Diversification of social complexity following a major evolutionary transition in bees.

Abstract

How social complexity evolved remains a long-standing enigma. In most animal groups, social complexity is typically classified into a few discrete classes. This approach is oversimplified and constrains our inference of social evolution to a narrow trajectory consisting of transitions between classes. Such categorical classifications also limit quantitative studies on the molecular and environmental drivers of social complexity. The recent accumulation of relevant quantitative data has set the stage to overcome these limitations. Here, we propose a data-driven, high-dimensional approach for studying the full diversity of social phenotypes. We curated and analyzed a comprehensive dataset encompassing 17 social traits across 80 species and studied the evolution of social complexity in bees. We found that honey bees, stingless bees, and bumble bees underwent a major evolutionary transition ∼80 mya, inconsistent with the stepwise progression of the social ladder conceptual framework. This major evolutionary transition was followed by a phase of substantial phenotypic diversification of social complexity. Other bee lineages display a continuum of social complexity, ranging from solitary to simple societies, but do not reach the levels of social complexity seen in honey bees, stingless bees, and bumble bees. Bee evolution, therefore, provides a remarkable demonstration of a macroevolutionary process in which a major transition removed biological constraints and opened novel evolutionary opportunities, driving the exploration of the landscape of social phenotypes. Our approach can be extended to incorporate additional data types and readily applied to illuminate the evolution of social complexity in other animal groups.