Primate vaginal microbiomes exhibit species specificity without universal Lactobacillus dominance

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.National Research Council of Science and Technology Morris Animal Foundation Wildlife Conservation Society Joslin Diabetes Center National Institutes of Health: BCS-0323596, R01RR016300, 5R01RR016300, BCS-0323553, R010D010980 Primate Research Institute, Kyoto University Society for Cultural Anthropology: BCS-0962807 Game and Wildlife Conservation Trust University of Illinois at Urbana-Champaign National Science Foundation: BCS-08-20709 National Center for Research Resources: VA247-P-0447UIUC RBUIUC-Carle TRNational Science Foundation (NSF) [BCS-08-20709]--[BCS-0323553]--[BCS-0323596]--[BCS-0962807]NSF HOMINID [BCS-09-35347]NCRR P40 [RR019963]US Department of Veterans Affairs [VA247-P-0447]United States Department of Health & Human Services--National Institutes of Health (NIH) - USA [5R01RR016300]--[R01RR016300]--[R010D010980]Morris Animal FoundationOffice of the President of the Republic of KenyaKenya Wildlife ServiceInstitute of Primate Research, KenyaUganda Wildlife AuthorityUganda National Council for Science and TechnologyChimpanzee Sanctuary and Wildlife Conservation TrustWildlife Conservation SocietyUniversity of VeracruzConsejo Nacional de Areas Protegidas GuatemalaThis project was funded by UIUC RB and UIUC-Carle TR grants (to BA Wilson), NSF grant no. BCS-08-20709 (to RMS), and NSF HOMINID grant no. BCS-09-35347 (to SRL). We gratefully acknowledge Jeanne Altmann, Susan C Alberts, Jenny Tung, John Polk, and the late Abigail Salyers, as well as collaborator support from NCRR P40 grant no. RR019963 and VA contract no. VA247-P-0447 (to JDC), NIH grant no. 5R01RR016300 (to TT) grants R01RR016300 and R010D010980 to NBF, NSF grants BCS-0323553 and BCS-0323596 to SCA and JA, NSF grant BCS-0962807 to LCO, the Morris Animal Foundation support to TG, as well as the Office of the President of the Republic of Kenya, the Kenya Wildlife Service, and the Institute of Primate Research, Kenya, The Uganda Wildlife Authority, The Uganda National Council for Science and Technology, the Chimpanzee Sanctuary and Wildlife Conservation Trust, The Wildlife Conservation Society, The University of Veracruz, and Consejo Nacional de Areas Protegidas Guatemala. We also thank Michael Worobey and Anthony Yannarell for their guidance with phylogenetic and statistical analyses, respectively

Primate vaginal microbiomes exhibit species specificity without universal Lactobacillus dominance

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