Olfactory Specialization in Drosophila suzukii Supports an Ecological Shift in Host Preference from Rotten to Fresh Fruit

It has been demonstrated that Drosophila suzukii is capable of attacking ripening fruit, making it a unique species within a fly family named for their attraction towards the fermentation products associated with rotten fruits, vinegar, and yeast. It also has been hypothesized that D. suzukii is more attracted to the volatiles associated with the earlier ripening stages of fruit development, and in turn, that D. suzukii is less attracted to fermented food resources, especially when compared with D. melanogaster. Here, we demonstrate that D. suzukii and its close relative D. biarmipes are in fact more sensitive to volatiles associated with the fruit-ripening process; however, in choice-assays, both spotted-wing species are more attracted to fermented fruit than to earlier stages of fruit development, which is similar to the behavioral preferences of D. melanogaster, and thus, fruit developmental stage alone does not explain the ecological niche observed for D. suzukii. In contrast, we show that both D. suzukii and D. biarmipes are more attracted to leaf odors than D. melanogaster in behavioral trials. For D. suzukii, this differential behavioral preference towards leaves appears to be linked to beta-cyclocitral, a volatile isoprenoid that we show is most likely a novel ligand for the "ab3A" neuron. In addition, this compound is not detected by either of the other two tested fly species.