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Cited by 35

The DOI matches its Crossref record; 57 of the 57 references it cites were found in a registry or an index.

Defense against territorial intrusion is associated with DNA methylation changes in the honey bee brain

Herb, Brian R., Shook, Molly S., Fields, Christopher J., Robinson, Gene E.·2018·BMC Genomics
DOI 10.1186/s12864-018-4594-0PMC PMC5870497
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Abstract

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 min post stimulus. For clusters of CpGs, we report four genomic regions differentially methylated between aggressive and control bees at the 5-min 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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Fig. 1 Regional DNA Methylation Differences Distinguish Aggressive And Control Bees. Aggressive bees (red) and control bees (blue) show distinct DNA methylation profiles. a) scaffold 2.11 contains 21 of the 50 min-120 DMRs. The region depicted spans the ~ 90 kb hotspot of DNA methylation change and contains many signaling genes. Top panel shows two examples of DMRs within scaffold 2.11 with smoothed lines representing average methylation levels of individual methylated CpG’s (ignoring CpGs with < 10% methylation levels). Middle panel displays “hotspot” region of scaffold 2.11 containing multiple DMRs. Horizontal bars within yellow DMR areas show average methylation levels for each DMR. b-c) Top panel presents DNA methylation level for a short segment of scaffold 11.16, with dots for individual CpGs and smoothed lines for average methylation levels for each phenotype. The DMR in (b) is located over the DH31-R (GB47217) calcitonin receptor, and the DMR in (c) is over the DH44 (GB48796) diuretic hormone gene, both important for stress response
Fig. 1 Regional DNA Methylation Differences Distinguish Aggressive And Control Bees. Aggressive bees (red) and control bees (blue) show distinct DNA methylation profiles. a) scaffold 2.11 contains 21 of the 50 min-120 DMRs. The region depicted spans the ~ 90 kb hotspot of DNA methylation change and contains many signaling genes. Top panel shows two examples of DMRs within scaffold 2.11 with smoothed lines representing average methylation levels of individual methylated CpG’s (ignoring CpGs with < 10% methylation levels). Middle panel displays “hotspot” region of scaffold 2.11 containing multiple DMRs. Horizontal bars within yellow DMR areas show average methylation levels for each DMR. b-c) Top panel presents DNA methylation level for a short segment of scaffold 11.16, with dots for individual CpGs and smoothed lines for average methylation levels for each phenotype. The DMR in (b) is located over the DH31-R (GB47217) calcitonin receptor, and the DMR in (c) is over the DH44 (GB48796) diuretic hormone gene, both important for stress responseCC BY · PubMed Central
Fig. 2 Gene expression changes in response to intruder are marked by both early and late epigenetic differences. Gene expression differences between aggressive and control bees that arise 120 min after interaction with an intruder are often marked with differences in DNA methylation. There were 140 genes that had differential methylation both before and after gene expression changes occurred. For both (a) and (b), the top panel depicts boxplots of DNA methylation levels at both time points for aggressive and control bees. Asterisks indicate significant differences between aggressive and control bees within time points. Note that different sets of CpGs have significant differences at different time points, thus marking gene before and after gene expression change at 120 min with distinct CpGs. The bottom panel shows the differentially expressed gene and the location of the CpGs within the gene body. (c) Summary of overlap between 120-min DEGs and suggestive CpG’s. Both 5-min and 120-min suggestive CpGs have significant overlaps with120-minute DEGs, with a high degree of co-localization within a subset of genes. (d) GO enrichments for genes both differentially expressed and differentially methylated in response to intruder exposure
Fig. 2 Gene expression changes in response to intruder are marked by both early and late epigenetic differences. Gene expression differences between aggressive and control bees that arise 120 min after interaction with an intruder are often marked with differences in DNA methylation. There were 140 genes that had differential methylation both before and after gene expression changes occurred. For both (a) and (b), the top panel depicts boxplots of DNA methylation levels at both time points for aggressive and control bees. Asterisks indicate significant differences between aggressive and control bees within time points. Note that different sets of CpGs have significant differences at different time points, thus marking gene before and after gene expression change at 120 min with distinct CpGs. The bottom panel shows the differentially expressed gene and the location of the CpGs within the gene body. (c) Summary of overlap between 120-min DEGs and suggestive CpG’s. Both 5-min and 120-min suggestive CpGs have significant overlaps with120-minute DEGs, with a high degree of co-localization within a subset of genes. (d) GO enrichments for genes both differentially expressed and differentially methylated in response to intruder exposureCC BY · PubMed Central

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Metadata

Authors
Herb, B. R., Shook, M. S., Fields, C. J., & Robinson, G. E.
Venue
BMC Genomics
Publisher
Springer Science and Business Media LLC
Published
2018-03-26
Volume
19
Issue
1
ISSN
1471-2164
DOI
10.1186/s12864-018-4594-0
PMC
PMC5870497
Cited by
35
References
57
Language
en
Licence
Funders
  • National Institutes of Health (R21-MH107962)
  • Simons Foundation (SFLife 291812)

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