Behavioral, transcriptomic and epigenetic responses to social challenge in honey bees

Abstract

Understanding how social experiences are represented in the brain and shape future responses is a major challenge in the study of behavior. We addressed this problem by studying behavioral, transcriptomic and epigenetic responses to intrusion in honey bees. Previous research showed that initial exposure to an intruder provokes an immediate attack; we now show that this also leads to longer-term changes in behavior in the response to a second intruder, with increases in the probability of responding aggressively and the intensity of aggression lasting 2 and 1 h, respectively. Previous research also documented the whole-brain transcriptomic response; we now show that in the mushroom bodies (MBs) there are 2 waves of gene expression, the first highlighted by genes related to cytoskeleton remodeling, and the second highlighted by genes related to hormones, stress response and transcription factors (TFs). Overall, 16 of 37 (43%) of the TFs whose cis-motifs were enriched in the promoters of the differentially expressed genes (DEGs) were also predicted from transcriptional regulatory network analysis to regulate the MB transcriptional response, highlighting the strong role played by a relatively small subset of TFs in the MB's transcriptomic response to social challenge. Whole brain histone profiling showed few changes in chromatin accessibility in response to social challenge; most DEGs were 'ready' to be activated. These results show how biological embedding of a social challenge involves temporally dynamic changes in the neurogenomic state of a prominent region of the insect brain that are likely to influence future behavior.

Temporal dynamics of neurogenomic plasticity in response to social interactions in male threespined sticklebacks

“…This result is consistent with the hypothesis that aggression and parental care share common neuroendocrine and neurogenomic substrates [36]. The relatively large number of upregulated DEG and increased chromatin accessibility at the 120 minute time point implies that much of the neurogenomic response to a brief territorial intrusion is related to recovery and preparing for the future, rather than producing the immediate behavioral response [38]. The increased accessibility and expression of genes related to immunity and learning at 120 minutes is consistent with this idea.…”

Deep evolutionary conservation of autism-related genes

“…To test this hypothesis, we exposed groups of 10 7-d-old honey bee nestmates to a social responsiveness assay in the laboratory, which involved exposures to two different social stimuli. One stimulus provided a social challenge: an unrelated bee as a territorial threat, which provokes an aggressive response (10,17). The other stimulus provided a social opportunity: a queen larva, which provokes alloparental care (19).…”

“…The upper part of the midbrain containing the MBs and some surrounding tissue (∼10%) was used for gene expression analysis. This MB preparation has been described in detail in previous work (10). The MB of each individual were placed in a new 1.5-mL microcentrifuge tube and kept frozen at −80°C until RNA extraction.…”

“…We used RNA sequencing (RNA-seq) to profile the mushroom bodies (MBs), a region of the insect brain involved in multimodal sensory integration (20) and recently implicated in honey bee social behavior (10).…”

“…However, this type of information is particularly important to our understanding of the relationship between animal behaviors and human mental health disorders. Emerging evidence for conserved molecular mechanisms for social behaviors between invertebrates and vertebrates (9)(10)(11)(12)(13)(14) suggests that there are similar connections to mental health disorders.…”