Abstract
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.
Zusammenfassung
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.
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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
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–S37
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 268:71–76
Birkhead TR, Møller AP (1992) Sperm competition in birds: evolutionary causes and consequences. Academic Press, New York
Bonduriansky R, Chenoweth SF (2009) Intralocus sexual conflict. Trends Ecol Evol 24:280–288
Burley N (1986) Sexual selection for aesthetic traits in species with biparental care. Am Nat 127:415–445
Bussière LF, Hunt J, Stolting KN, Jennions MD, Brooks R (2008) Mate choice for genetic quality when environments vary: suggestions for empirical progress. Genetica 134:69–78
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 126:536–542
Chaine AS, Lyon BE (2008) Adaptive plasticity in female mate choice dampens sexual selection on male ornaments in the lark bunting. Science 319:459–462
Chapman JR, Nakagawa S, Coltman DW, Slate J, Sheldon BC (2009) A quantitative review of heterozygosity-fitness correlations in animal populations. Mol Ecol 18:2746–2765
Charmantier A, Garant D (2005) Environmental quality and evolutionary potential: lessons from wild populations. Proc R Soc Lond B Biol Sci 272:1415–1425
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 19:532–542
David P, Bjorksten T, Fowler K, Pomiankowski A (2000) Condition-dependent signalling of genetic variation in stalk-eyed flies. Nature 406:186–188
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 141:817–835
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 60:563–571
Dunn PO, Lifjeld JT, Whittingham LA (2009) Multiple paternity and offspring quality in tree swallows. Behav Ecol Sociobiol 63:911–922
Edler R, Friedl TWP (2008) Within-pair young are more immunocompetent than extrapair young in mixed-paternity broods of the red bishop. Anim Behav 75:391–401
Edly-Wright C, Schwagmeyer PL, Parker PG, Mock DW (2007) Genetic similarity of mates, offspring health and extrapair fertilization in house sparrows. Anim Behav 73:367–378
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 93:11723–11728
Ferree ED, Dickinson J, Rendell W, Stern C, Porter S (2010) Hatching order explains an extrapair chick advantage in western bluebirds. Behav Ecol 21:802–807
Foerster K, Delhey K, Johnsen A, Lifjeld JT, Kempenaers B (2003) Females increase offspring heterozygosity and fitness through extra-pair matings. Nature 425:714–717
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 17:3697–3706
Fossøy F, Johnsen A, Lifjeld JT (2008) Multiple genetic benefits of female promiscuity in a socially monogamous passerine. Evolution 62:145–156
Fox CW, Reed DH (2011) Inbreeding depression increases with environmental stress: an experimental study and meta-analysis. Evolution 65:246–258
Friedl TWP, Klump GM (2005) Extrapair fertilizations in red bishops (Euplectes orix): do females follow conditional extrapair strategies? Auk 122:57–70
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 15:3833–3840
Greenfield MD, Rodriguez RL (2004) Genotype-environment interaction and the reliability of mating signals. Anim Behav 68:1461–1468
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, 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 40:97–101
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
Griffith SC, Holleley CE, Mariette MM, Pryke SR, Svedin N (2010) Low level of extrapair parentage in wild zebra finches. Anim Behav 79:261–264
Hoffmann AA, Merilä J (1999) Heritable variation and evolution under favourable and unfavourable conditions. Trends Ecol Evol 14:96–101
Ingleby FC, Hunt J, Hosken DJ (2010) The role of genotype-by-environment interactions in sexual selection. J Evol Biol 23:2031–2045
Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64
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 264:1057–1063
Jia FY, Greenfield MD, Collins RD (2000) Genetic variance of sexually selected traits in waxmoths: maintenance by genotype × environment interaction. Evolution 54:953–967
Johnsen A, Andersen V, Sunding C, Lifjeld JT (2000) Female bluethroats enhance offspring immunocompetence through extra-pair copulations. Nature 406:296–299
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 276:2285–2289
Keller LF (1998) Inbreeding and its fitness effects in an insular population of song sparrows (Melospiza melodia). Evolution 52:240–250
Keller LF, Grant PR, Grant BR, Petren K (2002) Environmental conditions affect the magnitude of inbreeding depression in survival of Darwin’s finches. Evolution 56:1229–1239
Kempenaers B (2007) Mate choice and genetic quality: a review of the heterozygosity theory. Adv Stud Behav 37:189–278
Kirkpatrick M, Barton NH (1997) The strength of indirect selection on female mating preferences. Proc Natl Acad Sci USA 94:1282–1286
Kleven O, Lifjeld JT (2004) Extra-pair paternity and offspring immunocompetence in the reed bunting (Emberiza schoeniclus). Anim Behav 68:283–289
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 71:839–845
Kruuk LEB, Sheldon BC, Merilä J (2002) Severe inbreeding depression in collared flycatchers (Ficedula albicollis). Proc R Soc Lond B Biol Sci 269:1581–1589
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 12:674–680
Lesbarrères D, Primmer CR, Laurila A, Merilä J (2005) Environmental and population dependency of genetic variability-fitness correlations in Rana temporaria. Mol Ecol 14:311–323
Lindén M, Gustafsson L, Pärt T (1992) Selection on fledging mass in collared flycatchers and great tits. Ecology 73:336–343
Lubjuhn T, Strohbach S, Brün J, Gerken T, Epplen JT (1999) Extra-pair paternity in great tits (Parus major): a long term study. Behaviour 136:1157–1172
Magrath RD (1990) Hatching asynchrony in altricial birds. Biol Rev 65:587–622
Magrath MJL, Vedder O, van der Velde M, Komdeur J (2009) Maternal effects contribute to the superior performance of extra-pair offspring. Curr Biol 19:792–797
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 75:1406–1415
Mays HL, Hill GE (2004) Choosing mates: good genes versus genes that are a good fit. Trends Ecol Evol 19:554–559
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 61:1748–1757
Møller AP, Alatalo RV (1999) Good-genes effects in sexual selection. Proc R Soc Lond B Biol Sci 266:85–91
Møller AP, Thornhill R (1998) Male parental care, differential parental investment by females and sexual selection. Anim Behav 55:1507–1515
Mousseau TA, Fox CW (1998) The adaptive significance of maternal effects. Trends Ecol Evol 13:403–407
Neff BD, Pitcher TE (2005) Genetic quality and sexual selection: an integrated framework for good genes and compatible genes. Mol Ecol 14:19–38
O’Brien EL, Dawson RD (2007) Context-dependent genetic benefits of extra-pair mate choice in a socially monogamous passerine. Behav Ecol Sociobiol 61:775–782
Petrie M (1994) Improved growth and survival of offspring of peacocks with more elaborate trains. Nature 371:598–599
Petrie M, Kempenaers B (1998) Extra-pair paternity in birds: explaining variation between species and populations. Trends Ecol Evol 13:52–58
Pryke SR, Griffith SC (2009) Genetic incompatibility drives sex allocation and maternal investment in a polymorphic finch. Science 323:1605–1607
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 53:1564–1572
Qvarnström A (2001) Context-dependent genetic benefits from mate choice. Trends Ecol Evol 16:5–7
Qvarnström A, Pärt T, Sheldon BC (2000) Adaptive plasticity in mate preference linked to differences in reproductive effort. Nature 405:344–347
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 77:611–617
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 270:259–264
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 59:645–657
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 20:1115–1125
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 276:337–345
Sheldon BC (2000) Differential allocation: tests, mechanisms and implications. Trends Ecol Evol 15:397–402
Sheldon BC, Ellegren H (1996) Offspring sex and paternity in the collared flycatcher. Proc R Soc Lond B Biol Sci 263:1017–1021
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 264:297–302
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 16:1288–1295
Stapleton MK, Kleven O, Lifjeld JT, Robertson RJ (2007) Female tree swallows (Tachycineta bicolor) increase offspring heterozygosity through extrapair mating. Behav Ecol Sociobiol 61:1725–1733
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 9:388–396
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 274:2865–2871
Szulkin M, Sheldon BC (2007) The environmental dependence of inbreeding depression in a wild bird population. PLoS ONE 2:e1027, 1–7
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 14:165–174
Veen T, Borge T, Griffith SC, Saetre GP, Bures S, Gustafsson L, Sheldon BC (2001) Hybridization and adaptive mate choice in flycatchers. Nature 411:45–50
Welch AM (2003) Genetic benefits of a female mating preference in gray tree frogs are context-dependent. Evolution 57:883–893
Westneat DF, Stewart IRK (2003) Extra-pair paternity in birds: causes, correlates, and conflict. Annu Rev Ecol Evol Syst 34:365–396
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 331–369
Wetzel DP, Westneat DF (2009) Heterozygosity and extra-pair paternity: biased tests result from the use of shared markers. Mol Ecol 18:2010–2021
Whittingham LA, Dunn PO (2001) Survival of extrapair and within-pair young in tree swallows. Behav Ecol 12:496–500
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 39:546–552
Yasui Y (1998) The ‘genetic benefits’ of female multiple mating reconsidered. Trends Ecol Evol 13:246–250
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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.
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Schmoll, T. A review and perspective on context-dependent genetic effects of extra-pair mating in birds. J Ornithol 152 (Suppl 1), 265–277 (2011). https://doi.org/10.1007/s10336-011-0683-4
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DOI: https://doi.org/10.1007/s10336-011-0683-4