Ovipositor morphology and mechanosensory innovation traits favor niche width expansion in Drosophila

Ecological niche breadth is key factor associated with adaptive radiation and speciation. For most Drosophila species, the firm surface of intact ripe fruit acts as a physical barrier to oviposition, effectively restricting them to the saprophagous resources. 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, using comparative behavioral assays across ten Drosophila species, we show that substrate physical hardness is a critical barrier preventing most species from exploiting ripe fruit. Among species capable of puncture oviposition, there are two distinct evolutionary strategies among Drosophila species. With its serrated ovipositor and strong preference for fresh fruit, D. suzukii represents a case of ripe-fruit specialization. In contrast, D. immigrans with the needle-like ovipositor, gains access to fresh fruit while retaining the ability to exploit decaying substrates, thereby expanding its resource niche. Thus, D. suzukii considered as the typical evolutionary niche specialization, while D. immigrans represents niche expansion. Furthermore, using the genetic toolkit of D. melanogaster, we further identify the Inactive (IAV) mechanosensory channel as important regulator of stiffness-dependent oviposition inhibition. Loss of iav reduced inhibition on firm substrates, while cross-species rescue experiments showed that IAV orthologs differed in their ability to restore this response in a common genetic background. Puncture oviposition was also associated with successful offspring development on firm fruit and with the use of firm-surfaced hosts under natural conditions. Together, these findings identified a novel niche expansion of D. immigrans among the saprophagous Drosophila.