An ant colony is a higher-level organism consisting of specialized germline (queens & males) and soma (workers) individuals that differentiate early in development. A full understanding of the molecular mechanisms on the queen-worker division requests investigation on both organismal and superorganismal levels. At organismal level, the brain cell repertoire variations among the colony individuals provide cellular basis for the division of social functions. We develop Monomorium pharaonis ant species as a model to investigate the evolution and development of caste differentiation rocess. Comparison of brain single-cell transcriptome data of queens, gynes (uninseminated queens), workers and males from same colony detected a high degree of specialization in the brain cellular composition of all four adult phenotypes, particularly in males and workers. At superorganismal level, we investigate the gene regulatory networks that mediate individual caste developmental fates by integrating Wheeler’s concept and Waddington’s epigenetic landscape. By constructing transcriptional trajectories for > 1400 individuals covering most developmental stages of two ant species, we found that caste differentiation is increasingly canalized from early development onwards, particularly in germline individuals (gynes/queens). The canalized genes with gyne/queen-biased expression were enriched for ovary and wing functions while canalized genes with worker-biased expression were enriched in brain and behavioural functions. This canalization process differentiated caste development can be disturbed by manipulating canalized genes inducing non-adaptive intermediate phenotypes between gynes and workers. Our series of studies suggest a strong selection in maintaining the canalization process that regulating the caste differentiation in social insects.
Evolutionary and developmental mechanisms of ant social caste system