Honey bee neurogenomic responses to affiliative and agonistic social interactions

Social interactions can be divided into two categories, affiliative and agonistic. How neurogenomic responses reflect these opposing valences is a central question in the biological embedding of experience. To address this question, we exposed honey bees to a queen larva, which evokes nursing, an affiliative alloparenting interaction, and measured the transcriptomic response of the mushroom body brain region at different times after exposure. Hundreds of genes were differentially expressed at distinct time points, revealing a dynamic temporal patterning of the response. Comparing these results to our previously published research on agonistic aggressive interactions, we found both shared and unique transcriptomic responses to each interaction. The commonly responding gene set was enriched for nuclear receptor signaling, the set specific to nursing was enriched for olfaction and neuron differentiation, and the set enriched for aggression was enriched for cytoskeleton, metabolism, and chromosome organization. Whole brain histone profiling after the affiliative interaction revealed few changes in chromatin accessibility, suggesting that the transcriptomic changes derive from already accessible areas of the genome. Although only one stimulus of each type was studied, we suggest that elements of the observed transcriptomic responses reflect molecular encoding of stimulus valence, thus priming individuals for future encounters. This hypothesis is supported by behavioral analyses showing that bees responding to either the affiliative or agonistic stimulus exhibited a higher probability of repeating the same behavior but a lower probability of performing the opposite behavior. These findings add to our understanding of the biological embedding at the molecular level. There are a total of 176 samples distributed between 3 factors: nurturance, with 88 nurturance (N) and 88 control (K); time after manipulation, with 58 30m, 60 60m, and 58 120m; and colony, with 60 colony R02, 60 colony R40, and 56 colony R41. The control and nurturance samples are paired by behavioral replicate, and we additionally report time spent in the waxen queen cell for bees exposed to queen cells. After observing the presence of Deformed Wing Virus (DWV) in a prior experiment on the same tissue, we screened each sample here for a proportion of reads aligning to the DWV genome of ≥ 0.005. No samples were excluded.