Neuronal and genetic bases of egg-laying behavior evolution in Drosophila suzukii – EVOSUGAR

Behaviors are generated by neuronal circuits which collect sensory information, process and integrate it to make informed decisions, and implement these decisions at the motor output level. Despite extensive work, understanding this process at the molecular, cellular and circuit level remains challenging. Besides, how these mechanisms are modified over evolutionary time scales to generate novel behaviors is also poorly understood. My project aims at filling this gap by using a neuro-genetic approach to dissect and compare neuronal circuit function in two genetically tractable species of fruit flies. I use two species which have divergent egg-laying behaviors: most species including the model Drosophila melanogaster lay their eggs in rotten/decaying fruits, whereas the invasive pest Drosophila suzukii prefers to lay in ripe fruits still on the plant. This behavior has dramatic consequences on fruit cultures since the recent worldwide invasion of D. suzukii. Previous work has shown that flies use gustatory information to discriminate ripe from rotten fruits and among these cues, fruit sugars (abundant in ripe fruits and depleted from rotten fruits) seem to play a particularly important role. Indeed, D. suzukii is significantly more responsive to sugars than D. melanogaster in egg-laying behavioral assays, raising the hypothesis that a change in neuronal circuits connected to sugar perception underlies - at least in part - the behavioral divergence.
I propose three independent and complementary aims to test this hypothesis and identify the neuronal bases of behavior evolution with this paradigm. Using genetic tools, I will compare homologous neuronal circuits functionally across species to identify the critical neuronal/circuit differences underlying behavioral divergence between the two species. This will involve transgenic manipulations with genetic tools commonly used in Drosophila neurobiology in combination with behavioral assays, neuro-anatomical analyses, neuronal activity sensors (calcium imaging) and genetic screens. Specifically, I will (1) test if inter-species functional differences occur in peripheral gustatory neurons detecting sugars (i.e.: sensory neurons). (2) I will test if differences occur in a dopaminergic circuit (i.e.: central nervous system) previously implicated in egg-laying decisions in D. melanogaster. (3) I will use an unbiased genetic screen that exploits natural variation to identify genes modulating the neuronal circuits that control the egg-laying response to sugars. These genes will help identify additional elements of the circuitry and will represent candidate evolutionary targets potentially involved in the divergence of D. suzukii's behavior.
Together, these approaches will reconstitute multiple elements of the neuronal circuitry controlling egg-laying behavior and test whether evolution has occurred at several possible levels of the circuit. In addition, I will address the question of behavioral evolution at multiple levels of analysis - circuit, cellular, molecular and genetic. My project will intersect two disciplines, neurobiology and evolution, to address a fundamental but largely unexplored issue using genetic tools and an experimental system that allow a functional dissection of neuronal circuits at the single-cell resolution. My results will contribute to understanding nervous system function, in particular with respect to the mechanisms of sensory integration and decision-making. My results will also be potentially relevant to insect pest control, by identifying the mechanisms through which D. suzukii has acquired access to a new ecological niche via behavioral changes. This project will also open several research avenues to pursue with my independent research team in the future.