Social Behavior and Host-Associated Microbes in Wild Baboons

Animal associated microbes—from single microbial taxa to whole microbial communities—have profound effects on animal health. Yet despite their importance, scientific understanding of the forces that shape host-associated microbial populations and communities is limited. A growing body of empirical work indicates that host social organization and behavior play a strong role in shaping these microbial populations and communities. If true, social effects on animal-associated microbes would constitute an unappreciated evolutionary consequence of social interactions and a new means by which social behavior affects animal health. However, many non-social forces—from host physiology to microbe-microbe interactions—also play strong roles in shaping microbiota.

I used genetic, behavioral, and comparative analyses to investigate the effects of both social and non-social factors on gut and vaginal microbiota at inter-host, intergroup, and interspecies levels. I did so using data from a well-studied population of wild baboons (Papio cynocephalus) in the Amboseli ecosystem, Kenya. I found that both social and non-social forces are important in shaping baboon microbial populations and communities. For instance, using strain typing to document the spread of Escherichia coli between baboon individuals and groups, I found that geographic overlap between baboon social groups promotes the spread of E. coli across host populations. Further, using next-generation sequencing of baboon vaginal microbiota, I found strong effects of baboon reproductive state on the relative abundance of microbial taxa, especially during ovulation. However, microbial diversity was linked to host promiscuity and females with more similar histories of sexual partners harbored more similar microbial communities. Finally, to understand the physiological mechanisms and evolutionary processes underlying interspecies variation in vaginal microbiota, I analyzed comparative data on vaginal tract pH and lactobacilli relative abundance from 26 mammalian species. I found that interspecies variation in the vaginal microbiome was not attributable to either differential reproductive physiology or evolutionary selective pressures for protective microbes. Overall, my dissertation provides new information on when social behavior influences host-associated microbial community structure and contributes to our understanding of the forces responsible for inter-host, intergroup, and interspecies variation in commensal microbial communities.