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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 Schmoll
Review

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.

Keywords

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

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.

Notes

Acknowledgements

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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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

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