The clonality window: relatedness and the group covariance effect in the evolution of division of labor

Cellular division of labor is closely associated with the emergence of organismality in the evolution of obligate multicellularity. Michod has suggested that a trade-off between viability and fecundity may-through a "group covariance effect"-lead to a group's fitness being augmented above the average of its constituents' fitnesses, offering a first step toward division of labor and obligate multicellularity. However, it is difficult to see how a group's fitness could be different from the aggregate of its constituents. Here, we investigate the same fitness trade-off and its consequences for division of labor. We recover the covariance effect, revealing that it is a consequence of cells sharing the products of their labors and clarifying that the group's fitness remains equal to the aggregate of the fitnesses of its constituent cells. We show that the covariance effect imparts an inclusive-fitness benefit for cells that share, but that-all else being equal-natural selection favors sharing only when groupmates are genetically identical, yielding a "clonality window." Lastly, we find that sharing is a critical determinant as to whether division of labor is favored by natural selection, such that the "clonality window" is also a prerequisite for division of labor in Michod's trade-off scenario.