The Coevolution of Cellularity and Metabolism Following the Origin of Life

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ORIGINAL ARTICLE

The Coevolution of Cellularity and Metabolism Following the Origin of Life Yuta A. Takagi1 · Diep H. Nguyen1,2 · Tom B. Wexler3,4 · Aaron D. Goldman1,5  Received: 31 January 2020 / Accepted: 27 July 2020 / Published online: 18 August 2020 © The Author(s) 2020

Abstract The emergence of cellular organisms occurred sometime between the origin of life and the evolution of the last universal common ancestor and represents one of the major transitions in evolutionary history. Here we describe a series of artificial life simulations that reveal a close relationship between the evolution of cellularity, the evolution of metabolism, and the richness of the environment. When environments are rich in processing energy, a resource that the digital organisms require to both process their genomes and replicate, populations evolve toward a state of non-cellularity. But when processing energy is not readily available in the environment and organisms must produce their own processing energy from food puzzles, populations always evolve both a proficient metabolism and a high level of cellular impermeability. Even between these two environmental extremes, the population-averaged values of cellular impermeability and metabolic proficiency exhibit a very strong correlation with one another. Further investigations show that non-cellularity is selectively advantageous when environmental processing energy is abundant because it allows organisms to access the available energy, while cellularity is selectively advantageous when environmental processing energy is scarce because it affords organisms the genetic fidelity required to incrementally evolve efficient metabolisms. The selection pressures favoring either non-cellularity or cellularity can be reversed when the environment transitions from one of abundant processing energy to one of scarce processing energy. These results have important implications for when and why cellular organisms evolved following the origin of life. Keywords  Origin of life · Digital life · Ancient life · Early evolution · Coevolution · Evolution of cellularity · Evolution of metabolism

Handling editor: David Liberles. Yuta A. Takagi and Diep H. Nguyen have contributed equally to this work Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/s0023​9-020-09961​-1) contains supplementary material, which is available to authorized users. * Aaron D. Goldman [email protected] 1



Department of Biology, Oberlin College, Oberlin, OH 44074, USA

2



Computational and Systems Biology, Massachusetts Institute of Technology, Cambridge, MA 02139, USA

3

Department of Computer Science, Oberlin College, Oberlin, OH 44074, USA

4

Verily Life Sciences, Cambridge, MA, USA

5

Blue Marble Space Institute of Science, Seattle, WA 98154, USA



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Introduction The cell is, by definition, the basic structural unit of all organisms. Cellular organization defines the boundaries between organisms and their environment, allowing organisms to contro