Ontogeny of superorganisms:Social control of queen specialization in ants

Abstract

A central question in life sciences is to understand the ontogeny of biological systems, which exist at multiple phenotypic scales and function via the cooperation of specialized entities. Examples of such systems include multicellular organisms, which consist of specialized cells, and insect societies (or superorganisms), which are composed of specialized individuals. Both systems are products of major evolutionary transitions, and they share commonalities in their ontogeny, as both develop from a single, pluripotent unit. While the ontogeny of multicellular organisms is well understood, the factors and mechanisms that control the ontogeny of superorganisms remain poorly studied. Here, we report experimental investigations of the process of colony foundation in ants. In most ant species, a new colony is established by a solitary founding queen that expresses behavioral pluripotency to produce the first workers, at which point the queen becomes strictly specialized in egg production. We demonstrate that the presence of workers is necessary and sufficient to induce this specialization of queens. Moreover, workers also maintain the queen specialization in mature colonies, as established queens isolated from their workers revert to expressing behavioral pluripotency. Our results also suggest that this underappreciated social control of queen specialization may be common in ants and regulated by ancestral mechanisms. These findings stand in contrast to the traditional view of social insect queens as being intrinsically specialized in egg production and may reshape our understanding of division of labor in insect societies. Significance statementInsect societies are characterized by division of labor between queens that specialize in producing eggs and workers that perform all non-reproductive tasks. Studies of division of labor traditionally focused on fully established colonies and there is limited information on the factors and mechanisms that initiate division of labor during colony foundation. Here, we report that the presence of workers not only initiates the queen specialization, but also maintains it continually throughout the colony life. Finding such a social control of the specialization of queens contradicts the commonly accepted view of social insect queens as intrinsically specialized egg-laying machines. Our study has the potential to reshape our understanding of the functioning and evolution of insect societies.