Transcriptomic analysis of instinctive and learned reward-related behaviors in honey bees

Abstract

We used transcriptomics to compare instinctive and learned, rewardbased honey bee behaviors with similar spatio-temporal components: mating flights by males (drones) and time-trained foraging flights by females (workers), respectively. Genome-wide gene expression profiling via RNA sequencing was performed on the mushroom bodies, a region of the brain known for multi-modal sensory integration and responsive to various types of reward. Differentially expressed genes (DEGs) associated with the onset of mating (623 genes) were enriched for the gene ontology (GO) categories of Transcription, Unfolded Protein Binding, Post-embryonic Development, and Neuron Differentiation. DEGs associated with the onset of foraging (473) were enriched for Lipid Transport, Regulation of Programmed Cell Death, and Actin Cytoskeleton Organization. These results demonstrate that there are fundamental molecular differences between similar instinctive and learned behaviors. In addition, there were 166 genes with strong similarities in expression across the two behaviors -a statistically significant overlap in gene expression, also seen in Weighted Gene CoExpression Network Analysis. This finding indicates that similar instinctive and learned behaviors also share common molecular architecture. This common set of DEGs was enriched for Regulation of RNA Metabolic Process, Transcription Factor Activity, and Response to Ecdysone. These findings provide a starting point for better understanding the relationship between instincts and learned behaviors. In addition, because bees collect food for their colony rather than for themselves, these results also support the idea that altruistic behavior relies, in part, on elements of brain reward systems associated with selfish behavior.

Deep evolutionary conservation of autism-related genes

“…25 To validate the method and results, we ran two sets of control analyses. Honey bee control gene sets were derived from two RNA-seq expression sets from honey bee MB: (i) DEGs comparing active and inactive male honey bees (44) and (ii) DEGs comparing worker bees trained to forage at specific times of day (45). Human control gene sets were derived as follows.…”

Honey bee foraging induces upregulation of early growth response protein 1, hormone receptor 38 and candidate downstream genes of the ecdysteroid signalling pathway

“…Interestingly, Egr-1 and Hr38 expression levels were already slightly but significantly increased at t 0 compared to BF. This expression difference might be a result of flight activity in search for the known feeder or even anticipation of foraging activity (Naeger & Robinson, 2016). The foraging-induced IEG response is accompanied by an upregulation of downstream genes.…”

“…First, Egr-1 has been suggested to be one of the major transcription factors regulating gene expression changes during the transition from nursing to foraging (Khamis et al, 2015). Second, Egr-1 expression is upregulated during orientation flights and in anticipation of mating flights (Lutz & Robinson, 2013;Naeger & Robinson, 2016). Lutz & Robinson (2013) also demonstrated that Egr-1 upregulation is a consequence of higher sensory processing and learning instead of motor activity.…”

Honey bee neurogenomic responses to affiliative and agonistic social interactions

“…Second, the bees were from three independent colonies in each experiment (one colony was used in both experiments) and they were collected 2 years apart. These factors have been shown to have a strong influence on brain gene expression in honey bees . Hence, the similarity between these two experiments increases our confidence in the experimental design and in the robustness of the similarities.…”