Sex-determining genes distinctly regulate courtship capability and target preference via sexually dimorphic neurons

Abstract

For successful mating, a male animal must execute effective courtship behaviors toward a receptive target sex, which is female. Whether the courtship execution capability and upregulation of courtship toward females are specified through separable sex-determining genetic pathways remains uncharacterized. Here, we found that one of the two <i>Drosophila</i> sex-determining genes, <i>doublesex</i> (<i>dsx</i>), specifies a male-specific neuronal component that serves as an execution mechanism for courtship behavior, whereas <i>fruitless</i> (<i>fru</i>) is required for enhancement of courtship behavior toward females. The <i>dsx</i>-dependent courtship execution mechanism includes a specific subclass within a neuronal cluster that co-express <i>dsx</i> and <i>fru</i>. This cluster contains at least another subclass that is specified cooperatively by both <i>dsx</i> and <i>fru</i>. Although these neuronal populations can also promote aggressive behavior toward male flies, this capacity requires <i>fru</i>-dependent mechanisms. Our results uncover how sex-determining genes specify execution capability and female-specific enhancement of courtship behavior through separable yet cooperative neurogenetic mechanisms.