Mandrills and microbes: The role of the skin microbiome in primate communication

Summary

This project combines microbial and behavioural ecology to examine key questions in animal behaviour, including how animals recognise kin, how they identify potential mates, and the costs and benefits of sociality.

Animals host a huge diversity of microbiota (including bacteria, fungi, archaea, protozoa and viruses) on and in their bodies. Some of these microbes are pathogenic, but many are beneficial to their hosts and play crucial roles in animal lives. For example, the fermentation hypothesis suggests that microbiota in animal scent glands digest animal secretions, producing odour cues that encode rich information about their host, such as individual identity, age, sex, reproductive status, health, diet, dominance, kin relationships and social relationships.

Olfactory profiles may even encode information about genotype, for example, possession of beneficial genes that confer disease resistance, such as the major histocompatibility complex (MHC). Odour cues are commonly hypothesised to underpin two key aspects of evolutionary theory: sexual selection (via mate choice and reproductive competition) and kin selection (the role of genetic relatedness in social behaviour).

Moreover, social relationships can mediate the acquisition and sharing of microbiota, influencing the costs and benefits of social behaviour with kin and non-kin.

Advances in microbial ecology have revolutionised our understanding of the microbiome. However, most of our knowledge of the microbiome in animals in their natural habitat is based on faecal samples, which are relatively easy to collect, and we know far less about the skin microbiome. Moreover, much of what we do know is for humans, and we know that the human microbiome (and skin) differs to that of other mammals, probably due to cultural practices including living in a built environment, wearing clothes, and use of soap.

This project combines behavioural observations, biological sampling, high-throughput sequencing, and bioinformatics to characterise the microbial communities on the skin of mandrills (a large species of Old World monkey) living under naturalistic conditions, and to test predictions of the fermentation hypothesis, that:

(i) The microbial community includes taxa likely to produce odorant molecules as metabolic by-products.

(ii) The composition of the microbial community differs predictably with host-specific characteristics (subject identity, age and maturational stage, sex, dominance rank, reproductive status), relatedness (e.g., mother/offspring), and other social relationships, measured via behavioural observation of the colony. We will also test variation in the microbial community over time, with season, between groups, and between sites on the body.

Mandrills are a particularly intriguing species for this study because they are one of very few catarrhine primates (Old World monkeys and apes, including humans) to possess a scent gland. Differences in the volatile profile of secretions from this sternal gland are linked to host-specific characteristics (age, sex, dominance rank), and to MHC genotype, suggesting that odour may facilitate sexual and kin selection in this species.

Moreover, mandrill behaviour suggests that they can recognise paternal kin, despite their polygynandrous mating system, suggesting that odour may underlie kin recognition.

The project will contribute to our understanding of mammalian microbiomes, particularly the primate skin microbiome. Potential for future work includes relating the microbial community composition to volatile profiles of odour gland secretions, and to host genotype.