The expression of care: Alloparental care frequency predicts neural control of facial muscles in primates.

Abstract

The adaptive value of facial expressions has been debated in evolutionary biology ever since Darwin's seminal work. Among mammals, primates, including humans, exhibit the most intricate facial displays. Although previous work has focused on the role of sociality in the evolution of primate facial expressions, this relationship has not been verified in a wide sample of species. Here, we examine the relationship between allomaternal care (paternal or alloparental) and the morphology of three orofacial brainstem nuclei (facial; trigeminal motor; hypoglossal) across primates to test the hypothesis that allomaternal care explains variation in the complexity of facial expressions, proxied by relative facial nucleus size and neuropil fraction. The latter represents the proportion of synaptically dense tissue and may, therefore, correlate with dexterity. We find that alloparental care frequency predicts relative neuropil fraction of the facial nucleus, even after controlling for social system organization, whereas allomaternal care is not associated with the trigeminal motor or hypoglossal nuclei. Overall, this work suggests that alloparenting requires increased facial dexterity to facilitate nonverbal communication between infants and their nonparent caregivers and/or between caregivers. Accordingly, alloparenting and complex facial expressions are likely to have coevolved in primates.