Brain remodeling during queen maturation by a gene-regulation network that was co-opted by ants with reproductive workers

Caste differentiation in ants is decided early in development to produce gynes as future colony germ-lines and workers as present colony soma. However, gynes need to be inseminated to become functional queens, a transition triggered by stored sperm that initiates reproductive role differentiation relative to gynes that remain unmated. Here we analyze the anatomy and transcriptomes of brains during this differentiation process within the reproductive caste of Monomorium pharaonis. Insemination terminated brain growth whereas unmated control gynes continued to increase their brain volume. Transcriptomes revealed that a specific gene regulatory network (GRN) mediates both brain anatomy changes and concomitant behavioral modifications. This reproductive role differentiation GRN hardly overlapped with the gyne-worker caste differentiation GRN, but it appears to have been coopted by distantly related ants where workers became germ-line individuals after the queen caste was secondarily lost, entirely or partially. The genes corazonin and neuroparsin-A in the anterior neurosecretory cells were overexpressed in individuals with less or non-reproductive roles across all four ant species investigated.