Genetic ancestry predicts male-female affiliation in a natural baboon hybrid zone

Abstract

Opposite-sex social relationships are important predictors of fitness in many animals, including several group-living mammals. Consequently, understanding sources of variance in the tendency to form opposite-sex relationships is important for understanding social evolution. Genetic contributions are of particular interest due to their importance in long-term evolutionary change, but little is known about genetic effects on male-female relationships in social mammals, especially outside the mating context. Here, we investigate the effects of genetic ancestry on male-female affiliative behavior in a hybrid zone between the yellow baboon (Papio cynocephalus) and the anubis baboon (P. anubis), in a population in which male-female social bonds are known predictors of lifespan. We place our analysis within the context of other social and demographic predictors of affiliative behavior in baboons. Genetic ancestry was the most consistent predictor of opposite-sex affiliative behavior we observed, with the exception of strong effects of dominance rank. Our results show that increased anubis genetic ancestry is associated with subtly, but significantly higher rates of opposite-sex affiliative behavior, in both males and females. Additionally, pairs of anubis-like males and anubis-like females were the most likely to socially affiliate, resulting in moderate assortativity in grooming and proximity behavior as a function of genetic ancestry. Our findings indicate that opposite-sex affiliative behavior partially diverged during baboon evolution to differentiate yellow and anubis baboons, despite overall similarities in their social structures and mating systems. Further, they suggest that affiliative behavior may simultaneously promote and constrain baboon admixture, through additive and assortative effects of ancestry, respectively.

Genetic variance and indirect genetic effects for affiliative social behavior in a wild primate

“…However, in the dyadic grooming index, we detected a significant interaction between the admixture score of the focal female and her partner: individuals with more anubis ancestry preferentially groomed partners that were more anubis-like, while more yellow-like females appeared insensitive to the ancestry of their partners. Similar effects of admixture score have been described for male mating success and for male-female affiliative behavior in our study population (Tung et al 2012, Fogel et al 2021), together suggesting that anubis-like females may behave more assortatively (with respect to ancestry) than yellow-like females in their choice of social or mating partners. This phenomenon could arise either through competitive access to preferred partners or because of differences in preference strength (e.g., if the costs of interacting with a member of a different sub-population are higher for more anubis-like females than for yellow-like females).…”

“…In addition, while we found no main effect of dominance rank on dyadic grooming, we did find an interaction effect, such that higherranking individuals gave more grooming to high-ranking partners, while lower-ranking individuals gave more grooming to low-ranking partners (Table 1). This result parallels our analysis of male-female grooming, in which the probability of grooming was highest for male-female pairs in which both partners were high-ranking (Fogel et al 2021). This result is also consistent with Seyfarth's model, which predicts that females compete for the opportunity to groom higher ranking females, and consequently high-ranking females have the greatest access to their preferred partners (Seyfarth 1977).…”

“…Second, among our environmental effects, the tendency for more anubis-like females to groom more anubis-like partners is intriguing, especially given that admixture scores have no detectable effect on aggregate grooming patterns. This result contributes to growing evidence of subtle behavioral differentiation between yellow and anubis baboons (Tung et al 2012, Franz et al 2015, Fogel et al 2021), which are generally viewed as behaviorally and ecologically similar. Finally, the strong genetic correlation between grooming given and grooming received demands further investigation to determine whether this correlation reflects the genetic architecture of this trait, or the fact that family effects on grooming phenotypes are not fully accounted for in our models.…”

Early life adversity and adult social relationships have independent effects on survival in a wild animal model of aging

“…Age was not included as a covariate even though social bonds vary with age, because age effects are captured by our functional principal components analysis (FPCA) approach to modeling the mediator (see below). Because our baboon study population represents an admixed population (yellow baboon ancestry is dominant, but all individuals exhibit some degree of admixture with anubis baboons), we also ran separate analyses that included a covariate measure of individual admixture, a ‘genetic hybrid score’ that represents the proportion of each individual’s genome estimated to be from P. anubis ancestry (see Supplementary Information, also ( 101, 102 ). Results that incorporated hybrid score (Tables S4-S5) were similar to those of the full model (Tables 2-3).…”