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.

Development, diet and dynamism: longitudinal and cross-sectional predictors of gut microbial communities in wild baboons.

Gut bacterial communities play essential roles in host biology, but to date we lack information on the forces that shape gut microbiota between hosts and over time in natural populations. Understanding these forces in wild primates provides a valuable comparative context that enriches scientific perspectives on human gut microbiota. To this end, we tested predictors of gut microbial composition in a well-studied population of wild baboons. Using cross-sectional and longitudinal samples collected over 13 years, we found that baboons harbour gut microbiota typical of other omnivorous primates, albeit with an especially high abundance of Bifidobacterium. Similar to previous work in humans and other primates, we found strong effects of both developmental transitions and diet on gut microbial composition. Strikingly, baboon gut microbiota appeared to be highly dynamic such that samples collected from the same individual only a few days apart were as different from each other as samples collected over 10 years apart. Despite the dynamic nature of baboon gut microbiota, we identified a set of core taxa that is common among primates, supporting the hypothesis that microbiota codiversify with their host species. Our analysis identified two tentative enterotypes in adult baboons that differ from those of humans and chimpanzees.

Erratum for Grieneisen and Blekhman, "Crowdsourcing Our National Gut".

[This corrects the article DOI: 10.1128/mSystems.00060-18.].

Crowdsourcing Our National Gut.

The microbes of the human intestinal tract play a profound role in our health. The complex interactions between our gut microbial communities and the external environment, and the resulting functional consequences, can be difficult to disentangle. To address this problem, McDonald et al. (mSystems 3:e00031-18, 2018, https://doi.org/10.1128/mSystems.00031-18) present the first set of results from the American Gut Project, a citizen science-based data set currently comprised of over 10,000 gut microbiome samples and associated life history data. By combining this extensive data set with other published studies, the authors uncover novel relationships between gut microbiome structure and function. For example, they found that dietary plant diversity and recent antibiotic use predict both microbial and metabolomic diversity. McDonald et al. also demonstrate that there is high diversity across human gut microbiomes, even compared to the diversity of environmental microbiomes. The results from this study illuminate the potential of the citizen science approach to further our knowledge of host-associated microbial communities.

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.

Common methods for fecal sample storage in field studies yield consistent signatures of individual identity in microbiome sequencing data.

Field studies of wild vertebrates are frequently associated with extensive collections of banked fecal samples-unique resources for understanding ecological, behavioral, and phylogenetic effects on the gut microbiome. However, we do not understand whether sample storage methods confound the ability to investigate interindividual variation in gut microbiome profiles. Here, we extend previous work on storage methods for gut microbiome samples by comparing immediate freezing, the gold standard of preservation, to three methods commonly used in vertebrate field studies: lyophilization, storage in ethanol, and storage in RNAlater. We found that the signature of individual identity consistently outweighed storage effects: alpha diversity and beta diversity measures were significantly correlated across methods, and while samples often clustered by donor, they never clustered by storage method. Provided that all analyzed samples are stored the same way, banked fecal samples therefore appear highly suitable for investigating variation in gut microbiota. Our results open the door to a much-expanded perspective on variation in the gut microbiome across species and ecological contexts.

Sex and hibernaculum temperature predict survivorship in white-nose syndrome affected little brown myotis (Myotis lucifugus).

White-nose syndrome (WNS), an emerging infectious disease caused by the novel fungus Pseudogymnoascus destructans, has devastated North American bat populations since its discovery in 2006. The little brown myotis, Myotis lucifugus, has been especially affected. The goal of this 2-year captive study was to determine the impact of hibernacula temperature and sex on WNS survivorship in little brown myotis that displayed visible fungal infection when collected from affected hibernacula. In study 1, we found that WNS-affected male bats had increased survival over females and that bats housed at a colder temperature survived longer than those housed at warmer temperatures. In study 2, we found that WNS-affected bats housed at a colder temperature fared worse than unaffected bats. Our results demonstrate that WNS mortality varies among individuals, and that colder hibernacula are more favourable for survival. They also suggest that female bats may be more negatively affected by WNS than male bats, which has important implications for the long-term survival of the little brown myotis in eastern North America.

Social networks predict gut microbiome composition in wild baboons.

Social relationships have profound effects on health in humans and other primates, but the mechanisms that explain this relationship are not well understood. Using shotgun metagenomic data from wild baboons, we found that social group membership and social network relationships predicted both the taxonomic structure of the gut microbiome and the structure of genes encoded by gut microbial species. Rates of interaction directly explained variation in the gut microbiome, even after controlling for diet, kinship, and shared environments. They therefore strongly implicate direct physical contact among social partners in the transmission of gut microbial species. We identified 51 socially structured taxa, which were significantly enriched for anaerobic and non-spore-forming lifestyles. Our results argue that social interactions are an important determinant of gut microbiome composition in natural animal populations-a relationship with important ramifications for understanding how social relationships influence health, as well as the evolution of group living.

The influence of social structure, habitat, and host traits on the transmission of Escherichia coli in wild elephants.

Social structure is proposed to influence the transmission of both directly and environmentally transmitted infectious agents. However in natural populations, many other factors also influence transmission, including variation in individual susceptibility and aspects of the environment that promote or inhibit exposure to infection. We used a population genetic approach to investigate the effects of social structure, environment, and host traits on the transmission of Escherichia coli infecting two populations of wild elephants: one in Amboseli National Park and another in Samburu National Reserve, Kenya. If E. coli transmission is strongly influenced by elephant social structure, E. coli infecting elephants from the same social group should be genetically more similar than E. coli sampled from members of different social groups. However, we found no support for this prediction. Instead, E. coli was panmictic across social groups, and transmission patterns were largely dominated by habitat and host traits. For instance, habitat overlap between elephant social groups predicted E. coli genetic similarity, but only in the relatively drier habitat of Samburu, and not in Amboseli, where the habitat contains large, permanent swamps. In terms of host traits, adult males were infected with more diverse haplotypes, and males were slightly more likely to harbor strains with higher pathogenic potential, as compared to adult females. In addition, elephants from similar birth cohorts were infected with genetically more similar E. coli than elephants more disparate in age. This age-structured transmission may be driven by temporal shifts in genetic structure of E. coli in the environment and the effects of age on bacterial colonization. Together, our results support the idea that, in elephants, social structure often will not exhibit strong effects on the transmission of generalist, fecal-oral transmitted bacteria. We discuss our results in the context of social, environmental, and host-related factors that influence transmission patterns.

Frequent arousal from hibernation linked to severity of infection and mortality in bats with white-nose syndrome.

White-nose syndrome (WNS), an emerging infectious disease that has killed over 5.5 million hibernating bats, is named for the causative agent, a white fungus (Geomyces destructans (Gd)) that invades the skin of torpid bats. During hibernation, arousals to warm (euthermic) body temperatures are normal but deplete fat stores. Temperature-sensitive dataloggers were attached to the backs of 504 free-ranging little brown bats (Myotis lucifugus) in hibernacula located throughout the northeastern USA. Dataloggers were retrieved at the end of the hibernation season and complete profiles of skin temperature data were available from 83 bats, which were categorized as: (1) unaffected, (2) WNS-affected but alive at time of datalogger removal, or (3) WNS-affected but found dead at time of datalogger removal. Histological confirmation of WNS severity (as indexed by degree of fungal infection) as well as confirmation of presence/absence of DNA from Gd by PCR was determined for 26 animals. We demonstrated that WNS-affected bats aroused to euthermic body temperatures more frequently than unaffected bats, likely contributing to subsequent mortality. Within the subset of WNS-affected bats that were found dead at the time of datalogger removal, the number of arousal bouts since datalogger attachment significantly predicted date of death. Additionally, the severity of cutaneous Gd infection correlated with the number of arousal episodes from torpor during hibernation. Thus, increased frequency of arousal from torpor likely contributes to WNS-associated mortality, but the question of how Gd infection induces increased arousals remains unanswered.