Regulation of Behavioral Plasticity: Mechanism Underlying Olfaction-Dependent Changes in Male Specific Courtship Behaviors in Drosophila melanogaster

Animal behaviors consists of both innate and plastic components. Hardwired neural circuits are established during development and confer animals the innate potential to solve the survival challenges. However, in an ever-changing environment, animals need to modify their behaviors constantly and accurately to increase their fitness. Sensory experience modulates animal behaviors via changes in gene expression and circuits neurophysiology. Olfaction, one of the most ancient modalities, regulates feeding and social behaviors such as courtship. It is intriguing how olfactory experience modifies animal behaviors. To study this question, we use the olfaction-driven male courtship in the fruit fly Drosophila melanogaster, which consists of stereotypical and quantifiable rituals wired by a well-defined, sexually dimorphic circuits. We found that social experience, conveyed by olfactory detection of fly body pheromone, converges with internal hormone signaling, exerts chromatin-based regulation on the important behavioral regulator, fruitlessM. fruM is a transcription factor that regulates male-specific behaviors in flies, and it is both necessary and sufficient for male courtship behaviors. We found that juvenile hormone signaling via its receptors Methoprene-tolerant (Met) and Germ-cell expressed (Gce), works coincidentally with calcium signaling and the histone acetyl transferase p300 downstream of Or47b pheromone signaling, to exert transcriptional regulation on fruM, and subsequently modifies neurophysiology and behaviors. As result, group-reared males gain courtship advantage in Or47b- and fruM- dependent manner. Next, we investigated if Or47b is involved in other aspects of behavioral plasticity. fruM mutant males do not court other flies when held isolation, but they acquire courtship learning with grouping experience in olfaction-dependent manner. We found that Or47b is involved in male-female courtship learning and male-male chaining learning in fruM mutant males. Our work elucidated the roles of Or47b in regulating courtship behavioral plasticity in males reared in different social environments. Pheromone signaling via Or47b enhances courtship success in group-reared males with or without the innate fruM -dependent programs. Our findings validated olfaction-driven male courtship behavior as a good model in studying sensory experience dependent behavioral plasticity, and lays ground for future studies on pheromone-driven modifications on genes and circuits driving male courtship.