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

Abstract

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 <i>Drosophila suzukii</i>, an invasive fruit pest, as a model. Unlike most <i>Drosophila</i> species, which prefer overripe fruit, <i>D. suzukii</i> 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 <i>Drosophila melanogaster</i>. Some changes are shared with its relative <i>Drosophila biarmipes</i>, whereas others are unique to <i>D. suzukii</i>. These shifts resulted not only from receptor sequence divergence but also from additional mechanisms. In one ORN, a second odorant receptor (<i>Or</i>), distinct from the ancestral <i>Or</i>, 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 <i>Or</i> 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 <i>Or</i>. This neofunctionalization is unique to <i>D. suzukii</i>. 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 <i>D. suzukii</i>.