The primate vaginal microbiome: Comparative context and implications for human health and disease

Abstract

The primate body hosts trillions of microbes. Interactions between primate hosts and these microbes profoundly affect primate physiology, reproduction, health, survival, and ultimately, evolution. It is increasingly clear that primate health cannot be understood fully without knowledge of host-microbial interactions. Our goals here are to review what is known about microbiomes of the female reproductive tract and to explore several factors that influence variation within individuals, as well as within and between primate species. Much of our knowledge of microbial variation derives from studies of humans, and from microbes located in nonreproductive regions (e.g., the gut). We review work suggesting that the vaginal microbiota affects female health, fecundity, and pregnancy outcomes, demonstrating the selective potential for these agents. We explore the factors that correlate with microbial variation within species. Initial colonization by microbes depends on the manner of birth; most microbial variation is structured by estrogen levels that change with age (i.e., at puberty and menopause) and through the menstrual cycle. Microbial communities vary by location within the vagina and can depend on the sampling methods used (e.g., swab, lavage, or pap smear). Interindividual differences also exist, and while this variation is not completely understood, evidence points more to differences in estrogen levels, rather than differences in external physical environment. When comparing across species, reproductive-age humans show distinct microbial communities, generally dominated by Lactobacillus, unlike other primates. We develop evolutionary hypotheses to explain the marked differences in microbial communities. While much remains to be done to test these hypotheses, we argue that the ample variation in primate mating and reproductive behavior offers excellent opportunities to evaluate host-microbe coevolution and adaptation. Am J Phys Anthropol 57:119-134,

Primate vaginal microbiomes exhibit species specificity without universal Lactobacillus dominance

“…Pregnant women are particularly vulnerable to microbial community disruptions (McGregor and French, 2000) and birth constraints greatly elevate risks of infection to both the fetus and mother. Although our correlational study cannot determine causes of the relationship between sexuality, birth and a distinctive microbial ecosystem, we hypothesize that humans effectively select microbial communities that minimize risks of sexual, gestational and post-parturition infection (see Stumpf et al (2013) for additional hypotheses concerning human uniqueness).…”

Microbiome Disturbances and Autism Spectrum Disorders

“…Next, we will review the handful of human epidemiologic studies correlating microbiota and bacterial metabolite changes in ASD patients. While the majority, if not all, of the studies to date have focused on the potential role of gut microbiome alterations and ASD, it is now clear that other organs and systems, including the oral cavity (Ding and Schloss, 2014), lung (Dickson et al, 2014), placenta Amarasekara et al, 2014;Antony et al, 2014;Doyle et al, 2014), and vagina (Stumpf et al, 2013;Ding and Schloss, 2014), possess unique microbiomes that may influence distal target systems. Therefore, we will consider whether disruptions in these other microbiomes may be contributing etiologies to ASD risk.…”

Comparative Functional Genomics of Lactobacillus spp. Reveals Possible Mechanisms for Specialization of Vaginal Lactobacilli to Their Environment

“…Even though the four Lactobacillus species commonly found and abundant in the human vagina have been isolated from other sites, their occurrence is extremely rare (10)(11)(12)(13)(14). Furthermore, the vaginal microbial community of nonhuman primates is not dominated by Lactobacillus species (15). For instance, in an analysis of the genital microbiota of the rhesus macaque, Spear et al (16) found that the communities were somewhat similar to human vaginal communities of women with bacterial vaginosis, which is characterized by a shift from a flora dominated by lactobacilli to a mixed flora (17), and when individuals belonging to the genus Lactobacillus were detected, they were present at a low relative abundance.…”