The Quarterly Review of Biology
Agency in the Evolutionary Transition to Multicellularity
Stuart A. Newman, Mariana Benítez, Ramray Bhat, Tilmann Glimm, K. Vijay Kumar, Vidyanand Nanjundiah, Daniel J. Nicholson, and Sahotra Sarkar
Abstract
This review explores agency, behavior intrinsic to an organism and initiated by it, as it relates to the development of multicellular organisms and its evolution. We ask how agential behaviors contribute to and change concomitantly with evolutionary transitions from unicellularity to multicellularity, including evolution of animals from their closest unicellular antecedents. We consider the relation of organizational properties to the agency of multicellular organisms and conclude, surprisingly, that it is not as strict as it is for individual cells. The main reasons are previously unacknowledged morphogenetic inherencies of multicellular matter and the capacity of development to amplify and partition functionalities of constituent cells. These modalities generate novel phenotypic enablements that enhance the scope of agential behavior. We discuss experimental approaches to distinguish between agency and evolved, stereotypical behaviors of organisms, including purposeful actions. We argue that evolved complexities of animal development make it unsuitable for exploring single-cell-to-multicellular transformations in agency experimentally. We focus our attention instead on agency in the life cycles of social bacteria and amoebae, and in the transitions between multicellular and unicellular states in cancer. Finally, we discuss mathematical representations of incompletely specified dynamical systems and how they may be used to characterize biological autonomy and agency.
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