Social relationships: key to gut microbiome composition in wild redfronted lemurs?

Abstract

The gut microbiome consists of the prokaryotic and eukaryotic communities inhabiting the gastrointestinal tract of an animal and plays a pivotal role in the health of the host. This microbial community is highly dynamic and the factors driving these fluctuations remain to be determined. This thesis presents a longitudinal study investigating the factors that shape the gut microbiome of wild redfronted lemurs aiming to detect an impact from social relationships. Social relationships can influence the gut microbiome directly through transmission of microorganisms during social interactions, or indirectly through activation of the hypothalamic-pituitary-adrenal (HPA) axis due to social stressors. In Chapter 2 the temporal variations in the diverse microbial communities of redfronted lemurs were analyzed. The study showed that fluctuations in diet, affiliative interactions, and precipitation impact the bacterial entire and active community. Temporal variations in bacterial diversity were driven by swift changes in the food items consumed (fruits, flowers, and leaves), affiliative interactions and precipitation. Feeding on leaves increased bacterial alpha diversity whereas feeding on flowers and higher precipitation decreased bacterial diversity. Feeding on flowers and fruits and affiliative interactions affected the gut microbiome composition. Specific bacterial genera associated to feeding on flowers and fruits, affiliative interactions, and precipitation were detected. Fermenters of polysaccharides and glycolipids like Succinivibrio, Oscillospiraceae, Prevotellaceae, and Anaerovibrio were positively affected with consumption of flowers and fruits. Rikenellaceae, Alloprevotella, Kiritimatiellae, and Spirochaetaceae were positively affected by affiliative interactions. Higher precipitation had a negative impact on Kiritimatiellae, suggesting that this order is acquired from other water sources only present during the dry season. Thus, showing that the investigated factors shape the longitudinal dynamics of the gut microbiome. Chapter 3 focused on the investigation of environmental selection in the gut niche due to host’s sex, age, HPA axis activation, parasite richness, diet and water intake. Additionally, dispersal processes of microorganisms between hosts through social interactions and with environmental water were examined. Bacterial alpha diversity increased with higher fecal glucocorticoid metabolite (fGCM) measurements, consumption on leaves, while being significantly lower in one group. Group membership, fGCM levels and precipitation explained the highest amount of variation in beta diversity. Associations between bacterial genera and all studied factors were detected, excluding host’s sex. For instance, Tyzzerella associated with higher fGCM concentrations whereas genera from Helicobacteraceae and Mycoplasmataceae presented negative associations. Parasite richness associated to changes in abundances of bacterial genera but had a small impact on bacterial beta diversity. As reported in humans, Succinivibrio and Verrucomicrobiota associated positively with parasite richness while genera from Lachnospiraceae had negative associations. Correlations between bacterial indicator taxa and social networks were detected, suggesting transmission of bacteria through social interactions. Thus, environmental selection at the gut niche and dispersal processes of microorganisms between hosts and the environment influenced the gut microbiome at different intensities. Finally, Chapter 4 reviews the impact of social behaviors in primates and their influence on parasite transmission and susceptibility to disease. Group-living provides advantages for an individual but also increases exposure to parasites. The same processes associated to parasite transmission and susceptibility can be important drivers of the gut microbiome. Thus, this knowledge and methods used in these investigations can be applicable to the study of the gut microbiome. In conclusion, this project demonstrates that social relationships impact the gut microbiome directly through social interactions, group membership and indirectly through HPA axis activation. Diet and precipitation are important drivers of the temporal variations in the gut microbiome. Parasite richness impacted the abundance of bacterial genera but not diversity, possibly because bacteria-parasite interactions are species specific. The detection of the temporal variations of the gut microbiome of wild redfronted lemurs and its drivers was possible due to the longitudinal setup with a dense sampling regime coupled with the collection of focal behavioral data and environmental records. Thus, the temporal dynamics of the gut microbiome of wild redfronted lemurs are shaped by factors inside and outside the hosts, including the dispersal processes of bacteria between hosts through social interactions.