The functioning of biological systems relies on the cooperation of specialized components. Understanding the processes that produce such specialization - the ontogeny of biological systems - is a major challenge in biology. Although biological systems exist at multiple phenotypic scales, most studies of their ontogeny have focused on multicellular organisms. Here we expand our understanding of the ontogeny of biological systems to superorganisms (i.e., insect societies with specialized individuals). Using the black garden ant Lasius niger as a study system, we investigate how founding queens, the earliest developmental stage of ant colonies, transition from expressing a diverse repertoire of behaviors to being strictly specialized in egg production. We demonstrate that the presence of workers is sufficient and necessary to inhibit the behavioral pluripotency, and thus initiate the specialization of queens. We show that this specialization is reversible, as queens revert to expressing behavioral pluripotency upon removal of their workers, even after having been specialized for several years. We report a similar social control of queen behavior in another species, suggesting that it may be common in ants. This is supported by further indications that the behavior and physiology of founding queens may be regulated by ancestral mechanisms. In addition to presenting a novel approach to study the ontogeny of biological systems, our study has the potential to reshape our understanding of the specialization of ant queens, and thus of division of labor in insect societies.

Background The reproductive division of labor of eusocial insects, whereby one or several queens monopolize reproduction, evolved in a context of high genetic relatedness. However, many extant eusocial species have developed strategies that decrease genetic relatedness in their colonies, suggesting some benefits of the increased diversity. Multiple studies support this hypothesis by showing positive correlations between genetic diversity and colony fitness, as well as finding effects of experimental manipulations of diversity on colony performance. However, alternative explanations could account for most of these reports, and the benefits of diversity on performance in eusocial insects still await validation. In this study, we experimentally increased worker diversity in small colonies of the ant Lasius niger while controlling for typical confounding factors. Results We found that experimental colonies composed of workers coming from three different source colonies produced more larvae and showed more variation in size compared to groups of workers coming from a single colony. Conclusions We propose that the benefits of increased diversity stemmed from an improved division of labor. Our study confirms that worker diversity enhances colony performance, thus providing a possible explanation for the evolution of multiply mated queens and multiple-queen colonies in many species of eusocial insects.

No abstract

No abstract

The reproductive division of labor of eusocial insects, whereby one or several queens monopolize reproduction, evolved in a context of high genetic relatedness. However, many extant eusocial species have developed strategies that decrease genetic relatedness in their colonies, suggesting some benefits of the increased diversity. Multiple studies support this hypothesis by showing positive correlations between genetic diversity and colony fitness, as well as finding effects of experimental manipulations of diversity on colony performance. However, alternative explanations could account for most of these reports, and the benefits of diversity on fitness in eusocial insects still await validation. In this study, we experimentally increased worker diversity in the ant Lasius niger while controlling for typical confounding factors. We found that experimental colonies composed of workers coming from three different source colonies produced more larvae and showed more variation in size compared to groups of workers coming from a single colony. We propose that the benefits of increased diversity stemmed from an improved division of labor. Our study confirms that worker diversity enhances colony performance, thus providing a possible explanation for the evolution of multiply mated queens and multiple-queen colonies in many species of eusocial insects.