Primate vaginal microbiomes exhibit species specificity without universal Lactobacillus dominance

Abstract

Bacterial communities colonizing the reproductive tracts of primates (including humans) impact the health, survival and fitness of the host, and thereby the evolution of the host species. Despite their importance, we currently have a poor understanding of primate microbiomes. The composition and structure of microbial communities vary considerably depending on the host and environmental factors. We conducted comparative analyses of the primate vaginal microbiome using pyrosequencing of the 16S rRNA genes of a phylogenetically broad range of primates to test for factors affecting the diversity of primate vaginal ecosystems. The nine primate species included: humans (Homo sapiens), yellow baboons (Papio cynocephalus), olive baboons (Papio anubis), lemurs (Propithecus diadema), howler monkeys (Alouatta pigra), red colobus (Piliocolobus rufomitratus), vervets (Chlorocebus aethiops), mangabeys (Cercocebus atys) and chimpanzees (Pan troglodytes). Our results indicated that all primates exhibited host-specific vaginal microbiota and that humans were distinct from other primates in both microbiome composition and diversity. In contrast to the gut microbiome, the vaginal microbiome showed limited congruence with host phylogeny, and neither captivity nor diet elicited substantial effects on the vaginal microbiomes of primates. Permutational multivariate analysis of variance and Wilcoxon tests revealed correlations among vaginal microbiota and host species-specific socioecological factors, particularly related to sexuality, including: female promiscuity, baculum length, gestation time, mating group size and neonatal birth weight. The proportion of unclassified taxa observed in nonhuman primate samples increased with phylogenetic distance from humans, indicative of the existence of previously unrecognized microbial taxa. These findings contribute to our understanding of host-microbe variation and coevolution, microbial biogeography, and disease risk, and have important implications for the use of animal models in studies of human sexual and reproductive diseases.

Vaginal Dysbiosis from an Evolutionary Perspective

“…L. crispatus is one of the most frequently detected phylotypes in the human vaginal microbiome (85%)11, but is among the lactobacilli with the lowest abundances in baboons8. In agreement with this observation, L. crispatus was detected in only one animal in our study (7.1%), a young female in a harem cage of 11 females.…”

Sexual transmission of beneficial microbes

“…STI prevalence among human populations is associated with higher levels of promiscuity [8], confirming the expected association between sexual behavior and infection rates. Promiscuity also impacts the overall community composition of the vaginal microbiome, increasing diversity in polygamous lizards [9], primates [10], and mice [11]. Mating multiply thus appears to lead to a greater sampling of the available microbial diversity within populations.…”

Lactobacilli Dominance and Vaginal pH: Why Is the Human Vaginal Microbiome Unique?

“…Comparative research on mammalian microbiomes is critical to understanding the basic evolutionary and ecological principles guiding microbiome structure and function across mammalian hosts (Ley et al, 2008b; Delsuc et al, 2014; Yildirim et al, 2014; Moeller et al, 2016). To date, most comparative studies in mammals find that hosts with similar lifestyles and evolutionary histories harbor similar microbiomes at a given body site, both in the bacterial taxa they contain and the functions they provide to hosts (Ley et al, 2008a; Delsuc et al, 2014).…”

“…To date, most comparative studies in mammals find that hosts with similar lifestyles and evolutionary histories harbor similar microbiomes at a given body site, both in the bacterial taxa they contain and the functions they provide to hosts (Ley et al, 2008a; Delsuc et al, 2014). One important exception to this pattern is the vaginal microbiome, where humans exhibit striking differences in community composition compared to other mammals (Spear et al, 2012; Swartz et al, 2014; Yildirim et al, 2014). Specifically, the human vaginal microbiome is dominated by Lactobacillus spp., which typically comprise >70% of resident bacteria in women, compared to <1% in other mammals.…”

“…Recently, a comparative analysis of the vaginal microbiome across non-human primates found that interspecies differences were predominantly explained by host species, with additional evidence that host socio-ecological factors, including host neonatal birth weight, may contribute to interspecies variation (Yildirim et al, 2014). However, no studies have yet directly correlated specific host risk factors with lactobacilli abundance and vaginal pH, the aspects of the vaginal microbiome thought to be protective in humans.…”