The evolutionary origins of primate scleral coloration

Abstract

Primate gaze following behaviors are of great interest to evolutionary scientists studying social cognition. The ability of an organism to determine a conspecifics likely intentions from their gaze direction may confer an advantage to individuals in a social group. This advantage could be cooperative and/or competitive. Humans are unusual in possessing depigmented sclerae whereas most other extant primates, including the closely related chimpanzee, possess dark scleral pigment. The origins of divergent scleral morphologies are currently unclear, though human white sclerae are often assumed to underlie our hyper-cooperative behaviors. Here, we use phylogenetic generalized least squares (PGLS) analyses with previously generated species-level scores of proactive prosociality, social tolerance (both n=15 primate species), and conspecific lethal aggression (n=108 primate species) to provide the first quantitative, comparative test of three complementary hypotheses. The cooperative eye [M. Tomasello, B. Hare, H. Lehmann, J. Call, J. Hum. Evol. 52, 314-320 (2007)] and self-domestication [B. Hare, Annu. Rev. Psychol. 68, 155-186 (2017)] explanations predict white sclerae to be associated with cooperative, rather than competitive, environments. The gaze camouflage hypothesis [H. Kobayashi, S. Kohshima, J. Hum. Evol. 40, 419-435 (2001)] predicts that dark scleral pigment functions as gaze direction camouflage in competitive social environments. We show that white sclerae in primates are associated with increased cooperative behaviors whereas dark sclerae are associated with reduced cooperative behaviors and increased intra-specific lethal aggression. Our results lend support to all three hypotheses of scleral evolution, suggesting that primate scleral morphologies evolve in relation to variation in social environment.