Abstract
Honey bees can learn both appetitive and aversive associations, using two olfactory conditioning protocols. Appetitive conditioning of the proboscis extension response (PER) involves associating an odor, the conditioned stimulus (CS) with a sucrose solution, the unconditioned stimulus (US). Conversely, aversive conditioning of the sting extension response (SER) involves associating the odor CS with an electric or thermal shock US. Here, we investigated the relationship between bees’ appetitive and aversive learning capacities at the individual level and the influence of bees’ genotype. As learning performance was shown to depend on an individuals’ sensitivity to the US, we systematically measured four different traits in each individual bee: sensitivity to sucrose, PER learning performance with a sucrose US, sensitivity to temperature, SER learning with a temperature US. First, we confirmed for both conditioning types that learning performance correlates with US responsiveness. Second, we found a trade-off between appetitive and aversive learning performances: bees that were better appetitive learners (and had a lower sucrose US threshold) learned less efficiently in the aversive conditioning (and had a higher temperature US threshold). Because the honey bee queen typically mates with 15–20 males, the workers from a honey bee hive belong to as many different patrilines, allowing for the search of the genetic determinism of cognitive abilities. Using microsatellite analysis, we show that a genetic determinism underlies the trade-off between appetitive and aversive capacities, with appetitively vs aversively biased patrilines. The honey bee hive thus appears as a genetically structured cognitive community.
Highlights
Where to find food and how to avoid danger? These are two simple but critical questions animals need to answer for surviving in a wild environment
Bees were subjected to a differential conditioning protocol in which they had to differentiate between a reinforced odor (CS+) and a non-reinforced odor (CS−)
The conditioned stimulus (CS)+ was associated with a sucrose reward and for aversive learning, the CS+ was associated with a temperature punishment
Summary
Where to find food and how to avoid danger? These are two simple but critical questions animals need to answer for surviving in a wild environment. The self-organization theoretical account presented above predicts that within a social group, different individuals should display different response thresholds to appetitive and aversive stimuli, as they are related to different tasks, respectively food-associated tasks and defense-oriented tasks. We asked how sensitivity and learning capacity in appetitive and aversive modalities are distributed among individuals composing a honeybee colony, in particular with regards to their patriline of origin. Performing the experiments on age-controlled individuals, we found a clear trade-off between aversive and appetitive abilities at the individual level This aversive vs appetitive trade-off appeared when taking into account the bees’ patrilines. These results suggest that within a eusocial insect colony workers compose an equilibrium of cognitively-specialized individuals, giving rise to a complex but highly-adaptable cognitive community
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