Origin of division of labor is decoupled from polymorphism in colonial animals

Abstract

Division of labor, the specialization of sometimes phenotypically divergent cell types or group members, is often associated with ecological success in eukaryotic colonial organisms. Despite its many independent evolutionary origins, how division of labor originates remains unclear. Conventional hypotheses tend towards an 'economic' model, so that biological division of labor may reflect a partitioning of pre-existing tasks and morphologies into specialized colony members. Here, we present an alternative model of the origin of division of labor, which can explain the evolution of new functions within a colony. We show that in colonies of the Cretaceous aged (103-96 Ma) fossil bryozoan of the genus Wilbertopora, the first cheilostome bryozoan to evolve polymorphism, new member morphologies were not a simple partitioning of pre-existing morphologies, but instead expanded into novel morphospace as they lost functions, specifically feeding. This expansion into new morphologies occurred primarily during two pulses of heightened morphological disparity, suggesting that the evolution of polymorphism corresponded to relaxed constraints on morphology and perhaps to the exploration of novel functions. Using a simple model of physiological connections, we show that regardless of the functionality of these new colony members, all non-feeding members could have been supported by neighboring feeding members. This suggests that the geometric constraints and physiological connectedness could be prerequisites for evolving both polymorphism and division of labor in modular organisms, and that a classic partitioning model of specialization cannot be broadly applied to biological systems.