Environment and diet shape the geography-specific Drosophila melanogaster microbiota composition

Geographic and environmental variation in the animal microbiota can be directly linked to the evolution and wild fitness of their hosts but often appears to be disordered. Here, we sought to better understand patterns that underlie wild variation in the microbiota composition of Drosophila melanogaster . First, environmental temperature predicted geographic variation in fly microbial communities better than latitude did. The microbiota also differed between wild flies and their diets, supporting previous conclusions that the fly microbiota is not merely a reflection of diet. Flies feeding on different diets varied significantly in their microbiota composition, and flies sampled from individual apples were exceptionally depauperate for the Lactic Acid Bacteria (LAB), a major bacterial group in wild and laboratory flies. However, flies bore significantly more LAB when sampled from other fruits or compost piles. Follow-up analyses revealed that LAB abundance in the flies uniquely responds to fruit decomposition, whereas other microbiota members better indicate temporal seasonal progression. Finally, we show that diet-dependent variation in the fly microbiota is associated with phenotypic differentiation of fly lines collected in a single orchard. These last findings link covariation between the flies’ dietary history, microbiota composition, and genetic variation across relatively small (single-orchard) landscapes, reinforcing the critical role that environment-dependent variation in microbiota composition can play in local adaptation and genomic differentiation of a model animal host.