A neuronal mechanism controlling the choice between feeding and sexual behaviors in Drosophila

Animals must express the appropriate behavior that meets their most pressing physiological needs and their environmental context. However, it is currently unclear how alternative behavioral options are evaluated and appropriate actions are prioritized. Here, we describe how fruit flies choose between feeding and courtship; two behaviors necessary for survival and reproduction. We show that sex- and food-deprived male flies prioritize feeding over courtship initiation, and manipulation of food quality or the animal’s internal state fine-tunes this decision. We identify the tyramine signaling pathway as an essential mediator of this decision. Tyramine biosynthesis is regulated by the fly’s nutritional state and acts as a satiety signal, favoring courtship over feeding. Tyramine inhibits a subset of feeding-promoting tyramine receptor (TyrR)-expressing neurons and activates P1 neurons, a known command center for courtship. Conversely, the perception of a nutritious food source activates TyrR neurons and inhibits P1 neurons. Therefore, TyrR and P1 neurons are oppositely modulated by starvation, via tyramine levels, and food availability. We propose that antagonistic co-regulation of neurons controlling alternative actions is key to prioritizing competing drives in a context- dependent manner. [Display omitted] •Drosophila males deprived of both food and sex have competing needs•Choosing between feeding or mating is modulated by food quality and internal drive•Tyramine signaling mediates the choice between feeding and courtship•Antagonism between feeding and courtship neurons determines the behavior selected How are alternative options evaluated in the brain and specific actions prioritized? Cheriyamkunnel et al. describe a novel neural mechanism by which fruit flies balance and prioritize the competing needs of feeding and mating by integrating nutrient availability and motivational drives.