Increased sugar valuation contributes to the evolutionary shift in egg-laying behavior of the fruit pest Drosophila suzukii

• Published in: PLoS biology 2023-12, Vol.21 (12), p.e3002432-e3002432
• Main Authors: Cavey, Matthieu, Charroux, Bernard, Travaillard, Solène, Manière, Gérard, Berthelot-Grosjean, Martine, Quitard, Sabine, Minervino, Caroline, Detailleur, Brice, Grosjean, Yaël, Prud'homme, Benjamin
• Format: Article
• Language: English
• Subjects: Acids; Analysis; Behavior; Behavior evolution; Biology and Life Sciences; Brain; Calcium imaging; Carbohydrates; Central nervous system; Chemoreception; Drosophila; Drosophila suzukii; Ecological niches; Egg laying; Eggs; Evolution; Fermentation; Fermented food; Fruit crops; Fruit flies; Fruits; Glucose; Identification and classification; Insects; Life Sciences; Neuroimaging; Niches; Oviposition; Pests; Physical Sciences; Physiology; Preferences; Research and Analysis Methods; Short Reports; Substrates; Sugar; Sweet taste; Taste receptors; Taste stimuli; Valuation
• ISSN: 1545-7885; 1544-9173; 1545-7885
• DOI: 10.1371/journal.pbio.3002432

Behavior evolution can promote the emergence of agricultural pests by changing their ecological niche. For example, the insect pest Drosophila suzukii has shifted its oviposition (egg-laying) niche from fermented fruits to ripe, nonfermented fruits, causing significant damage to a wide range of fruit crops worldwide. We investigate the chemosensory changes underlying this evolutionary shift and ask whether fruit sugars, which are depleted during fermentation, are important gustatory cues that direct D. suzukii oviposition to sweet, ripe fruits. We show that D. suzukii has expanded its range of oviposition responses to lower sugar concentrations than the model D. melanogaster, which prefers to lay eggs on fermented fruit. The increased response of D. suzukii to sugar correlates with an increase in the value of sugar relative to a fermented strawberry substrate in oviposition decisions. In addition, we show by genetic manipulation of sugar-gustatory receptor neurons (GRNs) that sugar perception is required for D. suzukii to prefer a ripe substrate over a fermented substrate, but not for D. melanogaster to prefer the fermented substrate. Thus, sugar is a major determinant of D. suzukii's choice of complex substrates. Calcium imaging experiments in the brain's primary gustatory center (suboesophageal zone) show that D. suzukii GRNs are not more sensitive to sugar than their D. melanogaster counterparts, suggesting that increased sugar valuation is encoded in downstream circuits of the central nervous system (CNS). Taken together, our data suggest that evolutionary changes in central brain sugar valuation computations are involved in driving D. suzukii's oviposition preference for sweet, ripe fruit.