Honey bee neurogenomic responses to affiliative and agonistic social interactions

Abstract

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.

Changes of gene expression but not cytosine methylation are associated with male parental care reflecting behavioural state, social context, and individual flexibility

“…We also established orthology between Amel OGS3.2 (Elsik et al, 2014) and Nicve OGS1.0 using OrthoFinder (default setting using diamond; v2.1.2; Emms and Kelly, 2015) to assess the overlap of differentially expressed 'direct caring' genes between Shpigler et al (2018) and the present study.…”

“…It is unclear how to compare such studies and the present study, which is more concerned with rapid changes and switches that can be reversed. A more comparable study is that of Shpigler et al (2018), which compared young nurses present with queen larvae to initiate alloparental care. Shpigler et al (2018) sampled the mushroom body of the brain of nurses at 30, 60 and 120 min after care was initiated followed by RNA-seq.…”

“…A more comparable study is that of Shpigler et al (2018), which compared young nurses present with queen larvae to initiate alloparental care. Shpigler et al (2018) sampled the mushroom body of the brain of nurses at 30, 60 and 120 min after care was initiated followed by RNA-seq. We examined the overlap of the genes identified by Shpigler et al (2018) by establishing one-to-one orthology and then investigated the overlap between our 552 DEGs for the caring versus non-caring contrast and their 1268 DEGs from any sampling point.…”

Valence of social information is encoded in different subpopulations of mushroom body Kenyon cells in the honeybee brain

“…To represent positive valence, a laboratory-based social affiliation assay was used [39,49]. To simulate in-hive conditions where nursing occurs [49,51], this assay was performed in the rearing incubator (33 ± 1°C, 50 ± 10% relative humidity), and groups of bees were similarly allowed to acclimate to light undisturbed for at least 60 min.…”

“…Honeybees have tiny brains of approximately 1 000 000 neurons, roughly one-third of which are dedicated to higher-order sensory processing, learning and memory in a region termed the mushroom bodies (MBs) [37,38]. Shpigler et al [39] demonstrated with transcriptomic analyses that unique profiles of gene expression in the MBs are associated with behavioural responses to social affiliation or agonism, which invoke caregiving and aggression, respectively. These are behavioural responses to social interactions of positive and negative survival value, respectively, and are therefore representative of opposing biological valences [39].…”