Early life exposure to queen mandibular pheromone mediates persistent transcriptional changes in the brain of honey bee foragers.

Behavioural regulation in insect societies remains a fundamental question in sociobiology. In hymenopteran societies, the queen plays a crucial role in regulating group behaviour by affecting individual behaviour and physiology through modulation of worker gene expression. Honey bee (Apis mellifera) queens signal their presence via queen mandibular pheromone (QMP). While QMP has been shown to influence behaviour and gene expression of young workers, we know little about how these changes translate in older workers. The effects of the queen pheromone could have prolonged molecular impacts on workers that depend on an early sensitive period. We demonstrate that removal of QMP impacts long-term gene expression in the brain and antennae in foragers that were treated early in life (1 day post emergence), but not when treated later in life. Genes important for division of labour, learning, chemosensory perception and ageing were among those differentially expressed in the antennae and brain tissues, suggesting that QMP influences diverse physiological and behavioural processes in workers. Surprisingly, removal of QMP did not have an impact on foraging behaviour. Overall, our study suggests a sensitive period early in the life of workers, where the presence or absence of a queen has potentially life-long effects on transcriptional activity.

Reproductive activation in honeybee (Apis mellifera) workers protects against abiotic and biotic stress.

Social insect reproductives exhibit exceptional longevity instead of the classic trade-off between somatic maintenance and reproduction. Even normally sterile workers experience a significant increase in life expectancy when they assume a reproductive role. The mechanisms that enable the positive relation between the antagonistic demands of reproduction and somatic maintenance are unclear. To isolate the effect of reproductive activation, honeybee workers were induced to activate their ovaries. These reproductively activated workers were compared to controls for survival and gene expression patterns after exposure to Israeli Acute Paralysis Virus or the oxidative stressor paraquat. Reproductive activation increased survival, indicating better immunity and oxidative stress resistance. After qPCR analysis confirmed our experimental treatments at the physiological level, whole transcriptome analysis revealed that paraquat treatment significantly changed the expression of 1277 genes in the control workers but only two genes in reproductively activated workers, indicating that reproductive activation preemptively protects against oxidative stress. Significant overlap between genes that were upregulated by reproductive activation and in response to paraquat included prominent members of signalling pathways and anti-oxidants known to affect ageing. Thus, while our results confirm a central role of vitellogenin, they also point to other mechanisms to explain the molecular basis of the lack of a cost of reproduction and the exceptional longevity of social insect reproductives. Thus, socially induced reproductive activation preemptively protects honeybee workers against stressors, explaining their longevity. This article is part of the theme issue 'Ageing and sociality: why, when and how does sociality change ageing patterns?'

Use of waggle dance information in honey bees is linked to gene expression in the antennae, but not in the brain.

Communication is essential for social animals, but deciding how to utilize information provided by conspecifics is a complex process that depends on environmental and intrinsic factors. Honey bees use a unique form of communication, the waggle dance, to inform nestmates about the location of food sources. However, as in many other animals, experienced individuals often ignore this social information and prefer to rely on prior experiences, i.e., private information. The neurosensory factors that drive the decision to use social information are not yet understood. Here we test whether the decision to use social dance information or private information is linked to gene expression differences in different parts of the nervous system. We trained bees to collect food from sugar water feeders and observed whether they utilize social or private information when exposed to dances for a new food source. We performed transcriptome analysis of four brain parts (11-16 bees per tissue type) critical for cognition: the subesophageal ganglion, the central brain, the mushroom bodies, and the antennal lobes but, unexpectedly, detected no differences between social or private information users. In contrast, we found 413 differentially expressed genes in the antennae, suggesting that variation in sensory perception mediates the decision to use social information. Social information users were characterized by the upregulation of biogenic amine genes, while private information users upregulated several genes coding for odour perception. These results highlight that decision-making in honey bees might also depend on peripheral processes of perception rather than higher-order brain centres of information integration.

Foraging and homing behavior of honey bees (Apis mellifera) during a total solar eclipse.

Exceptional natural phenomena, such as those that occur during a total solar eclipse, provide unique opportunities to study animal behavior outside the naturally evolved context, which can be informative in more general terms. Circumstantial descriptions of abnormal animal behavior during solar eclipses abound, although scientific studies conducted during an eclipse are relatively rare due to inherent logistical difficulties. Here, honey bee foraging and homing behavior were studied during the total solar eclipse of August 21, 2017. In the first experiment, we studied foraging behavior of honey bees during the progression of the solar eclipse and found that the foraging activity drastically decreased but did not completely cease during the totality of the eclipse, in contrast to previous reports of complete cessation. The data indicate that the level of ambient light can largely overrule the internal circadian rhythm of foraging honey bees. Furthermore, colonies with a higher need for foraging decreased their foraging activity less than satiated colonies, consistent with the hypothesis that individual foraging decisions may be influenced by colony state, which affects cost-benefit analyses. In a second experiment, the temporal dynamics of homing of released workers and drones was compared in periods before, during, and after the solar eclipse. During the totality of the eclipse, very few bees arrived back at their hive, while homing before the total eclipse was accelerated, particularly in drones. The results suggest that, while the homing abilities of honey bees are not compromised until the sun is completely eclipsed, they may still interpret the diminishing light as an indicator of deteriorating flight conditions. Our unique study provides some insight into the control of honey bee foraging behavior when external cues and internal circadian rhythms are at odds, lent support to the notion that food deprivation can lead to riskier foraging, and indicated that homing in honey bees is possible even with very small amounts of sunlight.