Modular Sensory and Morphological Adaptations Underlying Fresh-Fruit Exploitation in Drosophilid Flies

(1) Background: Drosophilid flies oviposit in damaged or fermenting substrates, whereas D. suzukii prefers to lay eggs in ripening fruits. This ecological shift requires females to recognize fruit-stage cues while overcoming the mechanical barrier imposed by fresh-fruit surfaces. Whether fresh-fruit exploitation requires a complete specialist syndrome or can arise through partial combinations of sensory and morphological traits remains unclear. (2) Methods: We combined field surveys with behavioral, chemical, biomechanical and morphological analyses across multiple drosophilid species to investigate potential mechanisms underlying the diversification of fresh-fruit exploitation. (3) Results: Field surveys indicated that the phylogenetically distant species D. immigrans exploits fruit-associated breeding substrates that overlap with those used by D. suzukii in natural habitats. Females of D. suzukii preferred ripe strawberry cues and avoided fermentation-associated substrates, whereas D. immigrans showed an intermediate behavioral profile. Volatile profiling revealed that fruit decay drives chemical similarity across fruits, with rotten substrates enriched in ethyl acetate and acetic acid. Firmness measurements confirmed that decay reduces the mechanical resistance of fruit substrates, while morphological comparisons revealed divergent ovipositor architectures. (4) Conclusions: Our findings are consistent with a modular framework for fresh-fruit exploitation, in which specialist and facultative strategies reflect different combinations of fermentation-cue avoidance, substrate access, and ovipositor morphology.