Gut microbiota variations in wild yellow baboons (Papio cynocephalus) are associated with sex and habitat disturbance.

Although male and female mammals differ in biological traits and functional needs, the contribution of this sexual dimorphism to variations in gut bacteria and fungi (gut microbiota) in relation to habitat type has not been fully examined. To understand whether the combination of sex and habitat affects gut microbiota variation, we analyzed 40 fecal samples of wild yellow baboons (Papio cynocephalus) living in contrasting habitat types (intact, well-protected vs. fragmented, less protected forests) in the Udzungwa Mountains of Tanzania. Sex determination was performed using the marker genes SRY (Sex-determining Region Y) and DDX3X-DDX3Y (DEAD-Box Helicase 3). Samples were attributed to 34 individuals (19 females and 15 males) belonging to five social groups. Combining the results of sex determination with two amplicon sequencing datasets on bacterial (V1-V3 region of the 16S rRNA gene) and fungal (ITS2) gut communities, we found that overall, baboon females had a significantly higher gut bacterial richness compared to males. Beta diversity estimates indicated that bacterial composition was significantly different between males and females, and this was true for individuals from both well- and less protected forests. Our results highlight the combined role of sex and habitat type in shaping variation in gut microbial communities in wild non-human primates.

Five Decades of Data Yield No Support for Adaptive Biasing of Offspring Sex Ratio in Wild Baboons (Papio cynocephalus).

AbstractOver the past 50 years, a wealth of testable, often conflicting hypotheses have been generated about the evolution of offspring sex ratio manipulation by mothers. Several of these hypotheses have received support in studies of invertebrates and some vertebrate taxa. However, their success in explaining sex ratios in mammalian taxa-especially in primates-has been mixed. Here, we assess the predictions of four different hypotheses about the evolution of biased offspring sex ratios in the baboons of the Amboseli basin in Kenya: the Trivers-Willard, female rank enhancement, local resource competition, and local resource enhancement hypotheses. Using the largest sample size ever analyzed in a primate population (n=1,372 offspring), we test the predictions of each hypothesis. Overall, we find no support for adaptive biasing of sex ratios. Offspring sex is not consistently related to maternal dominance rank or biased toward the dispersing sex, nor is it predicted by group size, population growth rates, or their interaction with maternal rank. Because our sample size confers power to detect even subtle biases in sex ratio, including modulation by environmental heterogeneity, these results suggest that adaptive biasing of offspring sex does not occur in this population.

Ecology and age, but not genetic ancestry, predict fetal loss in a wild baboon hybrid zone.

OBJECTIVES: Pregnancy failure represents a major fitness cost for any mammal, particularly those with slow life histories such as primates. Here, we quantified the risk of fetal loss in wild hybrid baboons, including genetic, ecological, and demographic sources of variance. We were particularly interested in testing the hypothesis that hybridization increases fetal loss rates. Such an effect would help explain how baboons may maintain genetic and phenotypic integrity despite interspecific gene flow. MATERIALS AND METHODS: We analyzed outcomes for 1020 pregnancies observed over 46 years in a natural yellow baboon-anubis baboon hybrid zone. Fetal losses and live births were scored based on records of female reproductive state and the appearance of live neonates. We modeled the probability of fetal loss as a function of a female's genetic ancestry (the proportion of her genome estimated to be descended from anubis [vs. yellow] ancestors), age, number of previous fetal losses, dominance rank, group size, climate, and habitat quality using binomial mixed effects models. RESULTS: Female genetic ancestry did not predict fetal loss. Instead, the risk of fetal loss is elevated for very young and very old females. Fetal loss is most robustly predicted by ecological factors, including poor habitat quality prior to a home range shift and extreme heat during pregnancy. DISCUSSION: Our results suggest that gene flow between yellow and anubis baboons is not impeded by an increased risk of fetal loss for hybrid females. Instead, ecological conditions and female age are key determinants of this component of female reproductive success.

Association of human disturbance and gastrointestinal parasite infection of yellow baboons in western Tanzania.

Human disturbance is an ongoing threat to many wildlife species, manifesting as habitat destruction, resource overuse, or increased disease exposure, among others. With increasing human: non-human primate (NHP) encounters, NHPs are increasingly susceptible to human-introduced diseases, including those with parasitic origins. As such, epidemiology of parasitic disease is becoming an important consideration for NHP conservation strategies. To investigate the relationship between parasite infections and human disturbance we studied yellow baboons (Papio cynocephalus) living outside of national park boundaries in western Tanzania, collecting 135 fresh faecal samples from nine troops occupying areas with varying levels of human disturbance. We fixed all samples in 10% formalin and later evaluated parasite prevalence and abundance (of isotrichid ciliates and Strongylida). We identified seven protozoan and four helminth taxa. Taxa showed varied relationships with human disturbance, baboon troop size and host age. In four taxa, we found a positive association between prevalence and troop size. We also report a trend towards higher parasite prevalence of two taxa in less disturbed areas. To the contrary, high levels of human disturbance predicted increased abundance of isotrichid ciliates, although no relationship was found between disturbance and Strongylida abundance. Our results provide mixed evidence that human disturbance is associated with NHP parasite infections, highlighting the need to consider monitoring parasite infections when developing NHP conservation strategies.

High social status males experience accelerated epigenetic aging in wild baboons.

Aging, for virtually all life, is inescapable. However, within populations, biological aging rates vary. Understanding sources of variation in this process is central to understanding the biodemography of natural populations. We constructed a DNA methylation-based age predictor for an intensively studied wild baboon population in Kenya. Consistent with findings in humans, the resulting 'epigenetic clock' closely tracks chronological age, but individuals are predicted to be somewhat older or younger than their known ages. Surprisingly, these deviations are not explained by the strongest predictors of lifespan in this population, early adversity and social integration. Instead, they are best predicted by male dominance rank: high-ranking males are predicted to be older than their true ages, and epigenetic age tracks changes in rank over time. Our results argue that achieving high rank for male baboons - the best predictor of reproductive success - imposes costs consistent with a 'live fast, die young' life-history strategy.

For most animals, age is one of the strongest predictors of health and survival, but not all individuals age at the same rate. In fact, animals of the same species can have different 'biological ages' even when they have lived the same number of years. In humans and other mammals this variation in aging shows up in chemical modifications known as DNA methylation marks. Some researchers call these marks 'epigenetic', which literally means 'upon the genes'. And some DNA methylation marks change with age, so their combined pattern of change is often called the 'epigenetic clock'. Environmental stressors, such as smoking or lack of physical activity, can make the epigenetic clock 'tick' faster, making the DNA of some individuals appear older than expected based on their actual age in years. These 'biologically older' individuals may also experience a higher risk of age-related disease. Studies in humans have revealed some of the reasons behind this fast biological aging, but it is unclear whether these results apply in the wild. It is possible that early life events trigger changes in the epigenetic clock, affecting health in adulthood. In primates, for example, adversity in early life has known effects on fertility and survival. Low social status also has a negative effect on health. To find out whether early experiences and the social environment affect the epigenetic clock, Anderson, Johnston et al. tracked DNA methylation marks in baboons. This revealed that epigenetic clocks are strong predictors of age in wild primates, but neither early adversity nor the strength of social bonds affected the rate at which the clocks ticked. In fact, it was competition for social status that had the most dramatic effect on the clock's speed. Samples of males taken at different times during their lives showed that their epigenetic clocks sped up or slowed down as they moved up or down the social ladder, reflecting recent social experiences, rather than events early in their lives. On average, epigenetic clock measurements overestimated the age in years of alpha males by almost a year, showing that fighting to be on top comes at a cost. This study highlights one way in which the social environment can influence aging. The next step is to understand how health is affected by the ways that animals attain social status. This could help researchers who study evolution understand how social interactions and environmental conditions affect survival and reproduction. It could also provide insight into the effects of social status on human health and aging.

Social bonds, social status and survival in wild baboons: a tale of two sexes.

People who are more socially integrated or have higher socio-economic status live longer. Recent studies in non-human primates show striking convergences with this human pattern: female primates with more social partners, stronger social bonds or higher dominance rank all lead longer lives. However, it remains unclear whether social environments also predict survival in male non-human primates, as it does in men. This gap persists because, in most primates, males disperse among social groups, resulting in many males who disappear with unknown fate and have unknown dates of birth. We present a Bayesian model to estimate the effects of time-varying social covariates on age-specific adult mortality in both sexes of wild baboons. We compare how the survival trajectories of both sexes are linked to social bonds and social status over the life. We find that, parallel to females, male baboons who are more strongly bonded to females have longer lifespans. However, males with higher dominance rank for their age appear to have shorter lifespans. This finding brings new understanding to the adaptive significance of heterosexual social bonds for male baboons: in addition to protecting the male's offspring from infanticide, these bonds may have direct benefits to males themselves. This article is part of the theme issue 'Evolution of the primate ageing process'.

Noninvasive measurement of mucosal immunity in a free-ranging baboon population.

Ecoimmunological patterns and processes remain understudied in wild primates, in part because of the lack of noninvasive methods to measure immunity. Secretory immunoglobulin A (sIgA) is the most abundant antibody present at mammalian mucosal surfaces and provides an important first line of defense against pathogens. Recent studies show that sIgA can be measured noninvasively in feces and is a good marker of mucosal immunity. Here we validated a commercial ELISA kit to measure fecal IgA in baboons, tested the robustness of its results to variation in collection and storage conditions, and developed a cost-effective in-house ELISA for baboon fecal IgA. Using data from the custom ELISA, we assessed the relationship between fecal IgA concentrations and gastrointestinal parasite burden, and tested how sex, age, and reproductive effort predict fecal IgA in wild baboons. We find that IgA concentrations can be measured in baboon feces using an in-house ELISA and are highly correlated to the values obtained with a commercial kit. Fecal IgA concentrations are stable when extracts are stored for up to 22 months at -20°C. Fecal IgA concentrations were negatively correlated with parasite egg counts (Trichuris trichiura), but not parasite richness. Fecal IgA did not vary between the sexes, but for males, concentrations were higher in adults versus adolescents. Lactating females had significantly lower fecal IgA than pregnant females, but neither pregnant nor lactating female concentrations differed significantly from cycling females. Males who engaged in more mate-guarding exhibited similar IgA concentrations to those who engaged in little mate-guarding. These patterns may reflect the low energetic costs of mucosal immunity, or the complex dependence of IgA excretion on individual condition. Adding a noninvasive measure of mucosal immunity will promote a better understanding of how ecology modulates possible tradeoffs between the immune system and other energetically costly processes in the wild.

Strain diversity of Treponema pallidum subsp. pertenue suggests rare interspecies transmission in African nonhuman primates.

In our most recent study, we found that in Tanzania infection with Treponema pallidum (TP) subsp. pertenue (TPE) is present in four different monkey species. In order to gain information on the diversity and epidemiological spread of the infection in Tanzanian nonhuman primates (NHP), we identified two suitable candidate genes for multi-locus sequence typing (MLST). We demonstrate the functionality of the MLST system in invasively and non-invasively collected samples. While we were not able to demonstrate frequent interspecies transmission of TPE in Tanzanian monkeys, our results show a clustering of TPE strains according to geography and not host species, which is suggestive for rare transmission events between different NHP species. In addition to the geographic stability, we describe the relative temporal stability of the strains infecting NHPs and identified multi-strain infection. Differences between TPE strains of NHP and human origin are highlighted. Our results show that antibiotic resistance does not occur in Tanzanian TPE strains of NHP origin.

The expression and function of TRPV4 channels in primate retinal ganglion cells and bipolar cells.

The transient receptor potential vanilloid 4 (TRPV4) channel may be opened by mechanical stimuli to mediate Ca2+ and Na+ influxes, and it has been suggested to mediate glaucoma retinopathy. However, it has been mostly unclear how TRPV4 activities affect the function of primate retinal ganglion cells (RGCs). We studied RGCs and bipolar cells (BCs) in the peripheral retina of the old-world primate using whole-cell current-clamp and voltage-clamp recordings, immunomarkers and confocal microscopy. RGCs were distinguished from displaced amacrine cells (ACs) by the absence of GABA and glycine immunoreactivity and possession of an axon and a large soma in the RGC layer. Strong TRPV4 signal was concentrated in medium to large somas of RGCs, and some TRPV4 signal was found in BCs (including PKCα-positive rod BCs), as well as the end feet, soma and outer processes of Mȕller cells. TRPV4 immunoreactivity quantified by the pixel intensity histogram revealed a high-intensity component for the plexiform layers, a low-intensity component for the soma layers of ACs and Mȕller cells, and both components in the soma layers of RGCs and BCs. In large RGCs, TRPV4 agonists 4α-phorbol 12,13 didecanoate (4αPDD) and GSK1016790A reversibly enhanced the spontaneous firing and shortened the delay of voltage-gated Na+ (Nav) currents under current-clamp conditions, and under voltage-clamp conditions, 4αPDD largely reversibly increased the amplitude and frequency of spontaneous excitatory postsynaptic currents. In BCs, changes in the membrane tension induced by either applying pressure or releasing the pressure both activated a transient cation current, which reversed at ~ -10 mV and was enhanced by heating from 24 °C to 30 °C. The pressure for the half-maximal effect was ~18 mmHg. These data indicate that functional TRPV4 channels are variably expressed in primate RGCs and BCs, possibly contributing to pressure-related changes in RGCs in glaucoma.

A missing piece of the Papio puzzle: Gorongosa baboon phenostructure and intrageneric relationships.

Most authors recognize six baboon species: hamadryas (Papio hamadryas), Guinea (Papio papio), olive (Papio anubis), yellow (Papio cynocephalus), chacma (Papio ursinus), and Kinda (Papio kindae). However, there is still debate regarding the taxonomic status, phylogenetic relationships, and the amount of gene flow occurring between species. Here, we present ongoing research on baboon morphological diversity in Gorongosa National Park (GNP), located in central Mozambique, south of the Zambezi River, at the southern end of the East African Rift System. The park exhibits outstanding ecological diversity and hosts more than 200 baboon troops. Gorongosa National Park baboons have previously been classified as chacma baboons (P. ursinus). In accordance with this, two mtDNA samples from the park have been placed in the same mtDNA clade as the northern chacma baboons. However, GNP baboons exhibit morphological features common in yellow baboons (e.g., yellow fur color), suggesting that parapatric gene flow between chacma and yellow baboons might have occurred in the past or could be ongoing. We investigated the phenostructure of the Gorongosa baboons using two approaches: 1) description of external phenotypic features, such as coloration and body size, and 2) 3D geometric morphometric analysis of 43 craniofacial landmarks on 11 specimens from Gorongosa compared to a pan-African sample of 352 baboons. The results show that Gorongosa baboons exhibit a mosaic of features shared with southern P. cynocephalus and P. ursinus griseipes. The GNP baboon phenotype fits within a geographic clinal pattern of replacing allotaxa. We put forward the hypothesis of either past and/or ongoing hybridization between the gray-footed chacma and southern yellow baboons in Gorongosa or an isolation-by-distance scenario in which the GNP baboons are geographically and morphologically intermediate. These two scenarios are not mutually exclusive. We highlight the potential of baboons as a useful model to understand speciation and hybridization in early human evolution.

Genes, geology and germs: gut microbiota across a primate hybrid zone are explained by site soil properties, not host species.

Gut microbiota in geographically isolated host populations are often distinct. These differences have been attributed to between-population differences in host behaviours, environments, genetics and geographical distance. However, which factors are most important remains unknown. Here, we fill this gap for baboons by leveraging information on 13 environmental variables from 14 baboon populations spanning a natural hybrid zone. Sampling across a hybrid zone allowed us to additionally test whether phylosymbiosis (codiversification between hosts and their microbiota) is detectable in admixed, closely related primates. We found little evidence of genetic effects: none of host genetic ancestry, host genetic relatedness nor genetic distance between host populations were strong predictors of baboon gut microbiota. Instead, gut microbiota were best explained by the baboons' environments, especially the soil's geologic history and exchangeable sodium. Indeed, soil effects were 15 times stronger than those of host-population FST, perhaps because soil predicts which foods are present, or because baboons are terrestrial and consume soil microbes incidentally with their food. Our results support an emerging picture in which environmental variation is the dominant predictor of host-associated microbiomes. We are the first to show that such effects overshadow host species identity among members of the same primate genus.

Analysis of 100 high-coverage genomes from a pedigreed captive baboon colony.

Baboons (genus Papio) are broadly studied in the wild and in captivity. They are widely used as a nonhuman primate model for biomedical studies, and the Southwest National Primate Research Center (SNPRC) at Texas Biomedical Research Institute has maintained a large captive baboon colony for more than 50 yr. Unlike other model organisms, however, the genomic resources for baboons are severely lacking. This has hindered the progress of studies using baboons as a model for basic biology or human disease. Here, we describe a data set of 100 high-coverage whole-genome sequences obtained from the mixed colony of olive (P. anubis) and yellow (P. cynocephalus) baboons housed at the SNPRC. These data provide a comprehensive catalog of common genetic variation in baboons, as well as a fine-scale genetic map. We show how the data can be used to learn about ancestry and admixture and to correct errors in the colony records. Finally, we investigated the consequences of inbreeding within the SNPRC colony and found clear evidence for increased rates of infant mortality and increased homozygosity of putatively deleterious alleles in inbred individuals.

The nutritional content of Tana River yellow baboon (Papio cynocephalus) foods in a partially forested habitat.

Here we report the first dietary macronutrient and mineral content information for a little-studied yellow baboon group (i.e., the Mchelelo troop) at the Tana River Primate National Reserve, Kenya. We compare forest to savanna samples for this troop found in a partially forested habitat. Observations conducted between 1988 and 1992 determined our list of foods. Subsequently, flora samples, representing 56 species, were collected between April 2008 and March 2009 with nutrient content determined via standard procedures for fiber, gross energy, ash/minerals, crude protein, and crude fat/lipids. Concentrations of specific minerals (calcium, iron, magnesium, manganese, phosphorus, potassium, zinc) were also measured. We predicted forest items would be higher in gross energy and lipids and savanna items higher in crude protein, fiber, and minerals. Our analyses support only the predicted difference in crude protein for savanna items for the overall dataset. In our examination of the top 15 foods, savanna items had significantly higher crude protein, ash, magnesium, and manganese while forest items had higher gross energy. Right-angled mixture triangles show some clustering by location but with substantial overlap in values. Our data provide further indication of the particularity and purposefulness of dietary choices made by primates. They also contribute to the broader discussions of primate nutritional ecology and are a first step towards an examination of macronutrient balancing for this group. Finally, we discuss the impact heavy reliance upon forest products by a "savanna species" may have upon competitors and forest composition. Ultimately, we show that there is still much to be learned about baboon nutrition.

Restricted MHC class I A locus diversity in olive and hybrid olive/yellow baboons from the Southwest National Primate Research Center.

Baboons are valuable models for complex human diseases due to their genetic and physiologic similarities to humans. Deep sequencing methods to characterize full-length major histocompatibility complex (MHC) class I (MHC-I) alleles in different nonhuman primate populations were used to identify novel MHC-I alleles in baboons. We combined data from Illumina MiSeq sequencing and Roche/454 sequencing to characterize novel full-length MHC-I transcripts in a cohort of olive and hybrid olive/yellow baboons from the Southwest National Primate Research Center (SNPRC). We characterized 57 novel full-length alleles from 24 baboons and found limited genetic diversity at the MHC-I A locus, with significant sharing of two MHC-I A lineages between 22 out of the 24 animals characterized. These shared alleles provide the basis for development of tools such as MHC:peptide tetramers for studying cellular immune responses in this important animal model.

Inverted intergeneric introgression between critically endangered kipunjis and yellow baboons in two disjunct populations.

Intergeneric hybridization and introgression was reported from one of two populations of the recently discovered kipunji (Rungwecebus kipunji), a critically endangered African monkey species of southern Tanzania. Kipunjis of the introgressed population (from Mount Rungwe) carry a mitochondrial DNA (mtDNA) haplotype closely related to those of parapatric yellow baboons (Papio cynocephalus), whereas the second kipunji population, in the Udzungwa Mountains, carries the original kipunji mtDNA haplotypes, which diverged from the baboon lineage about 3 million years ago. Interestingly, in our study of yellow baboons in Tanzania, we found that baboons from the southeastern boundary of the Udzungwa Mountains carry mtDNA haplotypes closely related to the original kipunji haplotype, whereas baboons from the northern boundary, as expected, carry mtDNA haplotypes of the northern yellow baboon clade. These findings provide evidence for a case of inverted intergeneric admixture in primates: (i) a baboon mtDNA haplotype introgressed the Mount Rungwe kipunji population by mitochondrial capture and (ii) an Udzungwa Mountains kipunji mtDNA haplotype introgressed a small subpopulation of yellow baboons by either mitochondrial capture or nuclear swamping. The baboon-kipunji example therefore constitutes an interesting system for further studies of the effects of genetic admixture on fitness and speciation.

Diet-induced early-stage atherosclerosis in baboons: Lipoproteins, atherogenesis, and arterial compliance.

BACKGROUND: The purpose of this study was to determine whether dietary manipulation can reliably induce early-stage atherosclerosis and clinically relevant changes in vascular function in an established, well-characterized non-human primate model. METHODS: We fed 112 baboons a high-cholesterol, high-fat challenge diet for two years. We assayed circulating biomarkers of cardiovascular disease (CVD) risk, at 0, 7, and 104 weeks into the challenge; assessed arterial compliance noninvasively at 104 weeks; and measured atherosclerotic lesions in three major arteries at necropsy. RESULTS: We observed evidence of atherosclerosis in all but one baboon fed the two-year challenge diet. CVD risk biomarkers, the prevalence, size, and complexity of arterial lesions, plus consequent arterial stiffness, were increased in comparison with dietary control animals. CONCLUSIONS: Feeding baboons a high-cholesterol, high-fat diet for two years reliably induces atherosclerosis, with risk factor profiles, arterial lesions, and changes in vascular function also seen in humans.

Group Living and Male Dispersal Predict the Core Gut Microbiome in Wild Baboons.

The mammalian gut microbiome plays a profound role in the physiology, metabolism, and overall health of its host. However, biologists have only a nascent understanding of the forces that drive inter-individual heterogeneity in gut microbial composition, especially the role of host social environment. Here we used 178 samples from 78 wild yellow baboons (Papio cynocephalus) living in two social groups to test how host social context, including group living, social interactions within groups, and transfer between social groups (e.g., dispersal) predict inter-individual variation in gut microbial alpha and beta diversity. We also tested whether social effects differed for prevalent "core" gut microbial taxa, which are thought to provide primary functions to hosts, versus rare "non-core" microbes, which may represent relatively transient environmental acquisitions. Confirming prior studies, we found that each social group harbored a distinct gut microbial community. These differences included both non-core and core gut microbial taxa, suggesting that these effects are not solely driven by recent gut microbial exposures. Within social groups, close grooming partners had more similar core microbiomes, but not non-core microbiomes, than individuals who rarely groomed each other, even controlling for kinship and diet similarity between grooming partners. Finally, in support of the idea that the gut microbiome can be altered by current social context, we found that the longer an immigrant male had lived in a given social group, the more closely his gut microbiome resembled the gut microbiomes of the group's long-term residents. Together, these results reveal the importance of a host's social context in shaping the gut microbiome and shed new light onto the microbiome-related consequences of male dispersal.

Ontogenetic changes in limb postures and their impact on effective limb length in baboons (Papio cynocephalus).

OBJECTIVES: Digitigrade hand and foot postures and extended elbows and knees are considered adaptations to running in cursorial mammals because they increase effective limb lengths (ELLs). However, the relationship between digitigrady and ELL in primates is not well understood. We documented the ontogeny of limb postures in baboons to better understand the function of digitigrady during walking. We hypothesized that the hand and foot would become more elevated and the elbow and knee more extended, leading to increased relative ELLs throughout ontogeny. MATERIALS AND METHODS: Longitudinal kinematic data were collected on four infant yellow baboons (Papio cynocephalus) as they aged from two to nine months, and again at two to three years. Hand/foot postures, elbow/knee angles, relative fore/hind limb ELLs, and dimensionless velocity were measured for 404 symmetrical walking strides. RESULTS: Digitigrade hand and foot postures were preferred at all ages. The elbow extended slightly and the knee flexed slightly with age. Elevated proximal hands, extended elbows, and extended knees were associated with long relative ELLs. For a given age, relative hind limb ELL was longer than relative forelimb ELL. DISCUSSION: In the forelimb, digitigrade hand postures and extended elbows function to increase relative ELL at slow walking velocity. Increased forelimb ELL may be an attempt to equalize forelimb and hind limb ELLs in baboons with an absolutely longer hind limb. Pedal digitigrady is not a main contributing factor to hind limb ELL. Results suggest that manual and pedal digitigrady in terrestrial cercopithecoids does not function to increase velocity.

Ovarian cycling and reproductive state shape the vaginal microbiota in wild baboons.

BACKGROUND: The vaginal microbiome is an important site of bacterial-mammalian symbiosis. This symbiosis is currently best characterized for humans, where lactobacilli dominate the microbial community and may help defend women against infectious disease. However, lactobacilli do not dominate the vaginal microbiota of any other mammal studied to date, raising key questions about the forces that shape the vaginal microbiome in non-human mammals. RESULTS: We used Illumina sequencing of the bacterial 16S rRNA gene to investigate variation in the taxonomic composition of the vaginal microbiota in 48 baboons (Papio cynocephalus), members of a well-studied wild population in Kenya. Similar to prior studies, we found that the baboon vaginal microbiota was not dominated by lactobacilli. Despite this difference, and similar to humans, reproductive state was the dominant predictor of baboon vaginal microbiota, with pregnancy, postpartum amenorrhea, and ovarian cycling explaining 18% of the variance in community composition. Furthermore, among cycling females, a striking 39% of variance in community composition was explained by ovarian cycle phase, with an especially distinctive microbial community around ovulation. Periovulatory females exhibited the highest relative abundance of lactic acid-producing bacteria compared to any other phase, with a mean relative abundance of 44%. To a lesser extent, sexual behavior, especially a history of shared sexual partners, also predicted vaginal microbial similarity between baboons. CONCLUSIONS: Despite striking differences in their dominant microbes, both human and baboon vaginal microbiota exhibit profound changes in composition in response to reproductive state, ovarian cycle phase, and sexual behavior. We found major shifts in composition during ovulation, which may have implications for disease risk and conception success. These findings highlight the need for future studies to account for fine-scale differences in reproductive state, particularly differences between the various phases of the ovarian cycle. Overall, our work contributes to an emerging understanding of the forces that explain intra- and inter-individual variation in the mammalian vaginal microbiome, with particular emphasis on its role in host health and disease risk.

Genomewide ancestry and divergence patterns from low-coverage sequencing data reveal a complex history of admixture in wild baboons.

Naturally occurring admixture has now been documented in every major primate lineage, suggesting its key role in primate evolutionary history. Active primate hybrid zones can provide valuable insight into this process. Here, we investigate the history of admixture in one of the best-studied natural primate hybrid zones, between yellow baboons (Papio cynocephalus) and anubis baboons (Papio anubis) in the Amboseli ecosystem of Kenya. We generated a new genome assembly for yellow baboon and low-coverage genomewide resequencing data from yellow baboons, anubis baboons and known hybrids (n = 44). Using a novel composite likelihood method for estimating local ancestry from low-coverage data, we found high levels of genetic diversity and genetic differentiation between the parent taxa, and excellent agreement between genome-scale ancestry estimates and a priori pedigree, life history and morphology-based estimates (r(2)  = 0.899). However, even putatively unadmixed Amboseli yellow individuals carried a substantial proportion of anubis ancestry, presumably due to historical admixture. Further, the distribution of shared vs. fixed differences between a putatively unadmixed Amboseli yellow baboon and an unadmixed anubis baboon, both sequenced at high coverage, is inconsistent with simple isolation-migration or equilibrium migration models. Our findings suggest a complex process of intermittent contact that has occurred multiple times in baboon evolutionary history, despite no obvious fitness costs to hybrids or major geographic or behavioural barriers. In combination with the extensive phenotypic data available for baboon hybrids, our results provide valuable context for understanding the history of admixture in primates, including in our own lineage.