Father–daughter inbreeding avoidance in a wild primate population

The most common way by which social animals avoid breeding with relatives is for members of one or both sexes to disperse before reproducing [1]. In capuchin monkeys — as in most primates — males disperse while females benefit from lifelong relationships with maternal kin within the group [2]. If α-males — who sire most offspring in a given group — retain their rank for longer than 6 years, the age at which females reach sexual maturity, father–daughter inbreeding could occur. Here, we combine data from long-term observations and DNA analyses and present extensive genetic evidence for effective avoidance of father–daughter inbreeding without dispersal in wild primates. Three wild groups of white­ faced capuchin monkeys habituated to observation were studied for up to 14 years in and near the Lomas Barbudal Biological Reserve in Costa Rica. Groups contained 2–11 adult males and 4–10 adult females. Male dominance ranks were determined by quantifying the number of times males cowered to or avoided one another in dyadic social contexts. There was always a clear α-male in each group, whereas the dominance relationships among subordinate males could not be consistently ascertained. The α-male of one group is estimated to have had a minimum tenure of 7 years and for the other two groups, two males, who continue to hold α ranks, have held their positions for at least 12 and 13 years, respectively. However, to be conservative, the results presented here are based exclusively upon analysis of conceptions during the time periods for which dominance ranks are based upon behavioral observations. We genotyped 172 monkeys using 18 microsatellite loci and determined the fathers of 41 surviving offspring conceived during these long tenures (see Supplemental Data published with this article online). The percentage of each group’s offspring sired by α-males ranged from 38% to 80% (Figure 1A), and each α male sired more offspring than did any subordinate male in