Biogenic amines and activity levels alter the neural energetic response to aggressive social cues in the honey bee <i>Apis mellifera</i>

Rittschof, Clare C.; Vekaria, Hemendra J.; Palmer, Joseph H.; Sullivan, Patrick G.

doi:10.1002/jnr.24443

“…We also found limited evidence that the brain molecular signature in the current study is enriched for genes modulated by social cues that induce aggression in adults. Interestingly, we do see a signature of carbohydrate metabolism among genes differentially expressed in the brain in our study, consistent with studies linking glycolysis and oxidative phosphorylation to social and environmental modulation of aggression (Li-Byarlay et al 2014;Rittschof et al 2014;Chandrasekaran et al 2015;Rittschof et al 2019). Finally, enrichment analyses provide some support for the hypothesis that variation in aggression in our study reflects variation in the pacing of behavioral maturation in adults.…”

Section: Discussionsupporting

confidence: 91%

“…It also shows substantial variation as a function of genetic background (Hunt et al 1998;Giray et al 2000;Guzman-Novoa et al 2004;Alaux et al 2009). However, transcriptomic studies suggest that the brain molecular profile associated with high aggression shows some similarities whether the source of behavioral variation is genetic or environmental (Alaux et al 2009;Chandrasekaran et al 2015;Rittschof et al 2015b), and this brain transcriptomic state has been connected to higher physiological levels (Chandrasekaran et al 2015;Rittschof et al 2019). A shared physiological profile of high aggression, regardless of the source of behavioral variation, could explain the widespread relationships between aggression and health outcomes within and among environments and genotypes.…”

Section: Introductionmentioning

confidence: 99%

The transcriptomic signature of low aggression honey bees resembles a response to infection

Rittschof

¹

,

Rubin

²

,

Palmer

³

2019

Preprint

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1

0

1

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“…We also found limited evidence that the brain molecular signature in the current study is enriched for genes modulated by social cues that induce aggression in adults. Interestingly, we do see a signature of carbohydrate metabolism among genes differentially expressed in the brain in our study, consistent with studies linking glycolysis and oxidative phosphorylation to social and environmental modulation of aggression (Li-Byarlay et al 2014;Rittschof et al 2014;Chandrasekaran et al 2015;Rittschof et al 2019). Finally, enrichment analyses provide some support for the hypothesis that variation in aggression in our study reflects variation in the pacing of behavioral maturation in adults.…”

Section: Discussionsupporting

confidence: 90%

“…It also shows substantial variation as a function of genetic background (Hunt et al 1998;Giray et al 2000;Guzman-Novoa et al 2004;Alaux et al 2009). However, transcriptomic studies suggest that the brain molecular profile associated with high aggression shows some similarities whether the source of behavioral variation is genetic or environmental (Alaux et al 2009;Chandrasekaran et al 2015;Rittschof et al 2015b), and this brain transcriptomic state has been connected to higher physiological levels (Chandrasekaran et al 2015;Rittschof et al 2019). A shared physiological profile of high aggression, regardless of the source of behavioral variation, could explain the widespread relationships between aggression and health outcomes within and among environments and genotypes.…”

Section: Introductionmentioning

confidence: 99%

The transcriptomic signature of low aggression honey bees resembles a response to infection

Rittschof

¹

,

Rubin

²

,

Palmer

³

2020

Preprint

Self Cite

2

1

0

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Background: Behavior reflects an organism's health status. Many organisms display a generalized suite of behaviors that indicate infection or predict infection susceptibility. We apply this concept to honey bee aggression, a behavior that has been associated with positive health outcomes in previous studies. We sequenced the transcriptomes of the brain, fat body, and midgut of adult sibling worker bees who developed as pre-adults in relatively high versus low aggression colonies. Previous studies showed that this pre-adult experience impacts both aggressive behavior and resilience to pesticides. We performed enrichment analyses on differentially expressed genes to determine whether variation in aggression resembles the molecular response to infection. We further assessed whether the transcriptomic signature of aggression in the brain is similar to the neuromolecular response to acute predator threat, exposure to a high-aggression environment as an adult, or adult behavioral maturation. Results: Across all three tissues assessed, genes that are differentially expressed as a function of aggression significantly overlap with genes whose expression is modulated by a variety of pathogens and parasitic feeding. In the fat body, and to some degree the midgut, our data specifically support the hypothesis that low aggression resembles a diseased or parasitized state. However, we find little evidence of active infection in individuals from the low aggression group. We also find little evidence that the brain molecular signature of aggression is enriched for genes modulated by social cues that induce aggression in adults. However, we do find evidence that genes associated with adult behavioral maturation are enriched in our brain samples. Conclusions: Results support the hypothesis that low aggression resembles a molecular state of infection. This pattern is most robust in the peripheral fat body, an immune responsive tissue in the honey bee. We find no evidence of acute infection in bees from the low aggression group, suggesting the physiological state characterizing low aggression may instead predispose bees to negative health outcomes when they are exposed to additional stressors. The similarity of molecular signatures associated with the seemingly disparate traits of aggression and disease suggests that these characteristics may, in fact, be intimately tied.

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“…It also shows substantial variation as a function of genetic background [3, 28, 35, 42]. However, transcriptomic studies suggest that the brain molecular profile associated with high aggression shows some similarities whether the source of behavioral variation is genetic or environmental [3, 16, 67], and this brain transcriptomic state has been connected to higher physiological levels in the brain [16, 70, 71]. A shared physiological profile of high aggression, regardless of the source of behavioral variation, could explain the widespread relationships between aggression and health outcomes within and among environments and genotypes.…”

Section: Introductionmentioning

confidence: 99%

The transcriptomic signature of low aggression in honey bees resembles a response to infection

Rittschof

¹

,

Rubin

²

,

Palmer

³

2019

Self Cite

View full text Add to dashboard Cite

BackgroundBehavior reflects an organism’s health status. Many organisms display a generalized suite of behaviors that indicate infection or predict infection susceptibility. We apply this concept to honey bee aggression, a behavior that has been associated with positive health outcomes in previous studies. We sequenced the transcriptomes of the brain, fat body, and midgut of adult sibling worker bees who developed as pre-adults in relatively high versus low aggression colonies. Previous studies showed that this pre-adult experience impacts both aggressive behavior and resilience to pesticides. We performed enrichment analyses on differentially expressed genes to determine whether variation in aggression resembles the molecular response to infection. We further assessed whether the transcriptomic signature of aggression in the brain is similar to the neuromolecular response to acute predator threat, exposure to a high-aggression environment as an adult, or adult behavioral maturation.ResultsAcross all three tissues assessed, genes that are differentially expressed as a function of aggression significantly overlap with genes whose expression is modulated by a variety of pathogens and parasitic feeding. In the fat body, and to some degree the midgut, our data specifically support the hypothesis that low aggression resembles a diseased or parasitized state. However, we find little evidence of active infection in individuals from the low aggression group. We also find little evidence that the brain molecular signature of aggression is enriched for genes modulated by social cues that induce aggression in adults. However, we do find evidence that genes associated with adult behavioral maturation are enriched in our brain samples.ConclusionsResults support the hypothesis that low aggression resembles a molecular state of infection. This pattern is most robust in the peripheral fat body, an immune responsive tissue in the honey bee. We find no evidence of acute infection in bees from the low aggression group, suggesting the physiological state characterizing low aggression may instead predispose bees to negative health outcomes when they are exposed to additional stressors. The similarity of molecular signatures associated with the seemingly disparate traits of aggression and disease suggests that these characteristics may, in fact, be intimately tied.

show abstract

Biogenic amines and activity levels alter the neural energetic response to aggressive social cues in the honey bee Apis mellifera

Cited by 26 publications

References 76 publications

The transcriptomic signature of low aggression honey bees resembles a response to infection

The transcriptomic signature of low aggression honey bees resembles a response to infection

The transcriptomic signature of low aggression honey bees resembles a response to infection

The transcriptomic signature of low aggression in honey bees resembles a response to infection

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