Effects of beekeeper-applied pesticides on the reproductive health of honey bee (Apis mellifera) queen physiology, gene expression and behavior

A honey bee queen’s developmental fate is highly plastic, and her reproductive physiology is greatly affected by the queen-rearing environment. Several environmental and biotic factors affect the reproductive quality of queens. We explored whether exposure of wax to field-relevant combinations of pesticides during development affects honey bee queen physiology, gene expression and behavior. We reared queens in plastic cups coated with molten beeswax that was either pesticide-free or containing field-relevant concentrations of agro-chemicals and miticides. Mated queens were placed in observation hives to measure egg-laying rate and worker retinue size. We then used the contents of their mandibular glands to measure worker attractiveness in caged bioassays and analyzed their chemical components. We then performed transcriptomic analysis of the queens’ brain. We found that exposure of wax to these pesticides during development significantly lowered the adult queens’ egg-laying rate and worker retinue size, lowered the attractiveness of queen mandibular gland contents to workers, and caused down- and up-regulation of genes involved in egg laying, thus supporting the idea that queen pheromones act as honest indicators of queen reproductive fitness and that pesticide exposure of wax during bee development is an important and concerning factor impairing honey bee health. Our results provide evidence that in honey bees, queen developmental plasticity influences several measures of fitness, supporting the idea that a colony can be viewed (at least in part) as the expanded phenotype of its queen, and thus, selection acting predominantly at the colony level is congruent with that at the individual level.