Pheromones are strong chemical cues that are sometimes thought to induce automatic behavioral responses, particularly in so-called ‘simple animals’ like fruit flies. Male flies fight with each other for the right to feed and mate on food patches, but when a female drops in, a male will court rather than act aggressively toward her. It was thought that a male determines the sex of an intruder to his food patch by sampling the strange fly's pheromones. Based on this, María de la Paz Fernández, Yick-Bun Chan and their colleagues predicted that a female fly expressing male pheromones would be quickly attacked by a resource-guarding male.
The authors tested their hypothesis by genetically engineering female flies to have a partial male pheromonal profile, though notably not including a male chemical called cVA that was recently described as an aggression-promoting pheromone. Fernández and Chan paired these masculinized females with wild-type males in small arenas with a dollop of food. The males displayed aggression toward these male-smelling females, which never happened toward wild-type females. However, males mated quite readily with the transformed females despite their smell. This made the authors curious whether females would be attacked or courted if they smelled feminine but behaved like males.
They engineered females by masculinizing their nervous systems but not their pheromones, paired them with wild-type males, and watched to see if the flies fought. They did, and they fought even more than males with females that smelled male. However, the males rarely initiated these fights. Rather, it was the females with masculinized brains who typically lunged aggressively toward the males, and because the males responded in kind, they rarely mated successfully.
Next, the authors wondered whether the combination of pheromones and behavior was enough to effectively change regular male–female interactions into complete male–male aggression, or vice versa. Fernández and Chan combined their earlier experiments by constructing females that had both masculinized nervous systems and the partially masculinized pheromones that they had used before. These females fought with wild-type males just as much as wild-type males did, but again, the fights were more commonly initiated by the females rather than the males, and a low level of successful mating persisted in these matchups.
Finally, Fernández and Chan repeated the experiments with male flies. Feminizing either a male's nervous system or the pheromones resulted in only very slightly decreased aggression between a wild-type and a transformed male. However, altering both pheromones and behavior reduced aggression dramatically, though some fighting persisted. Wild-type males rarely attempted to mate with males who had feminized behaviors, but the combination of pheromones and behavior greatly enhanced mating attempts, approaching the levels of typical male–female interactions.
These results from Fernández, Chan and colleagues suggest that although most of the differences between normal male–female and male–male encounters can be reversed by endowing females with a particular set of male pheromones and male-like aggressive behavior, some parts of the story are still left out. It is possible that one of the missing pieces is the aggression-promoting chemical cVA, which is produced by a different mechanism from the one transformed in this study. However, one message is clear: flies pay attention to more than just pheromones when determining whether to fight or court a stranger.