To increase reproductive fitness, animals modify behaviors as a function of their internal and environmental states. The molecular mechanisms driving these changes remain unknown.
In Drosophila transcription factor FruM is required for male courtship behaviors and is expressed in their underlying neural circuits (1, 2).
Previous studies showed that pheromone-sensing Or47b receptor regulates fruM expression in Or47b neurons, and Or47b neurons increase male courtship advantage with age (3).
Here we show that social experience and age collaborate to reprogram fruM expression via chromatin-based modulation in Or47b neurons. Both age and social experience increase enrichment of RNA polymerase II, histone acetyl transferase p300, and active chromatin marks around fruM P1 promoter, increasing fruM expression in Or47b neurons. Social isolation decreases these effects, which are rescued by pheromone exposure or regrouping. The effect of age on FruM expression is mediated by juvenile hormone (JH) signaling, an age-related regulator of Or47b odor responses and courtship competition. JH receptors associate with fruM P1 promoter and loss of JH signaling decreases fruM expression and open chromatin marks around fruM P1 promoter. Changes in fruM expression ultimately changes the expression of target ion channel genes known to regulate neurophysiology. Our results suggest coincident hormone and pheromone signals converge to modulate fruM expression using chromatin-based mechanisms.