The Aquatic Microbial Environment Shapes the Tadpole Microbiome and Antipredator Behavior

Host-associated microbial communities impact the brain and behavior through the microbiota-gut-brain (MGB) axis. Most studies of the gut microbiota use mammals in biomedical contexts; much less is known regarding wildlife species. We used larval amphibians to study the impact of the aquatic microbial environment on the gut and skin microbiota, brain, and antipredator behavior. We raised Northern Leopard Frog (Lithobates pipiens) tadpoles in pond water that was autoclaved or not autoclaved (natural); other studies show that these treatments produce variation in the tadpole gut microbiota. Tadpoles were also raised in the presence of stressors: predation-derived chemical cues and corticosterone. Compared to tadpoles raised in natural pond water, tadpoles raised in autoclaved pond water had altered gut and skin microbial communities, body size, brain size, brain shape, and behavioral responses to alarm pheromones. There was no effect of microbial environment or stressors on differential gene expression of the whole brain. The gut microbiota, but not the skin microbiota, was a significant predictor of behavioral endpoints. We found surprisingly few impacts of stressors on the tadpoles, although stressor treatments interacted with pond water treatments to influence the composition of the gut microbiota. Our findings demonstrate that tadpole behavior is modulated by the aquatic microbial community experienced during development in ways that are likely to affect survival.