Individual differences in learning and biogenic amine levels influence the behavioural division between foraging honeybee scouts and recruits

Abstract

Animals must effectively balance the time they spend exploring the environment for new resources and exploiting them. One way that social animals accomplish this balance is by allocating these two tasks to different individuals. In honeybees, foraging is divided between scouts, which tend to explore the landscape for novel resources, and recruits, which tend to exploit these resources. Exploring the variation in cognitive and physiological mechanisms of foraging behaviour will provide a deeper understanding of how the division of labour is regulated in social insect societies. Here, we uncover how honeybee foraging behaviour may be shaped by predispositions in performance of latent inhibition (LI), which is a form of non-associative learning by which individuals learn to ignore familiar information. We compared LI between scouts and recruits, hypothesizing that differences in learning would correlate with differences in foraging behaviour. Scouts seek out and encounter many new odours while locating novel resources, while recruits continuously forage from the same resource, even as its quality degrades. We found that scouts show stronger LI than recruits, possibly reflecting their need to discriminate forage quality. We also found that scouts have significantly elevated tyramine compared to recruits. Furthermore, after associative odour training, recruits have significantly diminished octopamine in their brains compared to scouts. These results suggest that individual variation in learning behaviour shapes the phenotypic behavioural differences between different types of honeybee foragers. These differences in turn have important consequences for how honeybee colonies interact with their environment. Uncovering the proximate mechanisms that influence individual variation in foraging behaviour is crucial for understanding the ecological context in which societies evolve.

Keywords: exploration-exploitation trade-off; foraging; honeybee; latent inhibition; non-associative learning; scout; tyramine.

Figure 1:. LI scores for each foraging group including controls that are not pre-exposed to the odours.

Different letters indicate significant differences based on a Dunn post-hoc test. High scores indiciate more responses to the novel odour, whereas Scores close to 1 indicate equal responses to the novel and the familiar odour, whereas higher scores indiciate more responsiveness to a novel odour. n=27 recruits, 10 recruit controls, 34 scouts, and 11 scout controls. For this boxplot and all following: thick horizontal bars are medians, boxes are 25–75^th percentile, lines are 1.5 * IQR, points are outliers.

Figure 2:. Learning curves of bees tested for LI to illustrate qualitative similarities in LI.

Both graphs are from the same bees, grouped by either LI score or foraging behaviour. (A) Learning curves of bees score defined as scouts and recruits when collected; n=34 scouts, 26 recruits. (B) Learning curves of bees as defined by their LI scores. High LI bees are defined as any bee with a score of 1.33 or higher (or (3 responses to a+1)/(2 responses to x+1)), n= 39 “high LI” bees, 43 “low LI” bees.

Figure 3:. Concentrations of biogenic amines in the brains of untrained scouts and recruits.

Only tyramine differs significantly between recruits (n=28) and scouts (n=28), which were collected and frozen directly from the colony and did not undergo LI testing. An asterisk indicates statistical significance at alpha = 0.05 using a Kruskal-Wallis test.

Figure 4:. Concentrations of biogenic amines for scouts, recruits, and controls after PER training and LI determination.

Only octopamine differs significantly between scouts (n=34), recruits (n=27), and controls (n=11 scout controls, 10 recruit controls). Controls are individuals that went through the LI procedure but received no odour during pre-exposure. Unique letters indicate statistically significant differences according to a Dunn post-hoc test.