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

Abstract

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 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.

Hornets possess long-lasting olfactory memories

“…DesJardins and Tibbetts (2018) studied P. fuscatus workers and males (drones) over a wide age range (5-30 days) and found that workers were consistently better at facial learning, but the two castes were equally good at colour learning. Similarly, Gong et al (2018) reported that the proportion of honey bee queens (Apis mellifera) exhibiting learning was 5-fold higher than that of honey bee workers at every tested age (5-25 days). Finally, it is possible that workers had decreased learning ability as a result of senescence, given that they were 5 days older, on average, than gynes and males.…”

“…In comparison, honey bee (A. mellifera) worker and queen olfactory learning can reach 80% and 90%, respectively, after six learning trials (Gong et al, 2018). Bumble bees (Bombus terrestris) achieved an average of 60% (Riveros and Gronenberg, 2009) or nearly 45% (Stanley et al, 2015) after six learning trials.…”

“…This straw was placed over the abdomen and under the wings (Fig. 1A), following a method developed for honey bees (Gong et al, 2018). Individuals were able to move their heads and proboscises but could not escape ( Fig.…”

“…Bumble bee queens (Bombus terrestris) exhibit significantly better learning of food source colour than workers (Sheehan and Tibbetts, 2008). Honey bee queens (A. mellifera) have significantly better memory than workers bees, even up to 7 days (Gong et al, 2018). Queen wasps (P. fuscatus) are better than workers at learning and remembering conspecific faces , and queens can retain these memories for at least 1 week (Biergans et al, 2015).…”

“…Multiple species (V. vulgaris, V. germanica and Vespula maculifrons) can learn to associate odour with rewarding food sources (El-Sayed et al, 2018;Overmyer and Jeanne, 1998;Jander, 1998). However, many details of learning acquisition and memory, particularly long-lasting memories, remain unexplored in wasps, hornets and other social insects (Gong et al, 2018), although we know that such memories can potentially last >30 days in honey bees (Lindauer, 1960(Lindauer, , 1963Menzel, 1968) and at least 21 days in bumble bees (Chittka, 1998).…”