Dipteran insects show a wide range of species-specific mating positions. Interspecific transitions from one position to another may reflect sexual or natural selection, or be pleiotropic consequences of other genetic changes. Like many cyclorrhaphan flies, Drosophila species mate with the male on the back of the female, positioned centrally. Mechanosensory sensilla on the male genitalia of three species of the melanogaster species sub-group of Drosophila have species-specific effects on mating position and on courtship success: ablation of a single pair of bristles on the genital claspers of D. melanogaster males halved homotypic mating success, and unilateral ablation produced a contralateral asymmetry in the male's mating posture. Ablation of mechanoreceptors on the male genital lateral plate affected mating posture less radically and had no effect on mating frequency. Surprisingly, ablation of sensilla on the claspers of D. simulans and D. sechellia males showed no effect on homotypic mating. A similar result was found for D. melanogaster x D. simulans hybrid males. The existence of major differences in the sensory bases of mating position and copulation success in closely related species shows how differing mating positions may have evolved and underlines the need for detailed functional studies in studying the evolution of insect genitalia: homologous structures may serve different functions in different species.