Social Contact Acts as Appetitive Reinforcement and Supports Associative Learning in Honeybees

Social learning is taxonomically widespread in the animal kingdom [1], and although it is long thought to be a hallmark of vertebrates, recent studies revealed that it also exists in insects [2-5]. The adaptive functions of social learning are well known, but its underlying mechanisms remain debated [2, 5, 6]. Social insects critically depend on the social transmission of information for successful food search and their colonies' fitness [7] and are tractable models for studying the social cues and cognitive mechanisms involved [2-5]. Besides the well-known dance language allowing them to communicate the location of food sources among nestmates [8], honeybees also learn chemosensory information about these sources both outside and within the hive [9, 10]. In the latter case, they associate the floral scent carried by returning foragers on their body with the nectar provided through mouth-to-mouth trophallaxis, similar to the manner in which foragers directly learn odorant-nectar reward associations at the foraging patch [9-11]. Strikingly, however, neither the dance nor trophallaxis is strictly necessary for foragers recruited within the hive to find the right floral source, and simple body contact between foragers may be sufficient [12]. What is the reinforcing agent in this case? We show here that simple social contact acts as appetitive reinforcement and can be used in associative olfactory learning. We demonstrate that this social reinforcement is mediated by bees' antennal movements and modulated by bees' behavioral development. These results unveil a social learning mechanism that may play a facilitating role in resource exploitation by social groups.