Early-life experience and disease exposure affect pathogen avoidance behaviour in macaques

Abstract

Pathogens exert strong selective pressure on group-living primates. In humans, disease defence includes both a biological and behavioural immune system, which includes the emotion of disgust and avoidance behaviours shaped by genetics, learning and culture. While pathogen avoidance is documented in nonhuman primates, little is known about how ecological and developmental factors influence pathogen sensitivity, that is, individual variation in pathogen avoidance. We conducted two studies to examine this in macaques. Our first study tested macaques (n = 54) from seven different species and four different rearing backgrounds in a visual food-choice task where food was either placed on a substrate with or without pathogenic cues. Macaques preferred feeding on non-contaminated substrates, with sanctuary-born individuals showing greater avoidance than former pets. Our second study tested sanctuary-born Japanese macaques (n = 55) from four groups; three groups had recently experienced an infectious disease outbreak. Macaques from exposed groups showed significantly higher avoidance of contaminated substrates. Together, our findings suggest that early life rearing experience and recent disease exposure shape pathogen sensitivity in macaques, demonstrating a flexible behavioural immune system in Old World monkeys. These findings suggest that flexible, context-sensitive pathogen avoidance is present in Old World monkeys, providing the behavioural foundations from which human disgust may have evolved.