Variation in parent-offspring kinship in socially monogamous systems with extra-pair reproduction and inbreeding

Abstract

Female extra‐pair reproduction in socially monogamous systems is predicted to cause cuckolded socially‐paired males to conditionally reduce paternal care, causing selection against extra‐pair reproduction and underlying polyandry. However, existing models and empirical studies have not explicitly considered that cuckolded males might be related to their socially‐paired female and/or to her extra‐pair mate, and therefore be related to extra‐pair offspring that they did not sire but could rear. Selection against paternal care, and hence against extra‐pair reproduction, might then be weakened. We derive metrics that quantify allele‐sharing between within‐pair and extra‐pair offspring and their mother and her socially‐paired male in terms of coefficients of kinship and inbreeding. We use song sparrow (Melospiza melodia) paternity and pedigree data to quantify these metrics, and thereby quantify the joint effects of extra‐pair reproduction and inbreeding on a brood's total allelic value to its socially‐paired parents. Cuckolded male song sparrows were almost always detectably related to extra‐pair offspring they reared. Consequently, although brood allelic value decreased substantially following female extra‐pair reproduction, this decrease was reduced by within‐pair and extra‐pair reproduction among relatives. Such complex variation in kinship within nuclear families should be incorporated into models considering coevolutionary dynamics of extra‐pair reproduction, parental care, and inbreeding.

Inbreeding parents should invest more resources in fewer offspring

“…A female that produces an outbred brood might have lower inclusive fitness than a female that produces an inbred brood of the same (or slightly smaller) size if the inbreeding female's viable offspring carry more identical-by-descent allele copies (see also [22]). Interestingly, if brood size is restricted by some physiological or external constraint (i.e.…”

“…Such theory ignores that parents might be able to increase the viability of their inbred offspring through PI, potentially mitigating ID. Because parents are more closely related to inbred offspring than they are to outbred offspring [12,21,22], inclusive fitness accrued from viable inbred offspring should be greater than that accrued from viable outbred offspring. Consequently, the inclusive fitness consequences of inbreeding and PI cannot be independent.…”

“…If inbreeding instead precludes a male from siring an additional outbred offspring, such as when there is an opportunity cost stemming from monogamy and associated biparental investment in offspring, then inbreeding is never beneficial [24]. However, existing theory that considers these inclusive fitness consequences of inbreeding assumes that PI is fixed despite resulting variation in parent–offspring relatedness [12,21,22]. …”

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

“…Hence, to quantify how polyandry translates into quantitative differences in relatedness among possible mates in future generations, we used standard pedigree algorithms (Lange 1997) to calculate the coefficient of kinship (k) between all adult females and all available adult males given the social (k SOC ) and genetic (k GEN ) pedigrees. The coefficient k measures the probability that two homologous alleles sampled from two individuals will be identical by descent relative to the pedigree baseline and equals the coefficient of inbreeding ( f ) of resulting offspring (Jacquard 1974;Lynch and Walsh 1998;Reid et al 2016). Values of k ≥ 0:25 indicate pairings between first-degree relatives (such as full sibs).…”

“…This is because shared ancestry between a focal pair's parents can increase the pair's relatedness above that expected given the same immediate relationship in an outbred population. For example, the relatedness between inbred half-sibs can approach that between outbred full sibs (Jacquard 1974;Lynch and Walsh 1998;Reid et al 2016). …”