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.

Keywords: grooming; heritability; indirect genetic effects; primate behavior; social behavior.

Figure 1.

Visualization of grooming metrics. (A) An example of our aggregate grooming index, representing grooming given by an adult female baboon OMO in 2003, considering all other adult females in her social group that year (individual females are identified by three-letter codes). Block arrows represent grooming given by OMO. The width of the arrow indicates the relative frequency of grooming observed; wider arrows indicate higher relative frequencies. OMO’s aggregate grooming given for 2003 is the sum of the width of the block arrows. (B) An example of our dyadic index. Here, we observed the grooming given by OMO to adult female OFR in a single year, represented by the large, gray block arrow. This phenotype is shaped by two components: the tendency of OMO to give grooming (direct effects), represented by the small gray arrow pushing the gray ball, and the tendency of OFR to elicit grooming from her partners (indirect effects) represented by the small black arrow pulling the black ball.