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

Abstract

Affiliative social behaviors are linked to fitness components in multiple species. However, the role of genetic variance in shaping such behaviors remains largely unknown, limiting our understanding of how affiliative behaviors can respond to natural selection. Here, we employed the ‘animal model’ to estimate environmental and genetic sources of variance and covariance in grooming behavior in the well-studied Amboseli wild baboon population. We found that the tendency for a female baboon to groom others (‘grooming given’) is heritable (h2=0.22± 0.048), and that several environmental variables – including dominance rank and the availability of kin as grooming partners – contribute to variance in this grooming behavior. We also detected small but measurable variance due to the indirect genetic effect of partner identity on the amount of grooming given within dyadic grooming partnerships. The indirect and direct genetic effects for grooming given were positively correlated (r=0.74± 0.09). Our results provide insight into the evolvability of affiliative behavior in wild animals, including the possibility for correlations between direct and indirect genetic effects to accelerate the response to selection. As such they provide novel information about the genetic architecture of social behavior in nature, with important implications for the evolution of cooperation and reciprocity.

Environmental, sex-specific and genetic determinants of infant social behaviour in a wild primate

“…In general, the heritability of behavioural traits is lower than that of morphological traits [40,83]. However, our value of h 2 = 0.043 is much lower than the average of h 2 approximately 0.30 reported in two meta-analyses of the heritability of social behaviour [39,47], and 4-6 times lower than the heritability of adult grooming behaviour (h 2 = 0.16-0.26) measured in our study population [44]. Part of this difference reflects measurement error: because first grooming events are relatively brief, one-time events in an individual's life, it is unlikely that we captured all first grooming events with high accuracy.…”

“…at a rate > n relatives/group size). We categorized first grooming partners by relatedness using the 'kinship' function in the 'kinship2' R package [64], which estimates relatedness coefficients between dyads based on multigeneration pedigree information [44,65]. All 781 of our subjects had known mothers and 489 had known fathers.…”

“…Finally, some of the unexplained variation in our model may be attributable to indirect genetic effects (IGEs) in which the genotypes of social partners affect focal phenotypes [88]. Given the demonstrated importance of IGEs in other studies of behaviour [44,89], the role of IGEs in the ontogeny of social interactions in the wild represents another important topic for future research.…”

“…In humans and non-human vertebrates, variation in affiliative social behaviour tends to be weakly, but measurably, heritable (e.g. in comparison to morphological or life-history traits [37][38][39][40][41][42][43][44][45][46][47]). However, in the absence of studies of the heritability of behavioural development in wild populations, the relative contributions of genes versus the environment, and the degree to which developmental features of social behaviour can respond to natural selection, remain unknown.…”

Early life adversity and adult social relationships have independent effects on survival in a wild primate

“…Our results suggest that adult social behaviors that maintain social bonds should be under strong selection. Because social behavior is almost always partially heritable, including in our study population [e.g., (65)(66)(67)], these behaviors have the potential to evolve via natural selection. Furthermore, our findings suggest that indirect genetic effects, in which the genotypes of social partners affect behavior, could play an important role in social selection and evolution (68,69).…”