Honey bee colonies exhibit an age-related division of labor, with worker bees performing discrete sets of behaviors throughout their lifespan. These behavioral states are associated with distinct brain transcriptomic states, yet little is known about the regulatory mechanisms governing them. We used CAGEscan (a variant of the Cap Analysis of Gene Expression technique) for the first time to characterize the promoter regions of differentially expressed brain genes during two behavioral states (brood care (aka “nursing”) and foraging) and identified transcription factors (TFs) that may govern their expression. More than half of the differentially expressed TFs were associated with motifs enriched in the promoter regions of differentially expressed genes (DEGs), suggesting they are regulators of behavioral state. Strikingly, five TFs (nf-kb, egr, pax6, hairy, and clockwork orange) were predicted to co-regulate nearly half of the genes that were upregulated in foragers. Finally, differences in alternative TSS usage between nurses and foragers were detected upstream of 646 genes, whose functional analysis revealed enrichment for Gene Ontology terms associated with neural function and plasticity. This demonstrates for the first time that alternative TSSs are associated with stable differences in behavior, suggesting they may play a role in organizing behavioral state.
SUMMARYHoney bees can form distinct spatiotemporal memories that allow them to return repeatedly to different food sources at different times of day. Although it is becoming increasingly clear that different behavioral states are associated with different profiles of brain gene expression, it is not known whether this relationship extends to states that are as dynamic and specific as those associated with foraging-related spatiotemporal memories. We tested this hypothesis by training different groups of foragers from the same colony to collect sucrose solution from one of two artificial feeders; each feeder was in a different location and had sucrose available at a different time, either in the morning or afternoon. Bees from both training groups were collected at both the morning and afternoon training times to result in one set of bees that was undergoing stereotypical food anticipatory behavior and another that was inactive for each time of day. Between the two groups with the different spatiotemporal memories, microarray analysis revealed that 1329 genes were differentially expressed in the brains of honey bees. Many of these genes also varied with time of day, time of training or state of food anticipation. Some of these genes are known to be involved in a variety of biological processes, including metabolism and behavior. These results indicate that distinct spatiotemporal foraging memories in honey bees are associated with distinct neurogenomic signatures, and the decomposition of these signatures into sets of genes that are also influenced by time or activity state hints at the modular composition of this complex neurogenomic phenotype. Supplementary material available online at
crop pollination by the western honey bee Apis mellifera is vital to agriculture but threatened by alarmingly high levels of colony mortality, especially in Europe and North America. Colony loss is due, in part, to the high viral loads of Deformed wing virus (DWV), transmitted by the ectoparasitic mite Varroa destructor, especially throughout the overwintering period of a honey bee colony. Covert DWV infection is commonplace and has been causally linked to precocious foraging, which itself has been linked to colony loss. taking advantage of four brain transcriptome studies that unexpectedly revealed evidence of covert DWV-A infection, we set out to explore whether this effect is due to DWV-A mimicking naturally occurring changes in brain gene expression that are associated with behavioral maturation. Consistent with this hypothesis, we found that brain gene expression profiles of DWV-A infected bees resembled those of foragers, even in individuals that were much younger than typical foragers. In addition, brain transcriptional regulatory network analysis revealed a positive association between DWV-A infection and transcription factors previously associated with honey bee foraging behavior. Surprisingly, single-cell RNA-Sequencing implicated glia, not neurons, in this effect; there are relatively few glial cells in the insect brain and they are rarely associated with behavioral plasticity. Covert DWV-A infection also has been linked to impaired learning, which together with precocious foraging can lead to increased occurrence of infected bees from one colony mistakenly entering another colony, especially under crowded modern apiary conditions. These findings provide new insights into the mechanisms by which DWV-A affects honey bee health and colony survival. Western honey bees (Apis mellifera) provide an essential pollination service for modern agriculture, with a value estimated at $15 billion per year in the United States 1,2. Extensive reliance on pollination by honey bees has led to great concerns over the massive losses of managed colonies that have occurred since 2006 3-5. These losses are widely thought to be caused by parasites, pathogens, pesticides and poor nutrition, and the main parasite is the ectoparasitic mite Varroa destructor 6-10. Varroa mites are the primary vectors of Deformed wing virus (DWV) 11,12 , a single-stranded, positive-sense RNA virus (family Iflaviridae) that specifically impacts arthropods 13-16. DWV is globally distributed, driving an economic and ecological crisis in honey bee populations 17. DWV was first discovered in symptomatic deformed winged honey bees from Japan in the early 1980s 18 , and the first full genome was sequenced in 2006 19 , hereafter referred to as type A or DWV-A 20. Martin et al. showed through screening the Hawaiian honey bee population that diverse DWV variants persisted prior to the arrival of Varroa 21 ; however, the establishment of Varroa selected for a single variant, DWV-A. DWV-A is currently the most prevalent variant in the North America 22 , thoug...
Waves of highly infectious viruses sweeping through global honey bee populations have contributed to recent declines in honey bee health. Bees have been observed foraging on mushroom mycelium, suggesting that they may be deriving medicinal or nutritional value from fungi. Fungi are known to produce a wide array of chemicals with antimicrobial activity, including compounds active against bacteria, other fungi, or viruses. We tested extracts from the mycelium of multiple polypore fungal species known to have antiviral properties. Extracts from amadou (Fomes) and reishi (Ganoderma) fungi reduced the levels of honey bee deformed wing virus (DWV) and Lake Sinai virus (LSV) in a dose-dependent manner. In field trials, colonies fed Ganoderma resinaceum extract exhibited a 79-fold reduction in DWV and a 45,000-fold reduction in LSV compared to control colonies. These findings indicate honey bees may gain health benefits from fungi and their antimicrobial compounds.
Worker honey bees (Apis mellifera) undergo a process of behavioral maturation leading to their transition from in-hive tasks to foraging -a process which is associated with profound transcriptional changes in the brain. Changes in brain gene expression observed during worker behavioral maturation could represent either a derived program underlying division of labor or a general program unrelated to sociality. Male bees (drones) undergo a process of behavioral maturation associated with the onset of mating flights, but do not partake in division of labor. Drones thus provide an excellent reference point for polarizing transcriptional changes associated with behavioral maturation in honey bees. We assayed the brain transcriptomes of adult drones and workers to compare and contrast differences associated with behavioral maturation in the two sexes. Both behavioral maturation and sex were associated with changes in expression of thousands of genes in the brain. Many genes involved in neuronal development, behavior, and the biosynthesis of neurotransmitters regulating the perception of reward showed sexbiased gene expression. Furthermore, most of the transcriptional changes associated with behavioral maturation were common to drones and workers, consistent with common genetic and physiological regulation. Our study suggests that there is a common behavioral maturation program that has been co-opted and modified to yield the different behavioral and cognitive phenotypes of worker and drone bees.
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