First demonstration of olfactory learning and long-term memory in honey bee queens

As the primary source of colony reproduction, social insect queens play a vital role. However, the cognitive abilities of queens are not well understood, although queen learning and memory are essential in multiple species such as honey bees, in which virgin queens must leave the nest and then successfully learn to navigate back over repeated nuptial flights. Honey bee queen learning has never been previously demonstrated. We therefore tested olfactory learning in queens and workers and examined the role of DNA methylation, which plays a key role in long-term memory formation. We provide the first evidence that honey bee queens have excellent learning and memory. The proportion of honey bee queens that exhibited learning was 5-fold higher than that of workers at every tested age and, for memory, 4-fold higher than that of workers at a very young age. DNA methylation may play a key role in this queen memory because queens exhibiting remote memory had a more consistent elevation in Dnmt3 gene expression as compared with workers. Both castes also showed excellent remote memory (7 day memory), which was reduced by 14-20% by the DNA methylation inhibitor zebularine. Given that queens live approximately 10-fold longer than workers, these results suggest that queens can serve as an excellent long-term reservoir of colony memory.