Quantifying inbreeding avoidance through extra‐pair reproduction

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.

Pedigree-based inbreeding coefficient explains more variation in fitness than heterozygosity at 160 microsatellites in a wild bird population

“…Additionally, blood sampling of all individuals at approximately 6 days after hatching since 1993 allows correcting the pedigree for extra-pair paternities and determining the sex [37][38][39][40][41]. F was calculated using the R package pedigreemm [42] for individuals with at least two (and a mean of eight) genetically verified ancestral generations plus earlier genetically not verified generations.…”

The Consequences of Polyandry for Sibship Structures, Distributions of Relationships and Relatedness, and Potential for Inbreeding in a Wild Population

“…Specifically, previous analyses showed substantial variance in relatedness and associated opportunity for inbreeding and inbreeding avoidance . However, comparisons of observed relatedness among mates with that expected given random mating revealed little evidence of active inbreeding avoidance through nonrandom social pairing (Keller and Arcese 1998;Reid et al 2006) or through nonrandom extrapair reproduction (Reid et al 2015a(Reid et al , 2015b. This is despite evidence of strong inbreeding depression in fitness (Keller 1998;Reid et al 2014;Nietlisbach et al 2017).…”

“…We first compiled a social pedigree linking all banded offspring to their observed mother and her socially paired male spanning 1975-2015 (Reid et al 2014(Reid et al , 2015a(Reid et al , 2015b. Since 1993, all adults and banded offspring were blood sampled and genotyped at ∼160 highly polymorphic microsatellite loci, and all offspring were assigned to genetic sires with 199% individual-level statistical confidence (Nietlisbach et al 2015(Nietlisbach et al , 2017Reid et al 2015a). We then compiled a genetic pedigree linking all banded offspring to their mother and true genetic father (Sardell et al 2010;Reid et al 2014Reid et al , 2015aReid et al , 2015bNietlisbach et al 2015).…”

“…Since 1993, all adults and banded offspring were blood sampled and genotyped at ∼160 highly polymorphic microsatellite loci, and all offspring were assigned to genetic sires with 199% individual-level statistical confidence (Nietlisbach et al 2015(Nietlisbach et al , 2017Reid et al 2015a). We then compiled a genetic pedigree linking all banded offspring to their mother and true genetic father (Sardell et al 2010;Reid et al 2014Reid et al , 2015aReid et al , 2015bNietlisbach et al 2015). We thereby generated two parallel pedigrees spanning 1993-2015 that describe sibship structures and the distributions of relationships and relatedness among all population members as they would have been had all observed breeding pairs been monogamous within broods (social pedigree) and given the realized pattern of extrapair reproduction and underlying polyandry (genetic pedigree; Lebigre et al 2012;Reid et al 2014).…”

“…To maximize use of all available pedigree data and relax the alternative assumption that all 1993 breeders are unrelated, we grafted each of the 1993-2015 social and genetic pedigrees onto the basal 1975-1992 social pedigree (Reid et al 2014(Reid et al , 2015a. To minimize error in estimates of relationships and relatedness stemming from inadequate pedigree depth and/or remaining paternity error for some individuals hatched during 1975-1992, we restricted analyses to adults alive during 2008-2015.…”