Diverse social interaction is key to honey bee (Apis mellifera, L.) thermoregulation

Abstract While high relatedness seems essential for social evolution, data from some organisms suggest more genetically diverse groups enjoy higher productivity. This phenomenon has been termed social heterosis. Unfortunately its proximate mechanisms are not wholly understood, due in part to the difficulty of connecting individual-level behavior to group-level outcomes. Here, we use the Western honey bee to examine how diverse social interaction impacts individual-level “task” performance (water foraging and entrance fanning) and measure the resulting change in a colony-level “emergent” phenotype (thermoregulation). With colonies consisting of workers from single or multiple inbred lines, we show both individual behavior and group phenotypes depend on social context with social heterosis occurring in some but not all combinations. We assess two potential mechanisms for social heterosis in diverse colonies: 1) task specialization between genotypes resulting in an optimized division of labor, and 2) increased participation or efficiency in task performance through a social rescue effect. While we found specialization across tasks in the first social mix, this did not result in an improved group phenotype. Meanwhile, we observed social heterosis in the second social mix seemingly driven by the rescue of task performance in one genotype without apparent specialization or change in task efficiency. This proof-of-concept experiment demonstrates task allocation can be quantified and linked to emergent phenotypes, but responses are context- and genotype-specific. These findings underscore the importance of social or indirect genetic effects in in understanding social evolution. Significance statement Social organisms share information and organize activities to better exploit their environment, making the group more productive than the sum of its parts. However, complex layers of interaction linking genes, individual behaviors, and group-level outcomes make understanding social evolution difficult. In this study, we demonstrate how genetic differences between individuals create group-level changes in honey bee nest-cooling. Using workers from diverse genetic lines, we created “solo” colonies consisting of single lines and “mixed” colonies of two lines. While we observed division of labor between genetic lines, this did not lead to greater group-level performance. Instead, it seems social stimuli in the mixed group allowed adaptive responses in genetic lines which were unresponsive in isolation. This work provides an example of a quantitative link from genetic to group-level changes and suggests indirect genetic effects as an important focus of further research in social evolution.