Research

Social interactions—and their deprivation— profoundly influence animal physiology and behavior. One of the most striking examples of socially modulated behavior is found in the courtship propensity of male Drosophila melanogaster. When isolated, wild-type males exhibit higher courtship activity than those kept with other males when later tested in mating assays, in which a test male is paired with a target female. In contrast, fruitless (fru) mutant males engage in vigorous male-to-male courtship when group-housed, but this behavior is suppressed when they are kept singly for several days before mating assays.

To investigate the molecular and cellular bases of this gene-environment interplay, I focus on the brain's P1 neurons, a central neural cluster that initiates courtship behavior. Artificial activation of P1 neurons robustly induces male courtship even in the absence of a potential mate. In vivo whole-cell patch-clamp recordings from P1 neurons have 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, I developed an optimized version of the Translating Ribosome Affinity Purification (TRAP), termed super-sensitive TRAP (STRAP). STRAP enabled us to identify a subset of social experience-responsive genes that are differentially translated in select populations of brain cells—including P1 neurons—depending on social conditions. I found that group housing downregulates the expression of a particular K+ channel gene in fru mutants but not in wild-type males, suggesting that P1 neurons are more likely to trigger courtship in fru mutants, but less likely in wild-type males, under group-housed conditions.

Thus, our approach provides a novel animal model for investigating the neurons, circuits, and molecules underlying behavior, offering new insights into the mechanisms of gene-environmental interactions. We anticipate that the discoveries made using fruit flies will contribute to understanding fundamental biological principles shared across animal species, including humans.