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

Authors: COOK, CHELSEA - Arizona State University; MOSQUIERO, THIAGO - University Of California; Brent, Colin; OZTURK, CAHIT - Arizona State University; GADAU, JURGEN - University Of Munster; PINTER-WOLLMAN, NOA - University Of California; SMITH, BRIAN - Arizona State University

Submitted to: Journal of Animal Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/31/2018
Publication Date: 2/20/2019
Citation: Cook, C.N., Mosquiero, T., Brent, C.S., Ozturk, C., Gadau, J., Pinter-Wollman, N., Smith, B.H. 2019. Individual differences in learning and biogenic amine levels influence the behavioural division between foraging honey bee scouts and recruits. Journal of Animal Ecology. 88:236-246.

Interpretive Summary: Individual variation in behavior can result from differences in learning capacity. In complex societies, this variation may play a role in establishing important divisions of labor. Here, we explore how honey bee foraging behavior may be shaped by how readily an individual can learn to associate familiar odors with important outcomes, such as food. We compared two types of foragers, scouts and recruits, hypothesizing that variation in learning ability would coincide with behavioral differences. Scouts encounter many new odors while searching for novel food sources, while recruits continuously forage from the same source, even as quality degrades. We found that scouts are less likely to learn to associate familiar odors with new resources than recruits, possibly reflecting their need to choose only the best quality of resources. Learning differences may be linked to brain neurotransmitter levels; scouts have significantly elevated tyramine compared to recruits, while octopamine levels decrease after training in recruits but not in scouts. The results suggest that variation in learning capacity shapes the behavioral differences that can lead to a complex division of labor in honey bees, which is crucial to understanding social evolution.

Technical Abstract: 1) Animals must effectively balance time spent exploring the environment for new food sources while exploiting known food sourcescaches. One way that animals accomplish this task is by dividing labour. In honey bees, foraging labour is divided by between scouts, which explore the landscape for novel foraging locations, and recruits, which exploit those locations until depleted. The underlying cognitive and physiological mechanisms that influence this division of labour have yet to be fully explored. 2) The goal of this study was to explore determine how honey bee foraging behaviour may be shaped by non-associative learning. Latent inhibition (LI) is a learning mechanism by which individuals more slowly learn to associate reward to information when they are already familiar with their lack of reinforcement. 3) We compared LI in two types of foragers, scouts and recruits, hypothesizing that variation in learning would correlate to variation in foraging behaviour. Scouts encounter many new odours while locating novel forage, while recruits continuously forage from the same source, even as quality degrades. 4) We found that scouts show stronger LI to unreinforced odours than recruits, possibly reflecting their need to discriminate forage quality. Learning differences may be linked to brain amine levels; scouts have significantly elevated tyramine compared to recruits. After associative odour training, recruits have significantly diminished octopamine in their brains compared to scouts. 5) The results suggest that variation in individual learning behaviour shapes the phenotypic differences that can lead to emergent division of foraging labour in honey bees. Insights such as these into the proximate mechanisms that influence individual variation is crucial to understanding social evolution.