Juvenile hormone as a key regulator for asymmetric caste differentiation in ants

Caste differentiation involves many functional traits that diverge during larval growth and metamorphosis to produce adults irreversibly adapted to reproductive division of labor. Investigating developmental differentiation is important for general biological understanding and has increasingly been explored for social phenotypes that diverge in parallel from similar genotypes. Here, we use Monomorium pharaonis ants to investigate the extent to which canalized worker development can be shifted toward gyne (virgin-queen) phenotypes by juvenile hormone (JH) treatment. We show that excess JH can activate gyne-biased development in workers so that wing-buds, ocelli, antennal and genital imaginal discs, flight muscles, and gyne-like fat bodies and brains emerge after pupation. However, ovary development remained unresponsive to JH treatment, indicating that JH-sensitive germline sequestration happens well before somatic differentiation. Our findings reveal important qualitative restrictions in the extent to which JH treatment can redirect larval development and that these constraints are independent of body size. Our findings corroborate that JH is a key hormone for inducing caste differentiation but show that this process can be asymmetric for higher colony-level germline versus somatic caste differentiation in superorganisms as defined a century ago by Wheeler. We quantified gene expression changes in response to JH treatment throughout development and identified a set of JH-sensitive genes responsible for the emergence of gyne-like somatic traits. Our study suggests that the gonadotropic role of JH in ovary maturation has shifted from the individual level in solitary insects to the colony level in an evolutionary-derived and highly polygynous superorganism like the pharaoh ant.