Fine-scale spatial variation shape fecal microbiome diversity and composition in black-tailed prairie dogs (Cynomys ludovicianus)

Background: Host associated gut microbiota are important in understanding the coevolution of host-microbe, and how they may help wildlife populations to adapt to rapid environmental changes. Mammalian gut microbiota composition and diversity may be affected by a variety of factors including geographic variation, seasonal variation in diet, habitat disturbance, environmental conditions, age, and sex. However, there have been few studies that examined how ecological and environmental factors influence gut microbiota composition in animals' natural environments. In this study, we explore how host habitat, geographical location and environmental factors affect the fecal microbiota of Cynomys ludovicianus at a small spatial scale. We collected fecal samples from five geographically distinct locations in the Texas Panhandle classified as urban and rural areas and analyzed them using high throughput 16S rRNA gene amplicon sequencing. Results: The results showed that microbiota of these fecal samples was largely dominated by the phylum Bacteroidetes. Fecal microbiome diversity and composition differed significantly across sampling sites and habitats. Prairie dogs inhabiting urban areas showed reduced fecal diversity due to more homogenous environment and, likely, anthropogenic disturbance. Urban prairie dog colonies displayed greater phylogenetic variation among replicates than those in rural habitats. Differentially abundant analysis revealed that bacterial species pathogenic to humans and animals were highly abundant in urban areas which indicates that host health and fitness might be negatively affected. Random forest models identified Alistipes shahii as the important species driving the changes in fecal microbiome composition. Despite the effects of habitat and geographic location of host, we found a strong correlation with environmental factors and that- average maximum temperature was the best predictor of prairie dog fecal microbial diversity. Conclusions: Our findings suggest that reduction in alpha diversity in conjunction with greater dispersion in beta diversity could be indicative of declining host health in urban areas; this information may, in turn, help determine future conservation efforts. Moreover, several bacterial species pathogenic to humans and other animals were enriched in prairie dog colonies near urban areas, which may in turn adversely affect host phenotype and fitness.