Sequential social experiences interact to modulate aggression but not brain gene expression in the honey bee (Apis mellifera)

Abstract

BackgroundIn highly structured societies, individuals behave flexibly and cooperatively in order to achieve a particular group-level outcome. However, even in social species, environmental inputs can have long lasting effects on individual behavior, and variable experiences can even result in consistent individual differences and constrained behavioral flexibility. Despite the fact that such constraints on behavior could have implications for behavioral optimization at the social group level, few studies have explored how social experiences accumulate over time, and the mechanistic basis of these effects. In the current study, I evaluate how sequential social experiences affect individual and group level aggressive phenotypes, and individual brain gene expression, in the highly social honey bee (Apis mellifera). To do this, I combine a whole colony chronic predator disturbance treatment with a lab-based manipulation of social group composition.ResultsCompared to the undisturbed control, chronically disturbed individuals show lower aggression levels overall, but also enhanced behavioral flexibility in the second, lab-based social context. Disturbed bees display aggression levels that decline with increasing numbers of more aggressive, undisturbed group members. However, group level aggressive phenotypes are similar regardless of the behavioral tendencies of the individuals that make up the group, suggesting a combination of underlying behavioral tendency and negative social feedback influences the aggressive behaviors displayed, particularly in the case of disturbed individuals. An analysis of brain gene expression showed that aggression related biomarker genes reflect an individual’s disturbance history, but not subsequent social group experience or behavioral outcomes.ConclusionsIn highly social animals with collective behavioral phenotypes, social context may mask underlying variation in individual behavioral tendencies. Moreover, gene expression patterns may reflect behavioral tendency, while behavioral outcomes are further regulated by social cues perceived in real-time.

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

“…This discrepancy could reflect differences in the stability of social effects experienced at these two different life stages. Socially-induced changes in aggression during adulthood are reversible (Alaux & Robinson 2007;Rittschof 2017;Shpigler et al 2017b), while effects induced during the pre-adult stages are relatively stable, present one week into adulthood, even when bees were kept in a common laboratory environment (Rittschof et al 2015a). Consistent with this hypothesis, the greatest degree of overlap between our gene expression results and previous aggression studies is with the shift in aggression associated with behavioral maturation in adult worker bees.…”

“…A recent study in honey bees showed that individuals exhibit different levels of social responsiveness, showing high or low levels of response to cues, whether or not these cues matched individual behavioral specialization (Shpigler et al 2017a). Similarly, chronic stress impacts how individuals respond to social cues in the context of aggression (Rittschof 2017). Behavioral variation could reflect individual variation in response thresholds to sensory stimuli.…”

“…We used different individual bees for the behavioral and molecular assays because the experience of an aggression assay causes extensive and lasting changes in gene expression (Alaux et al 2009;Rittschof et al 2014;Shpigler et al 2017b), which, in our case, could obscure the developmental effects we were targeting. All bees were kept in an incubator and fed 50% sucrose until they were 8 days old (Rittschof & Robinson 2013;Rittschof 2017). This approach allowed us to isolate the behavioral and molecular effects of the developmental environment, since all bees experienced a common laboratory environment for a prolonged time period as an adult.…”

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

“…One dish at a time, we introduced a foreign intruder bee to the group of six and observed aggressive interactions for 1 min. We made note of the most aggressive bee in the group, based on the amount of biting, abdomen flexion, and stinging directed toward the foreign intruder (Li‐Byarlay et al, ; Rittschof, ; Rittschof, Coombs, et al, ). We waited an additional 5 min following the 1 min observation period to shake the bees from the dish into a bag and knock them down on ice for dissection.…”

Brain mitochondrial bioenergetics change with rapid and prolonged shifts in aggression in the honey bee, Apis mellifera

“…For all brain assessments presented here, we analysed whole brains, with all glands removed, following previous studies (Alaux et al, 2009;Rittschof and Robinson, 2013;Rittschof et al, 2014;Chandrasekaran et al, 2015;Rittschof, 2017). We first assessed whether the aggressive behavioral response that results from alarm cue exposure is correlated with a shift in brain mitochondrial respiration.…”