Honeybee social regulatory networks are shaped by colony-level selection

Social interactions pervade all aspects of life in the social insects. Networks of interacting nestmates enable the maintenance of colony homeostasis and regulation of brood development. Artificial colony-level selection on the amount of pollen stored in honeybee colonies has produced high- and low-pollen-hoarding strains that have been used as a model system to study the genetic and physiological basis of differences in forager behavior that contribute to colony-level differences in pollen hoarding. Here we extend this model system using an interacting-phenotypes approach that explicitly studies genetic components arising from social interactions. High- and low-pollen-hoarding-strain larvae were reared in hives with high- or low-strain older larvae and high- or low-strain adult workers. The ovariole number and dry mass of focal individuals depended on interactions between the genotypes of the focal individuals and their brood and adult worker nestmates. These results show that trait expression by individual honeybee workers is modulated by the genotypic composition of the colony, indicating that individual-level phenotypes are properties of the composite "sociogenome." Thus, colony-level selection has produced strains with distinct combinations of socially interacting genes, which make up the social networks that regulate development and expressed phenotypes.