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

PNAS Nexus. 2024 Oct 22;3(11):pgae476. doi: 10.1093/pnasnexus/pgae476. eCollection 2024 Nov.

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 emerges remains unclear. Conventional hypotheses tend toward an "economic" model, so that biological division of labor may reflect a partitioning of preexisting 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, preexisting morphologies were not simply partitioned among new members, but instead expanded into novel morphospace as they lost functions, specifically feeding. This expansion 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 nonfeeding members could have been supported by neighboring feeding members. This suggests that 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.