The Collective Behavior of Ant Groups Depends on Group Genotypic Composition

Recently, researchers have documented variation between groups in collective behavior. However, how genetic variation within and between groups contributes to population-level variation for collective behavior remains unclear. Understanding how genetic variation of group members relates to group-level phenotypes is evolutionarily important because there is increasing evidence that group-level behavioral variation influences fitness and that the genetic architecture of group-level traits can affect the evolutionary dynamics of traits. Social insects are ideal for studying the complex relationship between individual and group-level variation because they exhibit behavioral variation at multiple scales of organization. To explore how the genetic composition of groups affects collective behavior, we constructed groups of pharaoh ants (Monomorium pharaonis) from 33 genetically distinct colonies of known pedigree. The groups consisted of either all workers from the same single colony or workers from two genetically different colonies, and we assayed the exploration and aggression of the groups. We found that collective exploration, but not aggression, depended on the specific genotypic combination of group members, i.e., we found evidence for genotype-by-genotype epistasis for exploration. Group collective behavior did not depend on the pedigree relatedness between genotypes within groups. Overall, this study highlights that specific combinations of genotypes influence group-level phenotypes, emphasizing the importance of considering nonadditive effects of genotypic interactions between group members.