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. Author SummaryAnimals 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 CO2 levels increase as fruit ripens and ferments, changes in how flies detect CO2 may have contributed to these ecological differences. We compared CO2 responses between D. suzukii and its sister species D. subpulchrella, and found that both species respond to CO2 differently from D. melanogaster: both in their oviposition preferences and neural CO2 sensitivity. By introducing either the D. subpulchrella or D. suzukii CO2 receptor gene coding sequences or regulatory regions into D. melanogaster, we found that this altered sensitivity can arise from changes either in the receptors 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.