Ikerbasque Keywords Metabolism, adaptive behavior, autopoiesis, chemotaxis A version of this paper with color figures is available online at http://dx.doi.org/10.1162/ artl_a_00047. Subscription required. Abstract We use a minimal model of metabolism-based chemotaxis to show how a coupling between metabolism and behavior can affect evolutionary dynamics in a process we refer to as behavioral metabolution. This mutual influence can function as an in-the-moment, intrinsic evaluation of the

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... e value of a novel situation, such as an encounter with a compound that activates new metabolic pathways. Our model demonstrates how changes to metabolic pathways can lead to improvement of behavioral strategies, and conversely, how behavior can contribute to the exploration and fixation of new metabolic pathways. These examples indicate the potentially important role that the interplay between behavior and metabolism could have played in shaping adaptive evolution in early life and protolife. We argue that the processes illustrated by these models can be interpreted as an unorthodox instantiation of the principles of evolution by random variation and selective retention. We then discuss how the interaction between metabolism and behavior can facilitate evolution through (i) increasing exposure to environmental variation, (ii) making more likely the fixation of some beneficial metabolic pathways, (iii) providing a mechanism for in-the-moment adaptation to changes in the environment and to changes in the organization of the organism itself, and (iv) generating conditions that are conducive to speciation. of artificial agents. This area of research includes models of minimally cognitive systems, collective behavioral dynamics, and the study of specific neurophysiological mechanisms (see, e.g., [8, 26] ). It is noteworthy, however, that there has been little study of the interaction between the chemistry of life and cognitive or adaptive behavior. In general, models that focus on the self-organization of chemical systems work with a set of fixed boundary conditions, making adaptive behavior unnecessary for system survival. And conversely, models that study behavior tend to abstract away everything except the sensory, control, and motor mechanisms. This is, perhaps, starting to change. There has been a series of recent models that explore the interaction between processes that determine how a system is constituted (metabolism) and mechanisms through which the system influences its interaction with its environment (behavior ). These models include computer simulations [16, 17, 45] as well as real chemical systems [25] , and they have led to some interesting reconceptualizations: Metabolic processes can be thought of as robust or even adaptive, able to intelligently modulate behavioral strategies [17] ; remarkably simple chemical reactions can perform chemotaxis [25] ; and in a range of bacteria, metabolism-based behavior appears to be more common than previously thought [2] . This article continues in this effort to explore the interface between metabolism and behavior. While the role of behavior in evolution has been a central topic in biology ever since Darwin, there have been very few attempts to systematically investigate the relevance of behavior in early evolution and the origin of life. This state of affairs is understandable, since it is only very recently that experimental evidence has shown that prebiotic protocells can indeed behave, i.e., move, or in some other way select their environment and/or alter their coupling with it. In this article we propose that metabolism-based behavior could have played an important evolutionary role in early life, providing protocells with an adaptive capability of seeking favorable environmental conditions. We discuss how this capability could facilitate the accumulation of novel metabolic pathways, leading potentially to more sophisticated protocells, and how the mechanisms underlying this behavior-based facilitation of evolution are so simply implemented that they could have played a role in bootstrapping genetic evolution. We shall start by introducing some central concepts and summarizing the results of previous models on metabolism-based bacterial chemotaxis (Section 2). In Section 3, we introduce the idea of behavioral metabolution, illustrating some of the evolutionary possibilities of the coupling between metabolism and behavior with a computational model of protocellular metabolism-based chemotaxis. The model consists of a minimal metabolic system capable of modulating behavior by influencing the probability of flagellar rotation (as in Escherichia coli chemotaxis). In the first scenario we explore with the model, the incorporation of a chemical compound into metabolism qualitatively improves the chemotactic strategy. In the second, an encounter with a specific chemical compound opens up a new metabolic pathway, and the metabolism-based behavior of the organism automatically regulates chemotaxis toward the newly metabolizable resource. Both experiments illustrate the adaptive potential of metabolism-based behavior. While we make no direct claims about the likelihood of these specific events occurring, the model nevertheless allows us to elaborate, in Section 4, some principles of behavioral metabolution and discuss their application to early prebiotic evolution and subsequent evolution of chemotaxis. Metabolism and Behavior: The Case of Bacterial Chemotaxis Metabolism can be conceptualized as the far-from-thermodynamic-equilibrium organization of chemical networks that produce and sustain their components by using available energetic and material resources [22, 30, 33, 50] . There is a long tradition of investigating the origins and essence of life through the study of metabolism. Recently, some of this research has focused upon metabolism in the context of protocells [37] . Protocells are theoretical predecessors to cells. They are individuated, self-maintaining systems that have similarities to cells, but are much simpler-lying halfway between life and chemistry. Rarely has M. D. Egbert et al. Behavioral Metabolution M. D. Egbert et al.