Abstract
Division of labor in social insects has made the evolution of collective traits possible that cannot be achieved by individuals alone. Differences in behavioral responses produce variation in engagement in behavioral tasks, which as a consequence, generates a division of labor. We still have little understanding of the genetic components influencing these behaviors, although several candidate genomic regions and genes influencing individual behavior have been identified. Here, we report that mixing of worker honeybees with different genotypes influences the expression of individual worker behaviors and the transcription of genes in the neuronal substrate. These indirect genetic effects arise in a colony because numerous interactions between workers produce interacting phenotypes and genotypes across organisms. We studied hygienic behavior of honeybee workers, which involves the cleaning of diseased brood cells in the colony. We mixed ∼500 newly emerged honeybee workers with genotypes of preferred Low (L) and High (H) hygienic behaviors. The L/H genotypic mixing affected the behavioral engagement of L worker bees in a hygienic task, the cooperation among workers in uncapping single brood cells, and switching between hygienic tasks. We found no evidence that recruiting and task-related stimuli are the primary source of the indirect genetic effects on behavior. We suggested that behavioral responsiveness of L bees was affected by genotypic mixing and found evidence for changes in the brain in terms of 943 differently expressed genes. The functional categories of cell adhesion, cellular component organization, anatomical structure development, protein localization, developmental growth and cell morphogenesis were overrepresented in this set of 943 genes, suggesting that indirect genetic effects can play a role in modulating and modifying the neuronal substrate. Our results suggest that genotypes of social partners affect the behavioral responsiveness and the neuronal substrate of individual workers, indicating a complex genetic architecture underlying the expression of behavior.
Highlights
The complexity and internal cohesion found within colonies of social insects stem from the coordinated behavioral activities of their colony members
Our results showed that genotypic mixing can modify gene expression in the neuronal substrate and can influence the uncapping behaviors of worker bees, the latter affecting the group performance
We showed that this indirect genetic effect has a variety of implications on uncapping behavior including effects on the uncapping engagement, the cooperation of workers at single cells, and the switching between hygienic tasks
Summary
The complexity and internal cohesion found within colonies of social insects stem from the coordinated behavioral activities of their colony members. The combined forces of potentially millions of individual workers allow colonies to modify their environments more efficiently, resulting in the tremendous ecological success of social insects in terrestrial ecosystems [1]. In the most advanced insect societies, such as those of honeybees (Apis mellifera), there is a strong reproductive division of labor into worker and queen castes. The queen reproduces, while the workers perform tasks mostly related to colony growth and development. Coordinated worker behaviors allow for the manifestation of complex, sophisticated traits that would be unachievable by single individuals, such as the building of intricate nest structures, the development of effective collective defense systems against diseases and predators and the ability to locate and exploit ephemeral food sources across the landscape
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