Ovipositor morphology and mechanosensory divergence drive niche breadth expansion in Drosophila

For most Drosophila species, the firm surface of intact ripe fruit acts as a physical barrier to oviposition, effectively restricting them to the saprophagous niche. How species overcome such mechanical constraints at the behavioral and sensory levels, and whether doing so leads to niche breadth expansion or niche specialization, remain poorly understood. Here we show across ten Drosophila species that substrate physical hardness is a critical barrier preventing most species from exploiting ripe fruit. Unlike saprophagous species, the pest D. suzukii and the widely distributed D. immigrans have evolved a tolerance for high substrate stiffness to perform puncture oviposition. This behavioral shift is enabled by distinct morphology of saw-like and needle-like ovipositors respectively, which are critical for breaching intact fruit. To uncover the neural basis for this mechanical adaptation, we screened mechanosensory mutants in D. melanogaster and identified the Inactive ( IAV ) channel as a key sensory gene mediating this behavior. Functional rescue experiments reveal that IAV has diverged in D. suzukii and D. immigrans , mediating a sensory relaxation that permits oviposition on stiff substrates. This mechanical breach confers a direct fitness advantage, allowing only the offspring of these two species to successfully complete larval development in fresh fruit. Finally, field surveys in the wild demonstrate that this modular adaptation facilitates niche overlap and resource partitioning in natural habitats. Overall, this work reveals how the divergence of mechanosensory channels and morphological innovations can overcome physical constraints to drive broad ecological niche expansion.