Reproductive state and sexual history shape the vaginal microbiota in wild baboons
The vaginal microbiome is one of the most important sites of bacterial-host symbiosis in mammals, playing a key role in defense against pathogens. This protective function is influenced by the composition of vaginal microbial communities, but to date the forces that shape vaginal microbiota remain poorly understood. We investigated variation in the baboon vaginal microbiota using an unusually well characterized population of wild savannah baboons (Papio cynocephalus) in the Amboseli ecosystem in Kenya. Long-term, individual-based research in this population allowed us to explore a wide range of factors that may shape vaginal microbiota, including individual reproductive state, age, maternal transmission, and patterns of sexual behavior. Vaginal swabs were collected from 48 sexually mature females between 2007 and 2010. Microbial community composition was assessed via sequencing of the V4 region of the 16S rRNA gene on the Illumina HiSeq2000 platform, which resulted in 1,777,373 rarefied reads per sample.
We found that reproductive state was the dominant driver of vaginal microbiome diversity and community composition. Multiple taxa showed significant changes in abundance with reproductive state, including genera associated with the disease-state bacterial vaginosis (BV) in human women. Within ovarian cycling, ovulating females showed remarkable differentiation from other cycle phases, characterized by relatively high levels of Firmicutes, Lactobacillales, and BV-associated genera. In addition to taxonomic variation, predictive metagenomic analyses revealed functional differences in the vaginal microbiome between reproductive states and cycle phases. This suggests there may be changes in the protective function of the vaginal microbiome in response to fluctuations in the host environment. We also found evidence for microbial transmission between sexual contacts. Specifically, females who shared mating partners had greater similarity in microbial community composition than those who did not. Overall, our results improve knowledge of individual-based sources of variation in the vaginal microbiome and may help shed light on the selective forces that have shaped these important bacterial communities.