Host dietary specialization and neutral assembly shape gut bacterial communities of wild dragonflies

Abstract

Host-associated gut microbiota can have significant impacts on host ecology and evolution and are often host-specific. Multiple factors can contribute to such host-specificity: (1) host dietary specialization passively determining microbial colonization, (2) hosts selecting for specific diet-acquired microbiota, or (3) a combination of both. The latter possibilities indicate a functional association and should produce stable microbiota. We tested these alternatives by analyzing the gut bacterial communities of six species of wild adult dragonfly populations collected across several geographic locations. The bacterial community composition was predominantly explained by sampling location, and only secondarily by host identity. To distinguish the role of host dietary specialization and host-imposed selection, we identified prey in the guts of three dragonfly species. Surprisingly, the dragonflies–considered to be generalist predators–consumed distinct prey; and the prey diversity was strongly correlated with the gut bacterial profile. Such host dietary specialization and spatial variation in bacterial communities suggested passive rather than selective underlying processes. Indeed, the abundance and distribution of 72% of bacterial taxa were consistent with neutral community assembly; and fluorescent in situ hybridization revealed that bacteria only rarely colonized the gut lining. Our results contradict the expectation that host-imposed selection shapes the gut microbiota of most insects, and highlight the importance of joint analyses of diet and gut microbiota of natural host populations.