Scaling of ovipositor size in two species of Drosophila: altered genital coupling mechanisms and evolution of allometric slopes.

Abstract

Animal genitalia typically exhibit limited size variation relative to overall body size, a pattern known as negative allometry. The 'one-size-fits-all' hypothesis suggests that genital compatibility between sexes constrains the evolution of extreme genital sizes, yet direct evidence remains scarce. Drosophila suzukii presents a unique opportunity to test this hypothesis from the female perspective. This species has evolved an enlarged, sclerotized ovipositor capable of piercing intact fruit skins. However, this innovation necessitated an altered genital coupling mechanism, as the modified ovipositor-also functioning as part of the female genitalia-posed a mechanical obstacle to copulation. In contrast, D. subpulchrella, the closest relative of D. suzukii, retains the ancestral coupling mechanism, which depends on genital size compatibility between sexes. Allometric analyses revealed that D. subpulchrella ovipositors exhibit shallower scaling slopes than other body parts, consistent with the negative allometry rule. Conversely, D. suzukii ovipositors display significantly steeper slopes, suggesting that the new coupling mechanism has relaxed the constraint on genital size. These findings provide novel support for the one-size-fits-all hypothesis, offering unprecedented resolution into the role of coupling mechanisms in shaping genital allometry.