Receptor sequence divergence, gain, loss, duplication, and neofunctionalization drive olfactory adaptation in <i>Drosophila suzukii</i>

Shifts in ecological niches are often driven by evolutionary changes in the olfactory system, yet the underlying mechanisms remain poorly understood. To investigate this, we used Drosophila suzukii , an invasive fruit pest, as a model. Unlike most Drosophila species, which prefer overripe fruit, D. suzukii strongly prefers laying eggs in ripe fruit. We found that this shift is accompanied by pronounced changes in the odorant tuning of only a few olfactory receptor neurons (ORNs) compared to Drosophila melanogaster . Some changes are shared with its relative Drosophila biarmipes , whereas others are unique to D. suzukii . These shifts resulted not only from receptor sequence divergence but also from additional mechanisms. In one ORN, a second odorant receptor ( Or ), distinct from the ancestral Or , mediates detection of a leaf-derived odorant, while a single amino acid substitution—likely acting with additional changes—in the ancestral Or fine-tunes sensitivity to fruit-ripening esters. In two additional ORNs, four gene duplicates derived from an ancestral Or mediate tuning shifts: Two duplicates maintain responses similar to the original ORN, while two tandem duplicates confer responses in a preexisting ORN that has lost its ancestral Or . This neofunctionalization is unique to D. suzukii . Finally, we show that two of the receptors underlying these innovations are required for attraction to ripe fruit but are dispensable for egg-laying preference. Our findings reveal how receptor sequence divergence, coexpression, loss, duplication, and neofunctionalization drive sensory adaptation and ecological specialization and provide a foundation for identifying additional attractants and repellents to control D. suzukii .