How evolution at the cellular level potentiates macroevolutionary change is central to understanding biological diversification. The >66,000 rove beetle species (Staphylinidae) form the largest metazoan family. Combining genomic and cell type transcriptomic insights spanning the largest clade, Aleocharinae, we retrace evolution of two cell types comprising a defensive gland—a putative catalyst behind staphylinid megadiversity. We identify molecular evolutionary steps leading to benzoquinone production by one cell type via a mechanism convergent with plant toxin release systems, and synthesis by the second cell type of a solvent that weaponizes the total secretion. This cooperative system has been conserved since the Early Cretaceous as Aleocharinae radiated into tens of thousands of lineages. Reprogramming each cell type yielded biochemical novelties enabling ecological specialization—most dramatically in symbionts that infiltrate social insect colonies via host-manipulating secretions. Our findings uncover cell type evolutionary processes underlying the origin and evolvability of a beetle chemical innovation.

细胞水平的进化如何增强宏观进化变化是理解生物多样性的核心。超过 66,000 种罗夫甲虫（Staphylinidae）构成了最大的后生动物家族。结合跨越最大分支 Aleocharinae 的基因组和细胞类型转录组学见解，我们追溯了两种细胞类型的进化，其中包括防御腺——葡萄球菌巨型多样性背后的假定催化剂。我们确定了分子进化步骤，导致一种细胞类型通过与植物毒素释放系统融合的机制产生苯醌，并由第二种细胞类型合成一种武器化总分泌的溶剂。这种合作系统自白垩纪早期以来一直得到保存，因为Aleocharinae辐射到数以万计的谱系。对每种细胞类型进行重新编程产生了生化新颖性，从而实现了生态专业化——最显着的是通过宿主操纵分泌物渗透到社会性昆虫群体的共生体。我们的研究结果揭示了甲虫化学创新的起源和进化性背后的细胞类型进化过程。