Ecological and genetic variables co-vary with social group identity to shape the gut microbiome of a pair-living primate.

Primates exhibit diverse social systems that are intricately linked to their biology, behavior, and evolution, all of which influence the acquisition and maintenance of their gut microbiomes (GMs). However, most studies of wild primate populations focus on taxa with relatively large group sizes, and few consider pair-living species. To address this gap, we investigate how a primate's social system interacts with key environmental, social, and genetic variables to shape the GM in pair-living, red-bellied lemurs (Eulemur rubriventer). Previous research on this species suggests that social interactions within groups influence interindividual microbiome similarity; however, the impacts of other nonsocial variables and their relative contributions to gut microbial variation remain unclear. We sequenced the 16S ribosomal RNA hypervariable V4-V5 region to characterize the GM from 26 genotyped individuals across 11 social groups residing in Ranomafana National Park, Madagascar. We estimated the degree to which sex, social group identity, genetic relatedness, dietary diversity, and home range proximity were associated with variation in the gut microbial communities residing in red-bellied lemurs. All variables except sex played a significant role in predicting GM composition. Our model had high levels of variance inflation, inhibiting our ability to determine which variables were most predictive of gut microbial composition. This inflation is likely due to red-bellied lemurs' pair-living, pair-bonded social system that leads to covariation among environmental, social, and genetic variables. Our findings highlight some of the factors that predict GM composition in a tightly bonded, pair-living species and identify variables that require further study. We propose that future primate microbiome studies should simultaneously consider environmental, social, and genetic factors to improve our understanding of the relationships among sociality, the microbiome, and primate ecology and evolution.

Shared Environment and Genetics Shape the Gut Microbiome after Infant Adoption.

The composition of the human gut microbiome is highly variable, and this variation has been repeatedly tied to variation in human health. However, the sources of microbial variation remain unclear, especially early in life. It is particularly important to understand sources of early life variation in the microbiome because the state of the microbiome in childhood can influence lifelong health. Here, we compared the gut microbiomes of children adopted in infancy to those of genetically unrelated children in the same household and genetically related children raised in other households. We observed that a shared home environment was the strongest predictor of overall microbiome similarity. Among those microbial taxa whose variation was significantly explained by our models, the abundance of a given taxon was more frequently explained by host genetic similarity (relatedness), while the presence of a given taxon was more dependent upon a shared home environment. This suggests that although the home environment may act as a species source pool for the gut microbiome in childhood, host genetic factors likely drive variation in microbial abundance once a species colonizes the gut.IMPORTANCE Our results demonstrate that the early life home environment can significantly alter the gut microbiome in childhood, potentially altering health outcomes or risk for adverse health outcomes. A better understanding of the drivers of gut microbiome variation during childhood could lead to more effective intervention strategies for overall health starting in early life.

Divergence in gut microbial communities mirrors a social group fission event in a black-and-white colobus monkey (Colobus vellerosus).

Host behavior and social factors have increasingly been implicated in structuring the composition of gut microbial communities. In social animals, distinct microbial communities characterize different social groups across a variety of taxa, although little longitudinal research has been conducted that demonstrates how this divergence occurs. Our study addresses this question by characterizing the gut microbial composition of an African Old World monkey, the black-and-white colobus (Colobus vellerosus), before and after a social group fission event. Gut microbial taxonomic composition of these monkeys was profiled using the V-4 hypervariable region of the bacterial 16S ribosomal RNA gene, and pairwise-relatedness values were calculated for all individuals using 17 short tandem repeat loci and partial pedigree information. The two social groups in this study were found to harbor distinct microbial signatures after the fission event from which they emerged, while these communities were not divergent in the same individuals before this event. Three genera were found to differ in abundance between the two new social groups: Parabacteroides, Coprococcus, and Porphyromonadaceae. Additionally, although this fission happened partially along lines of relatedness, relatedness did not structure the differences that we found. Taken together, this study suggests that distinct gut microbial profiles can emerge in social groups in <1 year and recommends further work into more finely mapping the timescales, causes, and potentially adaptive effects of this recurring trend toward distinct group microbial signatures.