The Evolution of Interdependent Cell Cycles During the Transition to Multicellularity

Homa Papoli Yazdi , Mohammad A. Siddiq, Hwei-Yen Chen , Charlie Kinahan Cornwallis 

In the evolution of complex multicellular organisms, cells that were once autonomous became obligately dependent on one another for survival and reproduction. Despite its importance, the process by which autonomous cellular machinery was restructured into obligately interdependent networks is poorly understood. Addressing this gap requires a framework that clearly categorizes the different levels of interdependence and identifies how the ancient, conserved eukaryotic cell-cycle machinery of unicellular species was modified so that cell survival and reproduction became conditional on other cells. Here, we first examine the cellular autonomy in unicellular organisms and how cell fitness in these organisms can be influenced by interactions with other cells, revealing ancestral mechanisms that may have been co-opted during the transition to multicellularity. Second, we trace how an increasingly interdependent cell network emerged, from undifferentiated multicellular organisms in which all cells maintain their reproductive ability to organisms with reversible and irreversible germ-soma differentiation. Central to this transition is understanding how cell cycle machinery was modified to integrate extracellular signals and enable the inheritance of cellular states across the cell cycles. Finally, we propose a framework to structure comparative studies of how cellular autonomy was progressively restricted during the repeated, independent origins of obligate multicellularity.