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Transcriptomic and epigenetic responses to social challenge and their association with future behavior in honey bees (RNA-Seq)

ABSTRACT: We studied behavioral, brain transcriptomic and epigenetic responses of honey bees to social challenge. Bees were exposed to two intruders at different intervals. The initial exposure caused two behavioral effects at the individual level: an increase in the intensity of aggression toward a second intruder at 30 and 60 minutes, and an increased probability of responding aggressively toward a second intruder that persisted for two hours. The shorter-lived response was associated with one pattern of gene expression in the mushroom bodies, highlighted by genes related to cytoskeleton remodeling. The longer-lived response was associated with a different pattern; highlighted by genes related to hormones, stress response and transcription factors. Histone profiling revealed few changes in chromatin accessibility in response to social challenge; most differentially expressed genes were “ready” to be activated. These results demonstrate how biological embedding of a social challenge involves changes in the neurogenomic state to influence future behavior.

ORGANISM(S): Apis mellifera

PROVIDER: GSE85876 | GEO | 2017/03/29

SECONDARY ACCESSION(S): PRJNA339620

REPOSITORIES: GEO

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Project description:BACKGROUND: Social insects, such as honey bees, use molecular, physiological and behavioral responses to combat pathogens and parasites. The honey bee genome contains all of the canonical insect immune response pathways, and several studies have demonstrated that pathogens can activate expression of immune effectors. Honey bees also use behavioral responses, termed social immunity, to collectively defend their hives from pathogens and parasites. These responses include hygienic behavior (where workers remove diseased brood) and allo-grooming (where workers remove ectoparasites from nestmates). We have previously demonstrated that immunostimulation causes changes in the cuticular hydrocarbon profiles of workers, which results in altered worker-worker social interactions. Thus, cuticular hydrocarbons may enable workers to identify sick nestmates, and adjust their behavior in response. Here, we test the specificity of behavioral, chemical and genomic responses to immunostimulation by challenging workers with a panel of different immune stimulants (saline, Sephadex beads and Gram-negative bacteria E. coli). RESULTS: While only bacteria-injected bees elicited altered behavioral responses from healthy nestmates compared to controls, all treatments resulted in significant changes in cuticular hydrocarbon profiles. Immunostimulation caused significant changes in expression of hundreds of genes, the majority of which have not been identified as members of the canonical immune response pathways. Furthermore, several new candidate genes that may play a role in cuticular hydrocarbon biosynthesis were identified. Finally, we identified common genes regulated by pathogen challenge in honey bees and other insects, suggesting that immune responses are conserved at the molecular level. CONCLUSIONS: These studies suggest that honey bee genomic responses to immunostimulation are substantially broader than expected, and may mediate the behavioral changes associated with social immunity by orchestrating changes in chemical signaling.

Project description:Background: Aggression is influenced by individual variation in temperament as well as behavioral plasticity in response to adversity. DNA methylation is stably maintained over time, but also reversible in response to specific environmental conditions, and may thus be a neuromolecular regulator of both of these processes. A previous study reported DNA methylation differences between aggressive Africanized and gentle European honey bees. We investigated whether threat-induced aggression altered DNA methylation profiles in the honey bee brain in response to a behavioral stimulus (aggression-provoking intruder bee or inert control). We sampled five minutes and two hours after stimulus exposure to examine the effect of time on epigenetic profiles of aggression. Results: There were DNA methylation differences between aggressive and control bees for individual cytosine-guanine dinucleotides (CpGs) across the genome. Eighteen individual CpG sites showed significant difference between aggressive and control bees 120 minutes post stimulus. For clusters of CpGs, we report four genomic regions differentially methylated between aggressive and control bees at the 5-minute time point, and 50 regions differentially methylated at the120-minute time point following intruder exposure. Differential methylation occurred at genes involved in neural plasticity, chromatin remodeling and hormone signaling. Additionally, there was a significant overlap of differential methylation with previously published epigenetic differences that distinguish aggressive Africanized and gentle European honey bees, suggesting an evolutionarily conserved use of brain DNA methylation in the regulation of aggression. Lastly, we identified individually statistically suggestive CpGs that as a group were significantly associated with differentially expressed genes underlying aggressive behavior and also co-localize with binding sites of transcription factors involved in neuroplasticity or neurodevelopment. Conclusions: There were DNA methylation differences in the brain associated with response to an intruder. These differences increased in number a few hours after the initial exposure and overlap with previously reported aggression-associated genes and neurobiologically relevant transcription factor binding sites. Many DNA methylation differences that occurred in association with the expression of aggression in real time also exist between Africanized bees and European bees, suggesting an evolutionarily conserved role for epigenetic regulation in aggressive behavior.

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Transcriptomic and epigenetic responses to social challenge and their association with future behavior in honey bees (RNA-Seq)

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