Evolutionary divergence in sugar valuation shifts Drosophila suzukii oviposition choice towards ripe fruit

Abstract

Behavior evolution can promote the emergence of agricultural pests via ecological niche changes. The underlying neuronal mechanisms are poorly understood. We investigate the chemosensory changes underlying the evolutionary shift of oviposition substrate of the pest Drosophila suzukii from rotten to ripe fruits. Using a model substrate for fermented fruits and genetic manipulations, we show that an increase in valuation of fruit sugars during oviposition decisions drives D. suzukii to oviposit on ripe fruits as opposed to the model D. melanogaster which prefers rotten fruits. Inter-species comparative in vivo calcium imaging of sugar Gustatory Receptor Neurons suggests that increased sugar valuation in D. suzukii is related to neuronal sensitivity changes at multiple levels of the oviposition circuitry. Our results show that the tuning of sugar valuation has contributed to the evolution of oviposition preference on ripe fruit of D. suzukii.

Evolution of chemosensory tissues and cells across ecologically diverseDrosophilids

“…D. suzukii originated in Eastern Asia but has expanded rapidly worldwide in the last decade 58,59 . Unlike the other species, D. suzukii females oviposit in ripe soft-bodied fruits and, as a result, have become a global agricultural pest [60][61][62][63][64][65] . Both D. simulans and D. melanogaster are generalists that feed on a broad range of decaying fruits and have nearly worldwide distributions 66 .…”