Sex differentiation and hormones are essential for the development of sexual signals in animals, and the regulation of sexual signals involves complex gene networks. However, it is unknown whether a core gene is able to connect the upstream regulators for controlling sexual signal outputs and behavioural consequences. Here, we identify a single gene that integrates both sex differentiation and hormone signalling with sexual attractiveness in an insect model. CYP4PC1 in the German cockroach, Blattella germanica, controls the rate-limiting step in producing female-specific contact sex pheromone (CSP) that stimulates male courtship. As revealed by behavioural, biochemical, molecular, genetic and bioinformatic approaches, in sexually mature females, CYP4PC1 expression and CSP production are coordinately induced by sex differentiation genes and juvenile hormone (JH) signalling. In adult males, direct inhibition of CYP4PC1 expression by doublesex^M binding in gene promoter and lack of the gonadotropic hormone JH prevent CSP production, thus avoiding male–male attraction. By manipulating the upstream regulators, we show that wild-type males prefer to court cockroaches with higher CYP4PC1 expression and CSP production in a dose-dependent manner, regardless of their sex. These findings shed light on how sex-specific and high sexual attractiveness is conferred in insects.

性别分化和激素对于动物性信号的发展至关重要，而性信号的调节涉及复杂的基因网络。然而，尚不清楚核心基因是否能够连接上游调节器以控制性信号输出和行为后果。在这里，我们在昆虫模型中鉴定出一个将性别分化和激素信号与性吸引力相结合的单一基因。德国小蠊（德国小蠊）中的CYP4PC1控制产生刺激雄性求爱的雌性特异性接触性信息素 (CSP) 的限速步骤。正如行为、生化、分子、遗传和生物信息学方法所揭示的，在性成熟的女性中，CYP4PC1表达和 CSP 产生是由性别分化基因和保幼激素 (JH) 信号协调诱导的。^{在成年男性中，通过基因启动子中的双性M}结合直接抑制CYP4PC1的表达以及缺乏促性腺激素 JH 会阻止 CSP 的产生，从而避免男性-男性的吸引力。通过操纵上游调节器，我们表明野生型雄性更喜欢以剂量依赖性方式吸引具有较高CYP4PC1表达和 CSP 产生的蟑螂，无论其性别如何。这些发现揭示了昆虫是如何赋予性别特异性和高性吸引力的。