Genetic similarity between mates predicts extrapair paternity—a meta-analysis of bird studies

Arct, Aneta; Drobniak, Szymon M.; Cichoń, Mariusz

doi:10.1093/beheco/arv004

Cited by 94 publications

(107 citation statements)

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“…The question of why females are unfaithful in socially monogamous species is currently the subject of a vibrant debate (Forstmeier et al 2014;Arct et al 2015;Drobniak et al 2015;Forstmeier 2015;Griffith 2015;Nakagawa et al 2015;Reid 2015). The theoretical predictions for female infidelity are clear: females are expected to gain indirect fitness benefits through higher genetic quality of the extrapair male, better genetic compatibility with the extrapair male in comparison to the social mate, or fertility insurance (Griffith et al 2002;Akçay and Roughgarden 2007).…”

Section: Introductionmentioning

confidence: 99%

“…Despite these theories, the empirical evidence for indirect benefits is conflicting (e.g., Møller and Alatalo 1999;Arnqvist and Kirkpatrick 2005;Rosivall et al 2009;Hsu et al 2014;Bowers et al 2015). Meta-analyses have also provided conflicting results for whether females gain fitness benefits from having extrapair offspring (EPO; Akçay and Roughgarden 2007;Arct et al 2015) and even suggest that female infidelity is costly (Hsu et al 2015). To further our understanding of the evolution of female polygamy, it is crucial to understand not only the benefits but also the costs of females producing EPO .…”

Section: Introductionmentioning

confidence: 99%

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Predictably Philandering Females Prompt Poor Paternal Provisioning

Schroeder

Hsu

Winney

et al. 2016

The American Naturalist

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Dryad data: http://dx.doi.org/10.5061/dryad.0t313.abstract: One predicted cost of female infidelity in socially monogamous species is that cuckolded males should provide less parental care. This relationship is robust across species, but evidence is ambiguous within species. We do not know whether individual males reduce their care when paired with cheating females compared with when paired with faithful females (within-male adjustment) or, alternatively, if the males that pair with cheating females are the same males that provide less parental care in general (between-male effect). Our exceptionally extensive long-term data set of repeated observations of a wild passerine allows us to disentangle paternal care adjustment within males-within pairs and between males-while accounting for environmental variables. We found a within-male adjustment of paternal provisioning, but not incubation effort, relative to the cuckoldry in their nest. This effect was mainly driven by females differing consistently in their fidelity. There was no evidence that this within-male adjustment also took place across broods with the same female, and we found no between-male effect. Interestingly, males that gained more extrapair paternity provided less care. Data from a cross-foster experiment suggested that males did not use kin recognition to assess paternity. Our results provide insight into the role of individual variation in parental care and mating systems.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Predictably Philandering Females Prompt Poor Paternal Provisioning

Schroeder

Hsu

Winney

et al. 2016

The American Naturalist

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“…Although the compatible genes hypothesis is emerging as an important component of EPP through its influence on offspring viability (Blomqvist et al, 2002;Masters et al, 2003;Richardson et al, 2005;Dowling and Mulder, 2006;Freeman-Gallant et al, 2006;Cohas et al, 2007;Rubenstein, 2007;Brouwer et al, 2011;Arct et al, 2015) the exact selective mechanism through which it acts remains unclear (reviewed in Griffith and Immler, 2009). Potential mechanisms can arise through pre-or post-copulatory (i.e., cryptic female choice; Eberhard, 1991;Colegrave et al, 2002;Birkhead and Pizzari, 2002) mate choice, or through sperm selection in which the sperm of more compatible males are more likely to fertilize an egg (Wilson et al, 1997;Zeh and Zeh, 1997;Birkhead and Møller, 1998;Tregenza and Wedell, 2000).…”

Section: Introductionmentioning

confidence: 99%

Population Social Structure Facilitates Indirect Fitness Benefits from Extra-Pair Mating

Wells

Gleeson

et al. 2017

Front. Ecol. Evol.

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Despite decades of research, empirical support for the "compatible genes" and "good genes" hypotheses as explanations for adaptive female extra-pair mating remains discordant. One largely un-tested theoretical prediction that could explain equivocal findings is that mating for compatible genes benefits should reduce selection for good genes. However, this prediction does not consider demographic parameters, such as social structuring, that can indirectly influence extra-pair paternity (EPP) outcomes. Drawing on evidence from a previous study, we re-evaluate this hypothesis whilst considering social structuring in a population of tui, Prosthemadera novaeseelandiae, a socially monogamous passerine. Previous research has found possible evidence for mating for good genes because male ornament size correlates with EPP success in this population. Here, we test whether non-random inbreeding of social-pairs indirectly provides the opportunity to gain compatibility benefits from EPP, and thus whether selection for compatible genes and good genes can operate simultaneously. We found that (1) social mates were more closely related than expected through random mating, (2) extra-pair males (EPMs) were less closely related to females than were the females' within-pair mates, and (3) genetically dissimilar males sired offspring with faster growth rates. These results demonstrate that females gain compatible genes benefits from EPP. However, contrary to the compatible genes hypothesis, females in highly-related pairs did not engage more frequently in extra-pair mating. Together with previous research investigating female mate choice in this population, our findings suggest that social pairings between relatives provide a pathway for females to gain compatible genes benefits whilst engaging in extra-pair mating for good genes. This study provides evidence that some fitness benefits from EPP arise automatically through non-random social mating rather than through direct selection on extra-pair mate choice. We argue that when variance in compatibility benefits is an outcome of population structuring, compatible genes benefits need not be gained at the expense of good genes benefits.

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“…For example, one main GCH prediction is that the incidence of EP young should increase with increasing social pair relatedness (genetic similarity). Using the 23 relevant studies published at the time, Akçay and Roughgarden (2007) found the overall effect to be non-significant, while Arct et al (2015), using an updated database of 39…”

Section: Introductionmentioning

confidence: 99%

No evidence that genetic compatibility drives extra‐pair behavior in female blue‐footed boobies

Kiere¹,

Ramos²,

Drummond³

2016

Journal of Avian Biology

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The function of female birds' extra-pair (EP) behavior has remained an unresolved question in ornithology and behavioral ecology for >30 years. The genetic compatibility hypothesis (GCH) proposes that females benefit by acquiring biological sires that yield more heterozygous, and therefore fitter, offspring than their social mates. We used ten polymorphic microsatellite loci to test GCH predictions and its assumption that fitness increases with heterozygosity in blue-footed boobies (Sula nebouxii), a long-lived tropical seabird. Our predictions were not supported. Heterozygosity was uncorrelated with quality indicators (fledging probability, fledgling or adult body size or mass, adult ornamentation, mean breeding success). Females were no more likely to have EP behavior or chicks when their social mates were less heterozygous or compatible, nor were EP males more heterozygous or compatible than the males they cuckolded. Finally, EP chicks were no more heterozygous than within-pair chicks overall or in half-sib comparisons, nor were within-pair chicks from all-within-pair nests more heterozygous that those with EP nestmates. There are both methodological and biological explanations for these consistently negative results. Inadequate sample size is possible but unlikely, since our samples were comparable or larger than those of similar studies with significant findings. Lack of identity disequilibrium (within-individual heterozygosity correlation) among our marker loci could be responsible, and suggests either insufficient marker coverage or lack of inbreeding, bottleneck, and/or admixture. An independent social pedigree revealed infrequent inbreeding, suggesting that pressure on females to select sires that maximize offspring heterozygosity may be genuinely lax. Alternatively, it is possible that the GCH is only upheld when selection on young is strongest; this would not be detected in our sample, which was taken during an extremely productive year. Whatever their cause, our results Accepted Ar ticle'This article is protected by copyright. All rights reserved.' expand the taxonomic breadth of avian EP behavior analyses and should be considered in future evaluations of the GCH.

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Genetic similarity between mates predicts extrapair paternity—a meta-analysis of bird studies

Cited by 94 publications

References 99 publications

Predictably Philandering Females Prompt Poor Paternal Provisioning

Predictably Philandering Females Prompt Poor Paternal Provisioning

Population Social Structure Facilitates Indirect Fitness Benefits from Extra-Pair Mating

No evidence that genetic compatibility drives extra‐pair behavior in female blue‐footed boobies

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