Gamete compatibility is fundamental to sexual reproduction. Wolbachia are maternally inherited endosymbiontic bacteria that manipulate gamete compatibility in many arthropod species. In Drosophila, the fertilization of uninfected eggs by sperm from Wolbachia-infected males often results in early developmental arrest. This gamete incompatibility is called cytoplasmic incompatibility (CI). We have recently found that Wolbachia modulate testis development and that, most unexpectedly, this effect was associated with Wolbachia infection in females, not males. This therefore raised the possibility that females influenced testis development by communicating with males prior to adulthood. We have tested this unorthodox hypothesis and found female pupae send a signal to male pupae during metamorphosis. This communication involves the perception of female pheromones by male olfactory receptors. This communication appeared to determine gamete compatibility in males. Moreover, Wolbachia interfere with this female-to-male communication through changes in female pheromone production. Reciprocaly, male pupae communicatie with female pupae at metamorphosis to restrict the compatibility range of the female gametes. Wolbachia also perturb this communication by feminizing pheromone production in males. Thus, Wolbachia broaden the compatibility range of eggs, promoting thereby the reproductive success of Wolbachia-infected females. In sum, we have found that Wolbachia perturbs a novel pheromone communication between male and female pupae that controls gamete compatibility, suggesting a novel regulatory mode of CI in insects (see Pontier and Schweisguth, Current Biology, 2015). A major goal is to now define how pheromone perception in the brain results in gamete modification!
S. Pontier and F. Schweisguth (2015) A Wolbachia-sensitive communication between male and female pupae controls gamete compatibility in Drosophila. Current Biology, 25, 2339-45