Molecular evolution of CO 2 -sensing ab1C neurons underlies divergent sensory responses in the Drosophila suzukii species group
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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 (CO 2 ), 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 CO 2 responses. We report a previously unrecognized shift in CO 2 -guided oviposition: D. suzukii and D. subpulchrella readily lay eggs on CO 2 -enriched substrates, unlike the strong aversion displayed by D. melanogaster . Electrophysiological recordings revealed a species-specific sensory tuning, characterized by an early spike in CO 2 -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 CO 2 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.
Author Summary
Animals rely on their senses to locate food sources and identify suitable reproductive sites in their environment. Closely related species can evolve strikingly different preferences as they adapt to new environments. For example, the invasive fruit fly D. suzukii lays its eggs in ripe fruit, unlike most other fruit flies, such as D. melanogaster , which prefer decaying fruit. Because CO 2 levels increase as fruit ripens and ferments, changes in how flies detect CO₂ may have contributed to these ecological differences. We compared CO 2 responses between D. suzukii and its sister species D. subpulchrella , and found that both species respond to CO 2 differently from D. melanogaster : both in their oviposition preferences and neural CO 2 sensitivity. By introducing either the D. subpulchrella or D. suzukii CO 2 receptor gene coding sequences or regulatory regions into D. melanogaster , we found that this altered sensitivity can arise from changes either in the receptor’s protein-coding region or in the DNA elements that control its expression. Our results show that evolution can act through multiple genetic mechanisms to fine-tune sensory systems, revealing how subtle molecular changes can generate ecological diversity among closely related species.
