Reproductive endocrinology of wild female woolly monkeys (Lagothrix lagotricha poeppigii) during puberty, ovarian cyclicity, and pregnancy.

Behavioral observations can provide clues about female reproductive status. However, the study of the endocrine dynamics that underlie processes such as puberty, ovulation, conception, and gestation, may help increase our understanding of female reproductive biology. We used noninvasive methods to study female reproductive endocrinology in wild woolly monkeys (genus Lagothrix). We extracted ovarian steroid hormones from fecal samples collected non-invasively to examine changes in the concentrations of progesterone and estrogen metabolites (pregnanediol-3-glucuronide and estrone-3-glucuronide, respectively) during periods of female puberty, ovarian cyclicity, and pregnancy. The two subadult females in our study showed significant increases in ovarian hormone concentrations before disappearing and presumably dispersing, suggesting that they might reach the onset of puberty before emigrating from their natal groups. Ovarian cycle length in adult females was, on average, ~22 days (N = 21). Of the 10 cycling females, five conceived and four gave birth to offspring, with an average gestation period of ~214 days, but the infant born to the female with the shortest estimated gestation period (182 days) disappeared within a month after parturition. The fact that less than half of all cycling females conceived, and that only three out of five of those females gave birth to offspring that survived past the first month, suggests that reproduction is energetically costly for female woolly monkeys. Ovarian cycle length and gestation period among woolly monkeys are similar to those in their closest relatives, spider monkeys and muriquis suggesting that reproductive physiology may be highly conserved among females within the Tribe Atelini.

Social groups constrain the spatiotemporal dynamics of wild sifaka gut microbiomes.

Primates acquire gut microbiota from conspecifics through direct social contact and shared environmental exposures. Host behaviour is a prominent force in structuring gut microbial communities, yet the extent to which group or individual-level forces shape the long-term dynamics of gut microbiota is poorly understood. We investigated the effects of three aspects of host sociality (social groupings, dyadic interactions, and individual dispersal between groups) on gut microbiome composition and plasticity in 58 wild Verreaux's sifaka (Propithecus verreauxi) from six social groups. Over the course of three dry seasons in a 5-year period, the six social groups maintained distinct gut microbial signatures, with the taxonomic composition of individual communities changing in tandem among coresiding group members. Samples collected from group members during each season were more similar than samples collected from single individuals across different years. In addition, new immigrants and individuals with less stable social ties exhibited elevated rates of microbiome turnover across seasons. Our results suggest that permanent social groupings shape the changing composition of commensal and mutualistic gut microbial communities and thus may be important drivers of health and resilience in wild primate populations.

Reproductive seasonality in two sympatric primates (Ateles belzebuth and Lagothrix lagotricha poeppigii) from Amazonian Ecuador.

With their large body size and "slow" life histories, atelin primates are thought to follow a risk-averse breeding strategy, similar to capital breeders, in which they accumulate energy reserves in anticipation of future reproductive events such as gestation and lactation. However, given the paucity of longitudinal data from wild populations, few studies to date have been able to compare the timing of reproductive events (e.g., copulations, conceptions, and births) in relation to shifting resource availability over multiple years. We examined the reproductive patterns of two atelin species-white-bellied spider monkeys (Ateles belzebuth) and lowland woolly monkeys (Lagothrix lagotricha poeppigii)-in relation to habitat-wide estimates of fruit availability at the Tiputini Biodiversity Station (TBS) in Amazonian Ecuador. Our sample included 4 years of data on births (N = 36) and copulations (N = 170) for Lagothrix, 10 years of data on births (N = 35) and copulations (N = 74) for Ateles, and 7 years of data on ripe fruit availability. Reproductive events were distinctly seasonal. For both species, births were concentrated between May and September, a time period in which ripe fruit was relatively scarce, while inferred conceptions occurred between September and January, when ripe fruit availability was increasing and maintained at high-levels throughout the forest. Interannual variation in births was relatively stable, except for in 2016 when twice as many infants were born following a strong El Niño event that may have led to unusually high levels of fruit productivity during the 2015 breeding season. Although copulations were observed year-round, an overwhelming majority (>90% for Lagothrix and >80% for Ateles) took place between August and February when females were most likely to conceive. Collectively, these data follow the reproductive patterns observed in other atelin primates, and, as proposed by others, suggest that atelins may follow a risk-averse breeding strategy.

Hierarchical social networks shape gut microbial composition in wild Verreaux's sifaka.

In wild primates, social behaviour influences exposure to environmentally acquired and directly transmitted microorganisms. Prior studies indicate that gut microbiota reflect pairwise social interactions among chimpanzee and baboon hosts. Here, we demonstrate that higher-order social network structure-beyond just pairwise interactions-drives gut bacterial composition in wild lemurs, which live in smaller and more cohesive groups than previously studied anthropoid species. Using 16S rRNA gene sequencing and social network analysis of grooming contacts, we estimate the relative impacts of hierarchical (i.e. multilevel) social structure, individual demographic traits, diet, scent-marking, and habitat overlap on bacteria acquisition in a wild population of Verreaux's sifaka (Propithecus verreauxi) consisting of seven social groups. We show that social group membership is clearly reflected in the microbiomes of individual sifaka, and that social groups with denser grooming networks have more homogeneous gut microbial compositions. Within social groups, adults, more gregarious individuals, and individuals that scent-mark frequently harbour the greatest microbial diversity. Thus, the community structure of wild lemurs governs symbiotic relationships by constraining transmission between hosts and partitioning environmental exposure to microorganisms. This social cultivation of mutualistic gut flora may be an evolutionary benefit of tight-knit group living.