Labor division of worker ants can be controlled by insulin synthesis targeted through miR-279c-5p in Solenopsis invicta (Hymenoptera: Formicidae).

Background: In social insects, the labor division of workers is ubiquitous and controlled by genetic and environmental factors. However, how they modulate this coordinately remains poorly understood.

Results: We report miR-279c-5p participation in insulin synthesis and behavioral transition by negatively regulating Rab8A in Solenopsis invicta. Eusocial specific miR-279c-5p is age-associated and highly expressed in nurse workers, and localized in the cytoplasm of neurons, where it is partly co-localized with its target, Rab8A. We determined that miR-279c-5p agomir suppressed Rab8A expression in forager workers, consequently decreasing insulin content, resulting in the behavioral shift to 'nurse-like' behaviors, while the decrease in miR-279c-5p increased Rab8A expression and increased insulin content in nurse workers, leading to the behavioral shift to 'foraging-like' behaviors. Moreover, insulin could rescue the 'foraging behavior' induced by feeding miR-279c-5p to nurse workers. The overexpression and suppression of miR-279c-5p in vivo caused an obvious behavioral transition between foragers and nurses, and insulin synthesis was affected by miR-279c-5p by regulating the direct target Rab8A.

Conclusion: We first report that miR-279c-5p is a novel regulator that promotes labor division by negatively regulating the target gene Rab8A by controlling insulin production in ants. This miRNA-mediated mechanism is significant for understanding the behavioral plasticity of social insects between complex factors and potentially provides new targets for controlling red imported fire ants. © 2023 Society of Chemical Industry.