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

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 regula...

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Main Authors: Brian R. Herb, Molly S. Shook, Christopher J. Fields, Gene E. Robinson
Format: Article
Language:English
Published: BMC 2018-03-01
Series:BMC Genomics
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12864-018-4594-0
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spelling doaj-24ecaf912d894fd697b60b0167fa241e2020-11-25T00:52:35ZengBMCBMC Genomics1471-21642018-03-0119111110.1186/s12864-018-4594-0Defense against territorial intrusion is associated with DNA methylation changes in the honey bee brainBrian R. Herb0Molly S. Shook1Christopher J. Fields2Gene E. Robinson3Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-ChampaignCarl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-ChampaignCarl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-ChampaignCarl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-ChampaignAbstract 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.http://link.springer.com/article/10.1186/s12864-018-4594-0AggressionDNA methylationBrainEpigeneticsTranscription factor binding sitesEvolution
collection DOAJ
language English
format Article
sources DOAJ
author Brian R. Herb
Molly S. Shook
Christopher J. Fields
Gene E. Robinson
spellingShingle Brian R. Herb
Molly S. Shook
Christopher J. Fields
Gene E. Robinson
Defense against territorial intrusion is associated with DNA methylation changes in the honey bee brain
BMC Genomics
Aggression
DNA methylation
Brain
Epigenetics
Transcription factor binding sites
Evolution
author_facet Brian R. Herb
Molly S. Shook
Christopher J. Fields
Gene E. Robinson
author_sort Brian R. Herb
title Defense against territorial intrusion is associated with DNA methylation changes in the honey bee brain
title_short Defense against territorial intrusion is associated with DNA methylation changes in the honey bee brain
title_full Defense against territorial intrusion is associated with DNA methylation changes in the honey bee brain
title_fullStr Defense against territorial intrusion is associated with DNA methylation changes in the honey bee brain
title_full_unstemmed Defense against territorial intrusion is associated with DNA methylation changes in the honey bee brain
title_sort defense against territorial intrusion is associated with dna methylation changes in the honey bee brain
publisher BMC
series BMC Genomics
issn 1471-2164
publishDate 2018-03-01
description 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.
topic Aggression
DNA methylation
Brain
Epigenetics
Transcription factor binding sites
Evolution
url http://link.springer.com/article/10.1186/s12864-018-4594-0
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