Social interactions and its deprivation strongly influence animal physiology and behavior. One of the most striking cases of social modulation of behavior is found in the courtship propensity of the male Drosophila melanogaster. Upon isolation, wild-type males exhibit higher courtship activity than those kept with other males when subsequently tested in mating assays, where a test male is paired with a target female. In contrast, fruitless (fru) mutant males engage in vigorous male-to-male courtship when housed together in a group, which is suppressed by keeping them singly for several days before mating assays.
To investigate the molecular and cellular underpinnings of this gene-environment interplay, we are focusing on brain P1 neurons, a central neural cluster initiating courtship: artificial activation of P1 neurons effectively elicits male courtship even in the absence of a courtship target. In vivo whole-cell patch clamp recordings from P1 neurons revealed that their electrical properties are differentially modulated by male-male social interactions, depending on whether a male fly carries the fru mutation.
At the molecular level, we developed an optimized version of the Translating Ribosome Affinity Purification (TRAP), i.e. super sensitive TRAP (STRAP). STRAP allowed us to identify a subset of social experience-responsive genes, which are differentially translated in a select population of brain cells, including P1 neurons, depending on social conditions. We found that group housing downregulates the expression of one of the K+ channel genes in fru mutants but not in wild-type males; this implies that P1 neurons would more likely elicit courtship in the fru mutant but less likely in the wild-type males when they are group housed.
Our approach will thus provide a novel animal model to investigate the neurons, circuits, and molecules underlying behavior, allowing us to uncover the mechanistic bases of gene-environmental interplay. We anticipate that the discoveries made using fruit flies will contribute to understanding the fundamental principles across all animals, including humans.