Neuronal function and dopamine signaling evolve at high temperature in Drosophila

Adaptation to local environments is a general principle in nature. In the light of the ongoing climatic change, the mechanisms for temperature adaptation are of particular interest(1-2). Many essential biological processes are temperature sensitive, and neuronal activity(3-7) is a particularly prominent one as it affects essential, fitness-related traits such as behavior and locomotion(8). Here, we investigate if temperature stress triggers adaptation of neuronal signaling. We used replicated laboratory evolution experiments with Drosophila simulans to explore the genetic and phenotypic consequences of adaptation to novel temperatures. A combination of next-generation sequencing, genetic and pharmacological manipulations enabled us to identify thermally adaptive traits that evolve at elevated temperature in controlled laboratory settings. We show an adaptive response in neuronal tissue, with lower expression of genes for dopamine synthesis, recycling and trans-synaptic signaling. This key neuronal adaptation resulted in enhanced locomotor activity in hot environments by modulating dopamine signaling with likely pleiotropic consequences. Our study provides the first direct and unambiguous evidence that environmental temperature drives adaptive changes in neuronal tissues. The discovery that dopamine function in the brain evolves in response to the environment has far-reaching impact on evolutionary biology, ecology and behavioral neuroscience.