Group membership, not diet, structures the composition and functional potential of the gut microbiome in a wild primate.

The gut microbiome has the potential to buffer temporal variations in resource availability and consumption, which may play a key role in the ability of animals to adapt to a broad range of habitats. We investigated the temporal composition and function of the gut microbiomes of wild common marmosets (Callithrix jacchus) exploiting a hot, dry environment-Caatinga-in northeastern Brazil. We collected fecal samples during two time periods (July-August and February-March) for 2 years from marmosets belonging to eight social groups. We used 16S rRNA gene amplicon sequencing, metagenomic sequencing, and butyrate RT-qPCR to assess changes in the composition and potential function of their gut microbiomes. Additionally, we identified the plant, invertebrate, and vertebrate components of the marmosets' diet via DNA metabarcoding. Invertebrate, but not plant or vertebrate, consumption varied across the year. However, gut microbiome composition and potential function did not markedly vary across study periods or as a function of diet composition. Instead, the gut microbiome differed markedly in both composition and potential function across marmosets residing in different social groups. We highlight the likely role of factors, such as behavior, residence, and environmental heterogeneity, in modulating the structure of the gut microbiome. IMPORTANCE: In a highly socially cohesive and cooperative primate, group membership more strongly predicts gut microbiome composition and function than diet.

The relationship between pinworm (Trypanoxyuris) infection and gut bacteria in wild black howler monkeys (Alouatta pigra).

Gut bacteria may coexist with other groups of organisms, such as nematode parasites, that inhabit the gastrointestinal tract of primates; however, the possible effects of endoparasites on bacterial communities are frequently overlooked. Here we explored whether infection with Trypanoxyuris, an oxyurid gastrointestinal parasite, is associated with changes in the gut bacterial community of wild black howler monkeys (Alouatta pigra), by comparing gut bacterial communities of consistently infected individuals and individuals that never tested positive for Trypanoxyuris throughout different months across the year. We additionally controlled for other sources of variation reported to influence the primate microbiome including individual identity, social group, and seasonality. Trypanoxyuris infection was not related to differences in gut bacterial alpha diversity, but was weakly associated with differences in gut bacterial community structure. In contrast, among the covariates considered, both individual identity and social group were more strongly associated with variation in the howler gut bacterial community. Our results suggest that gastrointestinal parasites may be associated, to some extent, with shifts in the gut bacterial communities hosted by free-ranging primates, although a causal link still needs to be established. Further studies of wild primate hosts infected with parasite species with different pathogenicity are needed to better elucidate health-related consequences from the parasite-microbiome interplay.

The gut microbiome and metabolome of saddleback tamarins (Leontocebus weddelli): Insights into the foraging ecology of a small-bodied primate.

Body mass is a strong predictor of diet and nutritional requirements across a wide range of mammalian taxa. In the case of small-bodied primates, because of their limited gut volume, rapid food passage rate, and high metabolic rate, they are hypothesized to maintain high digestive efficiency by exploiting foods rich in protein, fats, and readily available energy. However, our understanding of the dietary requirements of wild primates is limited because little is known concerning the contributions of their gut microbiome to the breakdown and assimilation of macronutrients and energy. To study how the gut microbiome contributes to the feeding ecology of a small-bodied primate, we analyzed the fecal microbiome composition and metabolome of 22 wild saddleback tamarins (adult body mass 360-390 g) in Northern Bolivia. Samples were analyzed using high-throughput Illumina sequencing of the 16 S rRNA gene V3-V5 regions, coupled with GC-MS metabolomic profiling. Our analysis revealed that the distal microbiome of Leontocebus weddelli is largely dominated by two main bacterial genera: Xylanibacter and Hallella (34.7 ± 14.7 and 22.6 ± 12.4%, respectively). A predictive analysis of functions likely carried out by bacteria in the tamarin gut demonstrated the dominance of membrane transport systems and carbohydrate metabolism as the predominant metabolic pathways. Moreover, given a fecal metabolome composed mainly of glucose, fructose, and lactic acid (21.7 ± 15.9%, 16.5 ± 10.7%, and 6.8 ± 5.5%, respectively), the processing of highly fermentable carbohydrates appears to play a central role in the nutritional ecology of these small-bodied primates. Finally, the results also show a potential influence of environmentally-derived bacteria in colonizing the tamarin gut. These results indicate high energetic turnover in the distal gut of Weddell's saddleback tamarin, likely influenced by dominant bacterial taxa that facilitate dietary dependence on highly digestible carbohydrates present in nectar, plant exudates, and ripe fruits.

The microbial reproductive ecology of white-faced capuchins (Cebus capucinus).

Changes in reproductive status influence energy and nutrient requirements in female primates. The gut microbiota may buffer changes in energy demands, with shifts in community composition increasing the energy production potential of the gut during pregnancy and lactation. In this study, we examine changes in the gut microbiome of wild, female white-faced capuchins (Cebus capucinus) across different reproductive states. Fecal samples (n = 39) were collected from five adult females over the course of a year. Gut microbial community composition was assessed using 16S rRNA gene sequences, and PICRUSt was used to make metagenomic functional predictions. We found a significant relationship between reproductive state and both the structure and predicted function of the gut microbiome, neither of which were associated with host diet. For example, the relative abundance of Firmicutes was significantly lower in lactating females compared with cycling females; the relative abundance of Actinobacteria was significantly higher in pregnant females compared with lactating females, and there was a trend toward higher relative abundances of Proteobacteria in pregnant females compared with cycling females. The results of this study suggest that, in addition to behavioral and dietary adaptions, the gut microbiota may play a role in allowing female primates to meet their changing energetic needs during reproduction. Further studies of the "microbial reproductive ecology" of primates will help advance our understanding of gut microbial contributions to primate energetics.

Influence of fruit and invertebrate consumption on the gut microbiota of wild white-faced capuchins (Cebus capucinus).

OBJECTIVES: Invertebrate consumption is thought to be an integral part of early hominin diets, and many modern human populations regularly consume insects and other arthropods. This study examines the response of gut microbial community structure and function to changes in diet in wild white-faced capuchins (Cebus capucinus), a primate that incorporates a large proportion of invertebrates in its diet. The goal of the study is to better understand the role of both fruit and invertebrate prey consumption on shaping primate gut microbiomes. MATERIALS AND METHODS: Fecal samples (n = 169) and dietary data were collected over 12 months. The V3-V5 region of microbial 16S rRNA genes was amplified and sequenced. The IM-TORNADO pipeline was used to analyze sequences. RESULTS: White-faced capuchin gut bacterial communities were characterized primarily by Firmicutes (41.6%) and Proteobacteria (39.2%). There was a significant relationship between the invertebrate diet composition of individual capuchins and their gut microbiome composition. However, there was no relationship between the fruit diet composition of individual capuchins and their gut microbiome composition, even when examining multiple timescales. DISCUSSION: The results of our study indicate that there is a stronger relationship between gut microbial community structure and invertebrate diet composition than between gut microbial community structure and fruit consumption. As invertebrates and other animal prey play an important role in the diet of many primates, these results give important insight into the role of faunivory in shaping the evolution of host-microbe interactions in primates.