Colony phase structure favors permanent worker evolution in juvenile social systems

Abstract

Permanent workers in social insects, who forgo reproduction to help others, are a defining feature of superorganisms and a major evolutionary transition. Most theories assume that helping in the natal nests is inherently mutually exclusive from dispersal to found a new colony. This assumption holds for many adult societies whose workers cannot molt and change castes (e.g., Hymenoptera), but not for juvenile societies whose workers may differentiate and disperse after a period of helping (e.g., termites). The evolutionary advantage of permanent workers remains unknown in such juvenile societies with developmental flexibility. Here we develop a demographic model in which individuals can disperse either before or after a period of helping, capturing reversible helpers and permanent workers in termites. We found that permanent workers are favored when colony growth is divided into distinct ergonomic and reproductive phases, even if their performance is the same as that of reversible helpers. Without this phase separation, there is no selective advantage for workers to lose dispersal for colony foundation. After the phase separation, on the other hand, permanent workers increase continuous demographic growth and evolve through kin selection. By mapping diverse termite social systems onto a continuous landscape of ontogeny, the model traces a pathway linking different social forms. These results generalize social evolution theory beyond adult-worker systems by providing a demographic mechanism that favors the loss of the reproductive option.