Data-driven analyses of social complexity in bees reveal phenotypic diversification following a major evolutionary transition

Abstract

How social complexity evolved is 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. This approach also limits quantitative studies on the molecular and environmental drivers of social complexity. However, the recent accumulation of relevant quantitative data has now set the stage to overcome these limitations. Here, we propose a data-driven approach for studying the full diversity of social phenotypes. We curated and analyzed a comprehensive dataset encompassing 17 social traits for 77 species and studied the evolution of social complexity in bees. We found that corbiculate bees -- honey bees, stingless bees, and bumble bees -- underwent a major evolutionary transition [~]70 mya, which is 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. Non-corbiculate bee lineages display a continuum of social complexity, ranging from solitary to simple societies, but do not reach levels of social complexity comparable to those of corbiculate bees. Bee evolution provides a unique 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 additional animal groups.