Ecological forces shaping gut microbiota in wild animal populations

Ren, Tiantian, Biology - Graduate School of Arts and Sciences, University of Virginia
Wu, Martin, Department of Biology, University of Virginia
Brodie, Edmund, Department of Biology, University of Virginia
Antonovics, Janis, Department of Biology, University of Virginia
Cox, Robert, Department of Biology, University of Virginia
Papin, Jason, Department of Biomedical Engineering, University of Virginia

Trillions of bacteria colonize the digestive tracts of animals and form complex communities known as gut microbiota. Gut microbiota play important roles in diverse aspects of host biology, including nutrition, immune system development and behavior. Changes in gut microbial composition have been linked to a plethora of health and disease states. Previous studies on human and laboratory animals have shown that host diet, age, sex, genetics, environmental exposure all drive normal gut microbial variation. However, the ecological forces that shape gut microbial community structure in wild animal populations remain largely unknown. Studying gut microbiota in host’s natural environment is crucial because it is where the actual actions of microbes-host coevolution take place. In this dissertation, I investigated the ecological forces shaping gut microbial communities in three wild animal populations, with each tackling the problem from a different angle. First, I conducted a longitudinal and cross-sectional study of gut microbiota in a well-studied population of wild baboons. Baboon gut microbiota were typical of omnivorous primates, and host age and diet had strong effects 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. Next, I conducted a comprehensive study of the temporal and spatial dynamics of gut microbiota of a well-studied red squirrel population. Red squirrels represent a very attractive system for studying gut microbial biogeography because they are territorial and experience strong seasonal fluctuations in their environment. This study revealed significant spatial patterns and seasonal rhythm of gut microbiota within a host population. Beyond the environmental effects, I also found evidences for individuality and maternal effect in red squirrel gut microbiota. Lastly, to test whether and how host adaptive radiations structure the composition of microbial communities, I investigated the gut microbiota of seven species of Anolis lizards belonging to three “ecomorphs” on Puerto Rico and Florida. Our results indicate that gut microbial communities are only weakly shaped by the diversification of their lizard hosts due to the strikingly high levels of microbial variation observed within Anolis species. In summary, I have characterized the temporal, spatial and phylogenetic patterns of gut microbiota in three different wild animal hosts, and identified various environmental and host factors underlying these patterns. These findings may contribute towards a better understanding of how ecological processes govern the gut microbial diversity in natural environment.

PHD (Doctor of Philosophy)
Microbiota, Wild animal, Gut microbiome
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