Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USA.
Division of Chemistry and Chemical Engineering, California Institute of Technology, Pasadena, CA 91125, USA.
Cell. 2024 Jul 11;187(14):3563-3584.e26. doi: 10.1016/j.cell.2024.05.012. Epub 2024 Jun 17.
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促进宏观进化变化是理解生物多样化的核心。超过 66000 种的隐翅虫物种（步甲科）形成了最大的后生动物家族。我们结合了跨越最大进化枝 Aleocharinae 的基因组和细胞类型转录组学的见解，追溯了两种组成防御腺的细胞类型的进化——防御腺可能是隐翅虫多样性的催化剂。我们确定了导致一种细胞类型通过与植物毒素释放系统趋同的机制产生苯醌的分子进化步骤，以及第二种细胞类型合成一种使总分泌物具有杀伤力的溶剂。这种合作系统自白垩纪早期 Aleocharinae 辐射到数万条谱系以来就一直保持不变。重新编程每个细胞类型产生了生化创新，使生态专业化成为可能——最显著的是通过通过宿主操纵分泌物渗透到社会性昆虫群体中的共生体。我们的发现揭示了甲虫化学创新起源和可进化性的细胞类型进化过程。
