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Sexual production in social insects marks the peak of colony development, yet the mechanisms regulating it remain unclear. We investigated the role of brood in colony development, worker reproduction and sexual production inBombus impatiens. While larvae are known to reduce worker egg laying and enhance the queen’s reproductive inhibition, these effects were previously tested only in small groups. We manipulated brood size in full-sized, young colonies by doubling or removing brood and monitored development. Colonies with doubled brood produced significantly more gynes, independent of the number of workers, while reduced-brood colonies exhibited a non-significant increase in male production that was driven by colony size. Worker ovary activation was lower in double-brood colonies, with no change in aggression. A follow-up experiment directly testing the effect of colony size showed that higher worker density led to higher ovary activation in workers but did not affect sexual production. These results suggest that brood strongly influences colony development and sexual production, possibly reflecting an extended phenotype of the queen, whereas worker ovary activation appears to be a more flexible process influenced by either brood presence or colony size. Understanding brood dynamics may be key to understanding the evolution of female castes in social insects. 

Abstract Worker reproduction in social insects is often regulated by the queen, but can be regulated by the brood and nestmates, who may use different mechanisms to induce the same outcomes in subordinates. Analysis of brain gene expression patterns in bumble bee workers (Bombus impatiens) in response to the presence of the queen, the brood, both or neither, identified 18 differentially expressed genes, 17 of them are regulated by the queen and none are regulated by the brood. Overall, brain gene expression differences in workers were driven by the queen’s presence, despite recent studies showing that brood reduces worker egg laying and provides context to the queen pheromones. The queen affected important regulators of reproduction and brood care across insects, such asneuroparsinandvitellogenin, and a comparison with similar datasets in the honey bee and the clonal raider ant revealed thatneuroparsinis differentially expressed in all species. These data emphasize the prominent role of the queen in regulating worker physiology and behavior. Genes that serve as key regulators of workers’ reproduction are likely to play an important role in the evolution of sociality.