An Orco dependent pathway suppresses egg-laying attraction to ripe fruit volatile compounds in Drosophila melanogaster but not in D. suzukii.

Abstract

Background: Most Drosophila species lay their eggs on a wide range of overripe or rotting fruits. By contrast, D. suzukii has evolved a strong preference for undamaged ripe fruits, a shift that has made it one of the most important pests of small fruits worldwide. Growing evidence suggests that this host preference shift is linked to modifications in the fly's olfactory system. Unlike D. melanogaster, D. suzukii is attracted by ripe strawberry volatile compounds for oviposition.

Results: In this study, we investigated the mechanisms underlying this behavioral divergence. We identified two strawberry volatiles, hexanoic acid and methyl butyrate, that, together recapitulate the species-specific oviposition preferences. D. suzukii is attracted by this two-component blend, whereas in D. melanogaster attraction to this blend is suppressed by an OR-dependent mechanism. In vivo calcium imaging of the antennal lobes revealed that the perception of these compounds is largely conserved between species, with only subtle differences. This suggests that the divergence in the olfactory perception of this two-component blend arises downstream of sensory neuron activity, within higher levels of olfactory processing.

Conclusions: Taken together, our results suggest that D. melanogaster has evolved an as-yet unidentified mechanism for integrating olfactory signals that suppresses attraction to unsuitable oviposition substrates when multiple key volatile are detected simultaneously.