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

We used transcriptomics to compare instinctive and learned, reward-based 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 Co-Expression 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.