From fruitless to sex: On the generation and diversification of an innate behavior

Abstract

Male sexual behavior in Drosophila melanogaster, largely controlled by the fruitless (fru) gene encoding the male specific FruM protein, is among the best studied animal behaviors. Although substantial studies suggest that FruM specifies a neuronal circuitry governing all aspects of male sexual behaviors, recent findings show that FruM is not absolutely necessary for such behaviors. We propose that another regulatory gene doublesex encoding the male-specific DsxM protein builds a core neuronal circuitry that possesses the potential for courtship, which could be either induced through adult social experience or innately manifested during development by FruM expression in a broader neuronal circuitry. FruM expression levels and patterns determine the modes of courtship behavior from innate heterosexual, homosexual, bisexual, to learned courtship. We discuss how FruM expression is regulated by hormones and social experiences and tunes functional flexibility of the sex circuitry. We propose that regulatory genes hierarchically build the potential for innate and learned aspects of courtship behaviors, and expression changes of these regulatory genes among different individuals and species with different social experiences ultimately lead to behavioral diversification.