SOCIOECOLOGICAL PREDICTORS OF MICROBIOME VARIATION IN WILD POPULATIONS OF AFRICAN MAMMALS

Host-associated microbial communities (e.g. microbiomes) influence multiple aspects of their host’s phenotype. Over a decade of research shows that the microbiome can vary with both host factors and environmental factors. However, much of the existing literature has been limited to intestinal microbiomes and to laboratory and domesticated animals. Multi-body site and longitudinal analyses of the microbiomes of wild mammals are lacking. Here, I address these gaps in knowledge and use DNA sequencing to survey the microbiomes of a highly gregarious carnivore, the spotted hyena (Crocuta crocuta). Due to their complex societies, spotted hyenas offer an excellent model system for investigating how host physiology and ecology interact with the microbiome, and for elucidating the contributions of the microbiome to host function. In this dissertation, I leverage over three decades of data and samples collected by my adviser from wild hyenas residing in the Masai Mara National Reserve, Kenya (MMNR). Because this dissertation involved many collaborations with other scientists, I use the first person plural throughout this dissertation. In Chapter 1, I evaluate whether the microbiomes at six body-sites vary with host age, sex, and social rank in spotted hyenas, and find that the microbiome is distinct among body sites, and that this differentiation in microbiomes occurs early in life. For Chapter 2, I conduct a longitudinal analysis of the gut microbiome across 3 generations of spotted hyenas from 4 lineages, and elucidate the potential ways gut microbes may be contributing to their host’s digestion of animal carcasses. Findings show that the composition of the gut microbiome is highly variable across time, but its functional repertoire of genes is highly consistent. Furthermore, our analyses reveal that the abundances of bacterial taxa are associated with long-term ecological changes in livestock grazing, anthropogenic disturbance, and herbivore densities that occurred in the Masai Mara reserve. Chapter 3 inquires whether host social interactions and close associations between individuals shape gut microbiota similarity and diversity in a social group of spotted hyenas, which exhibit fission-fusion dynamics. Consistent with our hypothesis, close hyena affiliates share a greater number of bacterial types than hyena dyads that rarely encountered one another, but contrary to our hypothesis, more socially connected individuals do not harbor more diverse gut microbiotas than more isolated individuals. Chapter 4 compares the gut microbiomes of 11 species of sympatric African herbivores from the MMNR and Laikipia region in Kenya, and determines the relative influence of host diet and host phylogenetic relatedness in structuring the microbiome. My findings indicate that across distantly related hosts, herbivore gut microbiotas are strongly shaped by host phylogenetic relatedness and taxonomy, but among closely related hosts, host diet explains the most variation in the gut microbiota. Findings suggest that the gut microbiota is species-specific, but can be further modified by host ecology, including host diet and geography, especially among closely related host species. Overall, my dissertation provides novel insight regarding the factors shaping the gut microbiome in wild carnivores and herbivores, at individual, group-level, and ecosystem-wide scales.