Social task and aggressiveness shape immunity gene expression levels in the head of highly eusocial bees

Living in crowded perennial nests, social insects encounter high risks of disease outbreaks and predation on colony resources. The innate immune system plays an important barrier against microbial pathogens, but its association with group defensive behaviours remains unexplored. Here we investigated the expression of innate immune system genes in the workers of three species of Brazilian stingless bees (Scaptotrigona postica, Frieseomelitta varia, and Melipona quadrifasciata), which differ in worker reproductive traits and colony defence strategies. First, we standardized a behavioural arena test to assess the species-specific individual aggressiveness level of the workers. Then, we quantified the transcript levels of four core genes of the Toll and Imd pathways in the heads and abdomens for the three main life cycle stages of the workers (nurse, guard and forager). For the heads we found a strong association between immunity gene expression and aggressiveness, with an upregulation in the heads of guards and foragers in comparison to their abdomen tissues of the aggressive species, S. postica. while the less aggressive species, especially M. quadrifasciata workers, did not show such strong upregulation. Our study establishes a potential molecular link between immunity pathways and complex social behaviours in the Brazilian stingless bees, which evolutionarily lost the sting apparatus for the defence of their colonies. BULLETED HIGHLIGHTSO_LIThe expression of immune system genes increases with social task/age in the abdomen and head of highly eusocial bees. C_LIO_LIThe expression of Toll and Imd pathway genes is upregulated in the heads of the more aggressive stingless bee species. C_LIO_LIIn the more docile stingless bee species, immune gene expression is higher in the abdomen than in the head. C_LIO_LIOur findings suggest a possible involvement of immunity pathway signalling in the regulation of key social behaviours. C_LI