
  24. Fox CW, Reed DH (2011) Inbreeding depression increases with environmental stress: an experimental study and meta-analysis. Evolution 65:246–258PubMedCrossRefGoogle Scholar
  25. Friedl TWP, Klump GM (2005) Extrapair fertilizations in red bishops (Euplectes orix): do females follow conditional extrapair strategies? Auk 122:57–70CrossRefGoogle Scholar
  26. Garvin JC, Abroe B, Pedersen MC, Dunn PO, Whittingham LA (2006) Immune response of nestling warblers varies with extra-pair paternity and temperature. Mol Ecol 15:3833–3840PubMedCrossRefGoogle Scholar
  27. Greenfield MD, Rodriguez RL (2004) Genotype-environment interaction and the reliability of mating signals. Anim Behav 68:1461–1468CrossRefGoogle Scholar
  28. Griffith SC (2007) The evolution of infidelity in socially monogamous passerines: neglected components of direct and indirect selection. Am Nat 169:274–281PubMedCrossRefGoogle Scholar
  29. Griffith SC, Immler S (2009) Female infidelity and genetic compatibility in birds: the role of the genetically loaded raffle in understanding the function of extrapair paternity. J Avian Biol 40:97–101CrossRefGoogle Scholar
  30. 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
  31. Griffith SC, Holleley CE, Mariette MM, Pryke SR, Svedin N (2010) Low level of extrapair parentage in wild zebra finches. Anim Behav 79:261–264CrossRefGoogle Scholar
  32. Hoffmann AA, Merilä J (1999) Heritable variation and evolution under favourable and unfavourable conditions. Trends Ecol Evol 14:96–101PubMedCrossRefGoogle Scholar
  33. Ingleby FC, Hunt J, Hosken DJ (2010) The role of genotype-by-environment interactions in sexual selection. J Evol Biol 23:2031–2045PubMedCrossRefGoogle Scholar
  34. Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64PubMedCrossRefGoogle Scholar
  35. Jia FY, Greenfield MD (1997) When are good genes good? Variable outcomes of female choice in wax moths. Proc R Soc Lond B Biol Sci 264:1057–1063CrossRefGoogle Scholar
  36. Jia FY, Greenfield MD, Collins RD (2000) Genetic variance of sexually selected traits in waxmoths: maintenance by genotype × environment interaction. Evolution 54:953–967PubMedGoogle Scholar
  37. Johnsen A, Andersen V, Sunding C, Lifjeld JT (2000) Female bluethroats enhance offspring immunocompetence through extra-pair copulations. Nature 406:296–299PubMedCrossRefGoogle Scholar
  38. Johnson LS, Thompson CF, Sakaluk SK, Neuhäuser M, Johnson BGP, Soukup SS, Forsythe SJ, Masters BS (2009) Extra-pair young in house wren broods are more likely to be male than female. Proc R Soc Lond B Biol Sci 276:2285–2289CrossRefGoogle Scholar
  39. Keller LF (1998) Inbreeding and its fitness effects in an insular population of song sparrows (Melospiza melodia). Evolution 52:240–250CrossRefGoogle Scholar
  40. Keller LF, Grant PR, Grant BR, Petren K (2002) Environmental conditions affect the magnitude of inbreeding depression in survival of Darwin’s finches. Evolution 56:1229–1239PubMedGoogle Scholar
  41. Kempenaers B (2007) Mate choice and genetic quality: a review of the heterozygosity theory. Adv Stud Behav 37:189–278CrossRefGoogle Scholar
  42. Kirkpatrick M, Barton NH (1997) The strength of indirect selection on female mating preferences. Proc Natl Acad Sci USA 94:1282–1286PubMedCrossRefGoogle Scholar
  43. Kleven O, Lifjeld JT (2004) Extra-pair paternity and offspring immunocompetence in the reed bunting (Emberiza schoeniclus). Anim Behav 68:283–289CrossRefGoogle Scholar
  44. Kleven O, Jacobsen F, Izadnegahdar R, Robertson RJ, Lifjeld JT (2006) No evidence of paternal genetic contribution to nestling cell-mediated immunity in the North American barn swallow. Anim Behav 71:839–845CrossRefGoogle Scholar
  45. Kruuk LEB, Sheldon BC, Merilä J (2002) Severe inbreeding depression in collared flycatchers (Ficedula albicollis). Proc R Soc Lond B Biol Sci 269:1581–1589CrossRefGoogle Scholar
  46. Leech DI, Hartley IR, Stewart IRK, Griffith SC, Burke T (2001) No effect of parental quality or extrapair paternity on brood sex ratio in the blue tit (Parus caeruleus). Behav Ecol 12:674–680CrossRefGoogle Scholar
  47. Lesbarrères D, Primmer CR, Laurila A, Merilä J (2005) Environmental and population dependency of genetic variability-fitness correlations in Rana temporaria. Mol Ecol 14:311–323PubMedCrossRefGoogle Scholar
  48. Lindén M, Gustafsson L, Pärt T (1992) Selection on fledging mass in collared flycatchers and great tits. Ecology 73:336–343CrossRefGoogle Scholar
  49. Lubjuhn T, Strohbach S, Brün J, Gerken T, Epplen JT (1999) Extra-pair paternity in great tits (Parus major): a long term study. Behaviour 136:1157–1172CrossRefGoogle Scholar
  50. Magrath RD (1990) Hatching asynchrony in altricial birds. Biol Rev 65:587–622CrossRefGoogle Scholar
  51. Magrath MJL, Vedder O, van der Velde M, Komdeur J (2009) Maternal effects contribute to the superior performance of extra-pair offspring. Curr Biol 19:792–797PubMedCrossRefGoogle Scholar
  52. Marr AB, Arcese P, Hochachka WM, Reid JM, Keller LF (2006) Interactive effects of environmental stress and inbreeding on reproductive traits in a wild bird population. J Anim Ecol 75:1406–1415PubMedCrossRefGoogle Scholar
  53. Mays HL, Hill GE (2004) Choosing mates: good genes versus genes that are a good fit. Trends Ecol Evol 19:554–559PubMedCrossRefGoogle Scholar
  54. Mills SC, Alatalo RV, Koskela E, Mappes J, Mappes T, Oksanen TA (2007) Signal reliability compromised by genotype-by-environment interaction and potential mechanisms for its preservation. Evolution 61:1748–1757PubMedCrossRefGoogle Scholar
  55. Møller AP, Alatalo RV (1999) Good-genes effects in sexual selection. Proc R Soc Lond B Biol Sci 266:85–91CrossRefGoogle Scholar
  56. Møller AP, Thornhill R (1998) Male parental care, differential parental investment by females and sexual selection. Anim Behav 55:1507–1515PubMedCrossRefGoogle Scholar
  57. Mousseau TA, Fox CW (1998) The adaptive significance of maternal effects. Trends Ecol Evol 13:403–407PubMedCrossRefGoogle Scholar
  58. 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
  59. O’Brien EL, Dawson RD (2007) Context-dependent genetic benefits of extra-pair mate choice in a socially monogamous passerine. Behav Ecol Sociobiol 61:775–782CrossRefGoogle Scholar
  60. Petrie M (1994) Improved growth and survival of offspring of peacocks with more elaborate trains. Nature 371:598–599CrossRefGoogle Scholar
  61. Petrie M, Kempenaers B (1998) Extra-pair paternity in birds: explaining variation between species and populations. Trends Ecol Evol 13:52–58PubMedCrossRefGoogle Scholar
  62. Pryke SR, Griffith SC (2009) Genetic incompatibility drives sex allocation and maternal investment in a polymorphic finch. Science 323:1605–1607PubMedCrossRefGoogle Scholar
  63. Qvarnström A (1999) Genotype-by-environment interactions in the determination of the size of a secondary sexual character in the collared flycatcher (Ficedula albicollis). Evolution 53:1564–1572CrossRefGoogle Scholar
  64. Qvarnström A (2001) Context-dependent genetic benefits from mate choice. Trends Ecol Evol 16:5–7PubMedCrossRefGoogle Scholar
  65. Qvarnström A, Pärt T, Sheldon BC (2000) Adaptive plasticity in mate preference linked to differences in reproductive effort. Nature 405:344–347PubMedCrossRefGoogle Scholar
  66. Rosivall B, Szöllösi E, Hasselquist D, Török J (2009) Effects of extrapair paternity and sex on nestling growth and condition in the collared flycatcher, Ficedula albicollis. Anim Behav 77:611–617CrossRefGoogle Scholar
  67. Schmoll T, Dietrich V, Winkel W, Epplen JT, Lubjuhn T (2003) Long-term fitness consequences of female extra-pair matings in a socially monogamous passerine. Proc R Soc Lond B Biol Sci 270:259–264CrossRefGoogle Scholar
  68. Schmoll T, Dietrich V, Winkel W, Epplen JT, Schurr F, Lubjuhn T (2005) Paternal genetic effects on offspring fitness are context dependent within the extrapair mating system of a socially monogamous passerine. Evolution 59:645–657PubMedGoogle Scholar
  69. Schmoll T, Schurr FM, Winkel W, Epplen JT, Lubjuhn T (2007) Polyandry in coal tits Parus ater: fitness consequences of putting eggs into multiple genetic baskets. J Evol Biol 20:1115–1125PubMedCrossRefGoogle Scholar
  70. Schmoll T, Schurr FM, Winkel W, Epplen JT, Lubjuhn T (2009) Lifespan, lifetime reproductive performance and paternity loss of within-pair and extra-pair offspring in the coal tit Periparus ater. Proc R Soc Lond B Biol Sci 276:337–345CrossRefGoogle Scholar
  71. Sheldon BC (2000) Differential allocation: tests, mechanisms and implications. Trends Ecol Evol 15:397–402PubMedCrossRefGoogle Scholar
  72. Sheldon BC, Ellegren H (1996) Offspring sex and paternity in the collared flycatcher. Proc R Soc Lond B Biol Sci 263:1017–1021CrossRefGoogle Scholar
  73. Sheldon BC, Merilä J, Qvarnström A, Gustafsson L, Ellegren H (1997) Paternal genetic contribution to offspring condition predicted by size of male secondary sexual character. Proc R Soc Lond B Biol Sci 264:297–302CrossRefGoogle Scholar
  74. Sheldon BC, Arponen H, Laurila A, Crochet PA, Merilä J (2003) Sire coloration influences offspring survival under predation risk in the moorfrog. J Evol Biol 16:1288–1295PubMedCrossRefGoogle Scholar
  75. Stapleton MK, Kleven O, Lifjeld JT, Robertson RJ (2007) Female tree swallows (Tachycineta bicolor) increase offspring heterozygosity through extrapair mating. Behav Ecol Sociobiol 61:1725–1733CrossRefGoogle Scholar
  76. Strohbach S, Curio E, Bathen A, Epplen JT, Lubjuhn T (1998) Extrapair paternity in the great tit (Parus major): a test of the “good genes” hypothesis. Behav Ecol 9:388–396CrossRefGoogle Scholar
  77. Suter SM, Keiser M, Feignoux R, Meyer DR (2007) Reed bunting females increase fitness through extra-pair mating with genetically dissimilar males. Proc R Soc Lond B Biol Sci 274:2865–2871CrossRefGoogle Scholar
  78. Szulkin M, Sheldon BC (2007) The environmental dependence of inbreeding depression in a wild bird population. PLoS ONE 2:e1027, 1–7Google Scholar
  79. Van de Casteele T, Galbusera P, Schenck T, Matthysen E (2003) Seasonal and lifetime reproductive consequences of inbreeding in the great tit Parus major. Behav Ecol 14:165–174CrossRefGoogle Scholar
  80. Veen T, Borge T, Griffith SC, Saetre GP, Bures S, Gustafsson L, Sheldon BC (2001) Hybridization and adaptive mate choice in flycatchers. Nature 411:45–50PubMedCrossRefGoogle Scholar
  81. Welch AM (2003) Genetic benefits of a female mating preference in gray tree frogs are context-dependent. Evolution 57:883–893PubMedGoogle Scholar
  82. Westneat DF, Stewart IRK (2003) Extra-pair paternity in birds: causes, correlates, and conflict. Annu Rev Ecol Evol Syst 34:365–396CrossRefGoogle Scholar
  83. Westneat DF, Sherman PW, Morton WL (1990) The ecology and evolution of extra-pair copulations in birds. In: Power DM (ed) Current ornithology, vol 7. Plenum Press, New York, pp 331–369Google Scholar
  84. Wetzel DP, Westneat DF (2009) Heterozygosity and extra-pair paternity: biased tests result from the use of shared markers. Mol Ecol 18:2010–2021PubMedCrossRefGoogle Scholar
  85. Whittingham LA, Dunn PO (2001) Survival of extrapair and within-pair young in tree swallows. Behav Ecol 12:496–500CrossRefGoogle Scholar
  86. Wilk T, Cichon M, Wolff K (2008) Lack of evidence for improved immune response of extra-pair nestlings in collared flycatcher Ficedula albicollis. J Avian Biol 39:546–552CrossRefGoogle Scholar
  87. Yasui Y (1998) The ‘genetic benefits’ of female multiple mating reconsidered. Trends Ecol Evol 13:246–250PubMedCrossRefGoogle Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2011

Authors and Affiliations

  1. 1.Evolutionary BiologyUniversity of BielefeldBielefeldGermany
  2. 2.Institute of Evolutionary Biology, Ashworth LaboritoriesThe University of EdinburghEdinburghUK

Personalised recommendations