Inbreeding risk, avoidance and costs in a group-living primate, Cebus capucinus

Abstract

Documenting inbreeding and its potential costs in wild populations is a complicated matter. Early infant death before genetic samples can be collected limits the ability of researchers to measure fitness costs, and pedigree information is necessary to accurately estimate relatedness between breeding individuals. Using data from 25 years of research from the Lomas Barbudal Capuchin Monkey Project, and a sample of 109 females that have given birth, we find that despite frequent co-residency of adult opposite-sexed individuals, capuchins produce offspring with close kin (i.e. related at the half sibling level or higher) less often than would be expected in the absence of inbreeding avoidance. We do not find support for alternative, non-behavioral explanations for this pattern and thus argue for mate choice. Furthermore, we find evidence for fitness costs among inbred animals in the form of delayed female age at first birth, but not significantly higher juvenile mortality. Further research is necessary in order to determine the mechanisms by which individuals develop sexual aversion to close kin. Significance Statement: Through a combination of demographic records, maternal pedigrees, and genetically determined paternity, this study provides a detailed study of inbreeding and inbreeding avoidance in a well-studied mammal population. This study provides (1) evidence that capuchin monkeys avoid mating with close kin at both the level of daughter-father and half sibling, and (2) evidence of fitness costs to inbreeding in the form of delayed first age at reproduction.

Inbreeding avoidance and female mate choice shape reproductive skew in capuchin monkeys (Cebus capucinus imitator)

“…We would only be able to answer this question confidently with continued longitudinal sampling from our study groups or additional sampling from surrounding social groups. However, we cautiously suggest that inbreeding avoidance between alpha males and their mature daughters is typical of white-faced capuchins in this area based on similar patterns reported from a near-by population (Muniz et al 2006;Godoy et al 2016a).…”

“…Inbreeding avoidance reinforces high reproductive skew in several cooperative breeders where mature offspring rarely have access to unrelated mating partners in the group (Cooney & Bennett 2000;Clutton-Brock et al 2001;Griffin et al 2003;Nelson-Flower et al 2011). In contrast, inbreeding avoidance can decrease the reproductive skew in pair-living or group-living animals if females can mate with lessrelated extra-group males or within-group subordinate males (plural breeding primates: Altmann et al 1996;Muniz et al 2006;Godoy et al 2016a;pair-living birds: Arct et al 2015; but see Reid 2015). Our study population appears to fall into this latter category of populations with active inbreeding avoidance leading to decreased reproductive skew, because the alpha male's probability of siring a particular offspring decreased when he was the sire of the offspring's mother.…”

“…; Godoy et al . ). If alpha males and their mature daughters avoid inbreeding and/or females prefer to mate with novel males, male reproductive skew may be relatively low in groups with long‐term alpha males.…”

“…; Godoy et al . ,b). Thus, mate choice for unrelated, novel males may lead to a lower reproductive skew in some populations.…”

“…The tenure of an alpha male can last up to 18 years , whereas females typically produce their first offspring around the age of 6 years . Because females remain philopatric, alpha males with such long tenures reside with their mature daughters (Muniz et al 2006;Godoy et al 2016a). If alpha males and their mature daughters avoid inbreeding and/or females prefer to mate with novel males, male reproductive skew may be relatively low in groups with long-term alpha males.…”