Coevolution of cultural intelligence, extended life history, sociality, and brain size in primates

Abstract

Explanations for primate brain expansion and the evolution of human cognition and culture remain contentious despite extensive research. While multiple comparative analyses have investigated variation in brain size across primate species, very few have addressed why primates vary in how much they use social learning. Here, we evaluate the hypothesis that the enhanced reliance on socially transmitted behavior observed in some primates has coevolved with enlarged brains, complex sociality, and extended lifespans. Using recently developed phylogenetic comparative methods we show that, across primate species, a measure of social learning proclivity increases with absolute and relative brain volume, longevity (specifically reproductive lifespan), and social group size, correcting for research effort. We also confirm relationships of absolute and relative brain volume with longevity (both juvenile period and reproductive lifespan) and social group size, although longevity is generally the stronger predictor. Relationships between social learning, brain volume, and longevity remain when controlling for maternal investment and are therefore not simply explained as a by-product of the generally slower life history expected for larger brained species. Our findings suggest that both brain expansion and high reliance on culturally transmitted behavior coevolved with sociality and extended lifespan in primates. This coevolution is consistent with the hypothesis that the evolution of large brains, sociality, and long lifespans has promoted reliance on culture, with reliance on culture in turn driving further increases in brain volume, cognitive abilities, and lifespans in some primate lineages.

Keywords: brain evolution; cultural evolution; phylogenetic comparative analysis; primates; social learning.

Fig. 1.

Posterior distributions of β coefficients for the effects of longevity, juvenile period, and group size on (A) social learning richness, (B) absolute brain volume, and (C) relative brain volume (i.e., brain volume accounting for body mass). Here, we present effects from the simplest models, including only either longevity, juvenile period, or group size as independent variables, together with research effort and body mass for the social learning model, and body mass for the relative brain model. However, these results are not strongly affected by the inclusion of additional potentially confounding variables (Methods, Results, and SI Appendix). Percentages indicate the percentage of posterior estimates that cross zero in the opposite to the predicted direction for each effect. Distributions shifted substantially away from zero indicate evidence for effects of predictor variables in the corresponding direction whereas those centered close to zero indicate little or no evidence for effects of predictor variables.

Fig. 2.

Summary of raw data on social learning, absolute brain volume, group size, and longevity for 52 primate genera, using the consensus phylogeny from 10ktrees (65). For illustration purposes only, all data are summarized as genus-level means, standardized with minimum 0 and maximum 1. Also for illustration purposes only, social learning is displayed as a proportion of research effort whereas, in statistical analyses, social learning is controlled for research effort by including research effort as an independent variable. Images show (A) bearded capuchin (Cebus libidinosus), (B) chimpanzees (Pan troglodytes), and (C) guinea baboons (Papio papio), illustrating lineages that represent convergent coevolution of high social learning abilities, large brain volumes, complex social relationships, and long lifespans. (A) Courtesy of Flickr/Bart van Dorp, (B) courtesy of Flickr/USAID in Africa, and (C) courtesy of Flickr/William Warby.