Agency in the Evolutionary Transition to Multicellularity

2024 · doi:10.32942/x2x895
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This review examines how organism-initiated cellular and multicellular behavior, termed agency, evolved and relates to autonomy, purposiveness, and organismal form and function.

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This paper is a conceptual review examining how organismal “agency” (behavior initiated by the organism) relates to evolutionary transitions from unicellularity to multicellularity, including the evolution of animals from unicellular ancestors. Synthesizing arguments about organizational properties, it concludes that agency is not as strictly constrained in multicellular organisms as in individual cells, attributing this to morphogenetic inherencies of multicellular matter and the developmental capacity to amplify and partition functions across constituent cells. The authors discuss experimental approaches to distinguish agency from evolved stereotypical or purposeful behaviors, and they explicitly argue that animal development is unsuitable for experimentally probing single-cell-to-multicellular transitions in agency. Relevance to endometriosis: the paper does not explicitly discuss endometriosis or adenomyosis; it was included in the corpus via a keyword match in the upstream search index.

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Abstract

This review discusses concepts of how agency, defined here as organism-initiated behavior (both species-characteristic and individually idiosyncratic), was aligned at the cellular and integrated in the multicellular levels during evolution. We consider agency in relation to the autonomy and purposiveness of cells and multicellular organisms. While the agency of cells in extant multicellular forms (and inferred in single-cell antecedents) is assumed in our analysis, we do not speculate on its origins. We attempt to discern the role of agency in the generation of form and function in social bacteria and amoebae, and we speculate on how these phenomena may relate to the emergence of phenotypically complex organisms. For the latter question, we explore the processes leading to morphological and functional enablements in metazoans and how these might change the character of organismal agency during evolution. We also consider how transitions between multicellular agency and unicellular agency (and back again) may characterize and drive the formation of cancers. We relate this problem to the philosophical discourse on dispositional causality and discuss experimental approaches to identifying genuine agency against a background of physically mediated directionality and evolved program-like behaviors of organisms. Lastly, we discuss the possible uses of mathematical representations of incompletely specified dynamical systems in the characterization of autonomy and agency.
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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. DOI https://doi.org/10.32942/X2X895 Subjects Life Sciences

Keywords

autonomy, Determinism, dispositional causation, incompletely specified systems, inherency, physical scaffolding, social microorganisms Dates Published: 2024-03-02 14:13 Last Updated: 2025-01-30 05:35 Older Versions License CC BY Attribution 4.0 International Additional Metadata Conflict of interest statement: The authors have no conflict of interest to declare Data and Code Availability Statement: Not applicable Language: English

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License: CC-BY-4.0