Mandrills use olfaction to socially avoid parasitized conspecifics

Abstract

The evolutionary transition from a solitary to a social lifestyle entails an elevated parasite cost because the social proximity associated with group living favors parasite transmission. Despite this cost, sociality is widespread in a large range of taxonomic groups. In this context, hosts would be expected to have evolved behavioral mechanisms to reduce the risk of parasite infection. Few empirical studies have focused on the influence of pathogen-mediated selection on the evolution of antiparasitic behavior in wild vertebrates. We report an adaptive functional relationship between parasitism and social behavior in mandrills, associated with evidence that they are able to gauge parasite status of their group members. Using long-term observations, controlled experiments, and chemical analyses, we show that (i) wild mandrills avoid grooming conspecifics infected with orofecally transmitted parasites; (ii) mandrills receive significantly more grooming after treatment that targets these parasites; (iii) parasitism influences the host's fecal odors; and (iv) mandrills selectively avoid fecal material from parasitized conspecifics. These behavioral adaptations reveal that selecting safe social partners may help primates to cope with parasite-mediated costs of sociality and that "behavioral immunity" plays a crucial role in the coevolutionary dynamics between hosts and their parasites.