Characterizing the vaginal microbiome in a sexually fluid primate (Pan paniscus).

While there have been recent breakthroughs in human vaginal microbiome research, very few non-human primate (NHP) vaginal microbiome studies exist due to difficulty in obtaining samples. In this study, we sought to: (1) characterize the bonobo vaginal microbiota for the first time, and (2) determine the relationship between vaginal pH and swelling size. During a 21-day study period, we collected observational data and 71 vaginal swabs from three cohoused adult females at the Ape Cognition and Conservation Initiative. After filtering and classification, a total of 3452 amplicon sequence variants were recruited from 12 vaginal samples. The most dominant phylum represented was Actinobacteria, and the most abundant genera were Gardnerella, Atopobium, and Prevotella. The mean pH score was 6.1 (range: 5.1-7.0), and pH levels varied with relative swelling size. This is the first study to examine the vaginal microbial composition in this species, and it conforms to previous NHP studies in that there was not the same bacterial dominance of Lactobacillus spp. often highlighted in human vaginal microbiota studies. Our findings suggest there may be other factors contributing to the protection of the bonobo vaginal environment, but future analysis of a larger sample is needed to fully understand how sociality and sexuality shape vaginal microbiota and host health.

Social network dynamics, infant loss, and gut microbiota composition in female Colobus vellerosus during time periods with alpha male challenges.

The gut microbiota of group-living animals is strongly influenced by their social interactions, but it is unclear how it responds to social instability. We investigated whether social instability associated with the arrival of new males and challenges to the alpha male position could explain differences in the gut microbiota in adult female Colobus vellerosus at Boabeng-Fiema, Ghana. First, we used a data set collected during May-August 2007 and May 2008-2009 that consisted of (i) 50 fecal samples from adult females in eight social groups for V4 16S rRNA sequencing to determine gut microbiota composition, and (ii) demographic and behavioral data ad libitum to determine male immigration, challenges to the alpha male position, and infant births and deaths. Sørensen and Bray-Curtis beta diversity indices (i.e., between-sample microbiota variation) were predicted by year, alpha male stability, group identity, and age. Next, we used a more detailed behavioral data set collected during focal observations of adult females in one group with a prolonged alpha male takeover and three cases of infant loss, to create 12-month versus 3-month 1-m proximity networks that preceded and overlapped the gut microbiome sampling period in that group. The long versus short-term networks were not correlated, suggesting temporal variation in proximity networks. In this group, beta diversity among the five adult females was predicted by similarity in infant loss status and short-term (rather than yearly) 1-m proximity ties. Although the mechanism driving this association needs to be further investigated in future studies, our findings indicate that alpha male takeovers are associated with gut microbiota variation and highlight the importance of taking demographic and social network dynamics into account.

Non-Reproductive Sexual Behavior in Wild White-Thighed Colobus Monkeys (Colobus vellerosus).

Rare behaviors are often missing from published papers, hampering phylogenetic analyses. Here, we report, for the first time, masturbation and same-sex sexual behavior (SSB) in both male and female black-and-white colobus monkeys. We recorded these behaviors during 32 months of observation (1573 h of focal animal sampling) on Colobus vellerosus collected at the Boabeng-Fiema Monkey Sanctuary in Ghana. Males were observed masturbating and involved in SSB more than females. Subadult males were the age-sex class that engaged in both of these behaviors most often and a third of all SSB observed in young males occurred when they were forming an all-male band (AMB), which are temporally transient social groups in this species. Our data support that masturbation in males may be a sexual outlet for individuals that do not have a current sexual partner, while in females it may function in mate attraction by advertising receptivity. SSB may occur as an evolutionary byproduct but given the temporal clustering of observed events in males prior to AMB formation, our data best support the hypothesis that these behaviors facilitate male-male bonding (i.e., act as social glue). Within AMB's, males engage in coalitionary behavior to take over social groups containing females and strong bonds are important for success and later access to females, which could have selected for SSB in C. vellerosus.

Impact of individual demographic and social factors on human-wildlife interactions: a comparative study of three macaque species.

Despite increasing conflict at human-wildlife interfaces, there exists little research on how the attributes and behavior of individual wild animals may influence human-wildlife interactions. Adopting a comparative approach, we examined the impact of animals' life-history and social attributes on interactions between humans and (peri)urban macaques in Asia. For 10 groups of rhesus, long-tailed, and bonnet macaques, we collected social behavior, spatial data, and human-interaction data for 11-20 months on pre-identified individuals. Mixed-model analysis revealed that, across all species, males and spatially peripheral individuals interacted with humans the most, and that high-ranking individuals initiated more interactions with humans than low-rankers. Among bonnet macaques, but not rhesus or long-tailed macaques, individuals who were more well-connected in their grooming network interacted more frequently with humans than less well-connected individuals. From an evolutionary perspective, our results suggest that individuals incurring lower costs related to their life-history (males) and resource-access (high rank; strong social connections within a socially tolerant macaque species), but also higher costs on account of compromising the advantages of being in the core of their group (spatial periphery), are the most likely to take risks by interacting with humans in anthropogenic environments. From a conservation perspective, evaluating individual behavior will better inform efforts to minimize conflict-related costs and zoonotic-risk.