Molecular evolution of CO2-sensing ab1C neurons underlies divergent sensory responses in the Drosophila suzukii species group

Abstract

Organisms evolve behavioral and morphological traits to adapt to their ecological niches, yet the genetic basis of adaptation remains largely unknown. Drosophila suzukii has evolved a distinctive oviposition preference for ripe fruit, unlike most Drosophila species such as D. melanogaster, which prefer overripe fruit. Carbon dioxide (CO2), a metabolic volatile that increases as fruit ripens and decays, may act as a critical ecological cue shaping these preferences. Here, we focus on D. suzukii and its sister species D. subpulchrella, which shows an intermediate preference, to investigate the genetic basis of CO2 responses. We report a previously unrecognized shift in CO2-guided oviposition: D. suzukii and D. subpulchrella readily lay eggs on CO2-enriched substrates, unlike the strong aversion displayed by D. melanogaster. Electrophysiological recordings revealed a species-specific sensory tuning, characterized by an early spike in CO2-evoked neuronal firing in D. suzukii and D. subpulchrella—a temporal response feature absent in D. melanogaster. To dissect the genetic basis of this shift, we generated transgenic D. melanogaster expressing either the D. suzukii Gr63a coding sequence or the D. subpulchrella Gr63a cis-regulatory element. Remarkably, both manipulations reproduced the early-onset firing pattern of CO2 sensitivity, demonstrating that either receptor function or expression can independently drive this sensitivity adaptation. Our findings reveal that evolution can shape ecological adaptation through distinct genetic mechanisms, leading to convergent physiological traits among closely related species.