Heritable Variation in Learning Phenotypes Drive Collective Cognition

Collective cognition allows animal groups to accomplish many tasks that could not be accomplished as effectively alone, such as schools of fish avoiding predators, flocks of birds moving thousands of miles across the Earth, and honey bee colonies collecting food from millions of flowers. Individuals in groups utilize local information to quickly adjust to ecological changes by implicitly or explicitly communicating information with group members to form a collective decision. However, individuals vary in their cognitive abilities, which influences the information each individual pays attention to or shares, thus influencing collective responses. Here, we show that individual differences in learning scales to shape collective foraging behavior in honey bees by utilizing a naturally variable and heritable learning behavior called latent inhibition (LI). We artificially selected two distinct phenotypes: high LI bees that are better at ignoring previously unrewarding familiar stimuli, and low LI bees that learn previously unrewarding and novel stimuli equally well. Colonies comprised of high LI individuals preferred to visit familiar food location, while low LI colonies visit novel and familiar food locations equally. However, in colonies of mixed learning phenotypes, the low LI bees showed a preference to visiting familiar feeders, which contrasts with their behavior when in a uniform group. We show that the shift in the feeder preference of low LI bees in uniform low LI versus mixed colonies is driven by foragers of the high LI phenotype dancing more intensely and attracting more followers. These results reveal that variation in individual learning phenotypes contributes to collective decision making in social animals.