Quantifying inbreeding avoidance through extra‐pair reproduction

Jane M Reid,A Bradley Duthie,Lukas F Keller,Peter Arcese,Matthew E Wolak,Pirmin Nietlisbach,Sylvain Losdat,Ryan R Germain

doi:10.1111/evo.12557

Abstract

Extra-pair reproduction is widely hypothesized to allow females to avoid inbreeding with related socially paired males. Consequently, numerous field studies have tested the key predictions that extra-pair offspring are less inbred than females’ alternative within-pair offspring, and that the probability of extra-pair reproduction increases with a female's relatedness to her socially paired male. However, such studies rarely measure inbreeding or relatedness sufficiently precisely to detect subtle effects, or consider biases stemming from failure to observe inbred offspring that die during early development. Analyses of multigenerational song sparrow (Melospiza melodia) pedigree data showed that most females had opportunity to increase or decrease the coefficient of inbreeding of their offspring through extra-pair reproduction with neighboring males. In practice, observed extra-pair offspring had lower inbreeding coefficients than females’ within-pair offspring on average, while the probability of extra-pair reproduction increased substantially with the coefficient of kinship between a female and her socially paired male. However, simulations showed that such effects could simply reflect bias stemming from inbreeding depression in early offspring survival. The null hypothesis that extra-pair reproduction is random with respect to kinship therefore cannot be definitively rejected in song sparrows, and existing general evidence that females avoid inbreeding through extra-pair reproduction requires reevaluation given such biases.

Highlights

The null hypothesis that extra-pair reproduction is random with respect to kinship cannot be definitively rejected in song sparrows, and existing general evidence that females avoid inbreeding through extra-pair reproduction requires reevaluation given such biases
STUDY SYSTEM AND PEDIGREE The hypothesis that females systematically alter their relatedness to the sire of their offspring through extra-pair reproduction is most appropriately tested in socially monogamous populations where females encounter a diversity of close, distant and nonrelatives as potential social and extra-pair mates, and where such variation is likely to have existed across sufficient generations for associated inbreeding strategies to have evolved (Szulkin et al 2013)
The difference in k between a female and her socially paired versus extra-pair male was calculated as kDIFF = kEP – kinship with her socially paired male (kSOC)

Summary

Introduction

Extra-pair reproduction, and polyandry more generally, are widely hypothesized to have evolved to allow females to avoid inbreeding with related socially paired or previously mated males, thereby circumventing constraints on initial mate choice (Jennions and Petrie 2000; Tregenza and Wedell 2000; Griffith et al 2002; Kempenaers 2007; Firman and Simmons 2008; Griffith and Immler 2009). Through extra-pair reproduction; second, that observed changes in relatedness differ from those expected under some null model of random extra-pair reproduction and constitute active inbreeding avoidance or preference defined as negative or positive deviations from null expectation; and third, that the probability of extra-pair reproduction varies with a female’s relatedness to her socially paired male (e.g., Blomqvist et al 2002; Foerster et al 2003; Tarvin et al 2005; Suter et al 2007; Cohas et al 2008; Brouwer et al 2011; Wang and Lu 2011; Varian-Ramos and Webster 2012; Harrison et al 2013; Kingma et al 2013; Leclaire et al 2013). Apparent diversity might arise because such relationships are extremely challenging to quantify in wild populations, meaning that estimates might be subject to substantial sampling variance and divergent bias

Methods

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Discussion

Conclusion