Ant colonies with permanent division of labour between castes and highly distinct roles of the sexes have been conceptualized to be superorganisms, but the cellular and molecular mechanisms that mediate caste/sex-specific behavioural specialization have remained obscure. Here we characterized the brain cell repertoire of queens, gynes (virgin queens), workers and males of Monomorium pharaonis by obtaining 206,367 single-nucleus transcriptomes. In contrast to Drosophila, the mushroom body Kenyon cells are abundant in ants and display a high diversity with most subtypes being enriched in worker brains, the evolutionarily derived caste. Male brains are as specialized as worker brains but with opposite trends in cell composition with higher abundances of all optic lobe neuronal subtypes, while the composition of gyne and queen brains remained generalized, reminiscent of solitary ancestors. Role differentiation from virgin gynes to inseminated queens induces abundance changes in roughly 35% of cell types, indicating active neurogenesis and/or programmed cell death during this transition. We also identified insemination-induced cell changes probably associated with the longevity and fecundity of the reproductive caste, including increases of ensheathing glia and a population of dopamine-regulated Dh31-expressing neurons. We conclude that permanent caste differentiation and extreme sex-differentiation induced major changes in the neural circuitry of ants.

具有种姓之间永久分工和性别角色高度不同的蚁群已被概念化为超有机体，但介导种姓/性别特异性行为专业化的细胞和分子机制仍然模糊不清。在这里，我们通过获得 206,367 个单核转录组来表征Monomorium pharaonis的皇后、女性（处女皇后）、工人和雄性的脑细胞库。与果蝇相比, 蘑菇体肯扬细胞在蚂蚁中含量丰富，并显示出高度的多样性，大多数亚型在工人大脑中富集，这是进化衍生的种姓。男性大脑与工人大脑一样专业，但细胞组成趋势相反，所有视叶神经元亚型的丰度更高，而女性和女王大脑的组成仍然普遍，让人想起孤独的祖先。从处女雌性到受精后的角色分化导致大约 35% 的细胞类型发生丰度变化，表明在此过渡期间活跃的神经发生和/或程序性细胞死亡。我们还确定了可能与生殖种姓的长寿和繁殖力相关的授精诱导的细胞变化，包括鞘状胶质细胞的增加和多巴胺调节的群体表达Dh31的神经元。我们得出结论，永久种姓分化和极端性别分化导致蚂蚁神经回路发生重大变化。