Early-life experience of an aggressive social environment leads to lasting effects in the honey bee
Early-life social experiences cause lasting changes in behavior and health for a variety of animals including humans, but it is not well understood how social information ‘gets under the skin’ resulting in these effects. Adult honey bees (Apis mellifera) exhibit socially coordinated collective nest defense, providing a model for social modulation of aggressive behavior. Here we report for the first time that a honey bee’s early-life social environment has lasting effects on individual aggression: bees that experienced high-aggression environments during pre-adult stages showed increased aggression when they reached adulthood relative to siblings that experienced low-aggression environments, even though all bees were kept in a common environment during adulthood. Unlike other animals including humans however, high-aggression honey bees were more, rather than less, resilient to a neonicotinoid pesticide immune challenge, and aggression was negatively correlated with ectoparasitic mite presence. In honey bees, early-life social experience has broad effects, but increased aggression is decoupled from negative health outcomes. Because honey bees and humans share aspects of their physiological response to aggressive social encounters, our findings represent a step towards identifying ways to improve individual resiliency. Moreover, the pre-adult social experience may be crucial to the health of the ecologically threatened honey bee.
2015 Rittschof, C.C., C.B. Coombs, M. Frazier, C.M. Grozinger, and G.E. Robinson. Early-life experience affects honey bee aggression and resilience to immune challenge. Scientific Reports, in press.
Video clips of the intruder assay used to measure aggressive behaviors in the lab. In the top clip the intruder is crawling along the top of the dish. One bee lifts up to threaten the bee with mandibles open. She then chases the intruder. In the bottom clip, the unmarked intruder bee is grabbed by a bee with a yellow dot on her thorax. She pulls the bee to the ground and flexes her abdomen in a threat before releasing the intruder.
2015 [Invited Review] Rittschof, C.C., C.M. Grozinger, and G.E. Robinson. The energetic basis of behavior: bridging behavioral ecology and neuroscience. Current Opinion in Behavioral Sciences, in press.
Though studies in behavioral ecology and neuroscience independently emphasize a role for energy metabolism in modulating complex behavioral phenotypes, few studies have integrated both neurobiological and behavioral ecological perspectives to examine the mechanisms underpinning behavioral variation under different energetic conditions. Understanding these mechanisms across scales of biological organization has implications for behavioral evolution. Here we review the scope of known relationships between energy metabolism and behavior, focusing on honey bees, in which aggression, a complex behavior requiring multi-modal sensory integration, has been found to be associated with contrasting changes in energy metabolism at the whole-organism and brain levels. We explore the implications of tissue differences in metabolic rate, and how changes in energy metabolism in the aggressive brain may have consequences other than energy production. Increased knowledge of the brain energy correlates of behavior will clarify the role of energy in behavioral regulation and evolution.
|Relationships between energy metabolism and aggression across levels of biological organization|
See also: Trends in Neurosciences Spotlight Article:
Understanding the functional link between honey bee brain metabolism and aggression
Metabolic state in the aggressive brain resembles a common pattern in cancer and developing tissue
*Joint first authors
Using transcriptomic and metabolomics analyses of honey bee brains, we showed that aggression is associated with a shift towards aerobic glycolysis, a state characterized by increased glycolysis and decreased oxidative phosphorylation. Previous studies have shown this metabolic state to occur across many cell types, including tumors, developing tissues, and the healthy brain, though its function in the brain is unknown. Here we link this state to natural variation in behavior for the first time. Possible functional outcomes include increased excitability and changes in neural structure or neurotransmitter production.
Territorial intrusion induces similar neuromolecular changes across diverse species
Proceedings of the National Academy of Sciences (10.1073/pnas.1420369111):
Rittschof, C.C. et al. Neuromolecular responses to social challenge: common mechanisms across mouse, stickleback fish and honey bee
There is increasing evidence that certain complex phenotypes have shared molecular underpinnings. For instance, body patterning during development is regulated by conserved genes, and species-specificity is often the result of lineage specific mutations that influence the expression of these genes and associated gene networks. With colleagues at the Institute for Genomic Biology (University of Illinois), we applied this idea to social behaviors, comparing the neuromolecular response to territory intrusion across the house mouse, stickleback fish, and honey bee. These species are separated by ~650 million years of evolution and show differences in ecology and social organization. Nevertheless, territorial aggression is common to all three (and many other species), raising the possibility that this pattern of behavior could repeatedly evolve using the same molecular mechanisms. We found evidence for molecular similarities at the level of biological processes, gene network components, and individual genes. Similar to previous studies in the honey bee, brain energy metabolism emerged as a core process involved in territorial response. We also identified several transcription factors that were modulated by territorial intrusion in all three species. These included genes associated with autism spectrum disorders and socially-induced stress in humans and the response to conspecific song in birds, suggesting cross-species similarities in molecular mechanisms underlying social behavior could extend beyond our focal species. Neurodevelopmental processes were strongly implicated in the response to territory intrusion, suggesting conserved genes may regulate brain patterning during development as well as behavioral plasticity during adulthood.
Bees exposed to an aggression-inducing social cue show strong down-regulation of genes encoding oxidative phosphorylation proteins in the brain. Using pharmacological manipulations, we demonstrated a causal relationship between decreased oxidative phosphorylation activity and aggression. This effect, however, was dependent on a bee's prior social experience. These results suggest that modulating metabolic state may be one way that a social experience takes root in the brain, with lasting consequences for individual behavior. We also found that RNAi against mRNA that encodes an oxidative phosphorylation protein in fruit fly neurons causes increased aggression, while similar treatment in the glia has no affect on behavior. These results suggest the relationship between aggression and brain metabolism is evolutionarily conserved and cell-type specific.
Below: We assessed aggression using an assay whereby treated and control bees (kept in groups) are exposed to a foreign "intruder" bee. We measure aggressive behaviors towards the intruder.
H.L. Byarlay & C.C. Rittschof*, J. Massey, B. Pittendrigh, and G.E. Robinson. Socially responsive effects of brain oxidative metabolism on aggression. Proceedings of the National Academy of Sciences. 111: 12533-12537.
Chronic predator disturbance affects aggression and foraging activity
We manipulated the social environment within the bee hive by treating colonies with a chronic predator-like disturbance. This disturbance led to decreased colony aggressive response and foraging activity, as well as changes in aggression-related brain gene expression. We identified a subset of genes that are useful biomarkers of aggressive response.
Above and below: We built small colonies using bees of known age and genetic origin. The videos are clips from an assay used to measure colony aggression when colonies were 9 days old. We banged a brick on the roof of the colony while waving a cloth containing honey bee alarm pheromone in front of the entrance. We measured the number of bees that came out of the entrance in response. Control colonies (above) were left undisturbed for the 8 days preceding the assay while treatment colonies (below) were disturbed on a chronic basis during the 8 day time frame.
Rittschof, C.C. and G.E. Robinson. Manipulation of colony environment modulates honey bee aggression and brain gene expression. Genes, Brain, and Behavior. 12: 802-811.