UC San Diego

Animals modify their behaviors in response to changes in their external social environment and internal physiological state to maximize their chances of survival and reproduction. This behavioral flexibility allows animals to have different responses to the same sensory stimulus depending on the needs of the animals and their environment. To understand how such flexibility arises in the nervous system, we studied how social environment can modulate mating behavior in the vinegar fly, Drosophila melanogaster. We found that when mature male flies are raised in an environment of high population density, they enhance their courtship display towards females. A similar enhancement is not observed in immature males, suggesting that there is an interaction between signals arising from the internal state (reproductive maturity) and the external environment (population density) of the fly. We identified the neural substrate of this behavioral modulation as plasticity in a single type of aphrodisiac pheromone sensing neuron that enhances its pheromone sensitivity only in mature males raised in dense housing conditions. Neuronal sensitization is induced by a synergistic interaction between juvenile hormone, a signal for reproductive maturity, and activity-dependent signaling pathways. Further, the adaptive responses of pheromone sensing neurons are sexually dimorphic in nature - they are observed in males but not in females. Sex differences in neuronal plasticity are regulated by FruitlessM, a male-specific transcription factor that regulates pheromone sensitivity in these neurons. Our findings indicate that FruitlessM likely functions as a genomic coincidence detector—integrating internal reproductive maturity and external population density—to modulate mating behavior in a sexually dimorphic manner.

Mechanistic studies into cellular and molecular basis of behavioral flexibility are largely possible due to the availability of genetic tools that allow precise manipulations of neural circuits. In a parallel effort, we expanded the fly toolkit by developing a new method to alter gene expression in a spatially and temporally controlled manner, and demonstrated its utility in mapping and manipulating neuronal circuits underlying odor preference behavior. We anticipate that the development of these tools will further advance our understanding of how internal state and environmental context modulate behaviors in an integrated fashion.