Genotypic trade-off between appetitive and aversive capacities in honeybees

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.