ABSTRACT:I contrast an ecological account of natural agency with the traditional Cartesian conception using recent research in bacterial cognition and cellular decision making as a test case. I argue that the Cartesian conception—namely, the view that agency presupposes cognition—generates a dilemma between mechanism, the view that bacteria are mere automata, and intellectualism, the view that they exhibit full-blown cognition. Unicellular organisms, however, occupy a middle ground between these two extremes. On the one hand, their capacities and activities are too adaptive to count as mere machines. On the other hand, they lack the open-ended responsiveness of cognitive agents to rational norms. An ecological conception of agency as the gross behavioral capacity to respond to affordances, I argue, does not presuppose cognition and allows for degrees of agency along a continuum, from the simplest adaptive agents, such as unicellular organisms, to the most sophisticated cognitive agents. Bacteria, I conclude, are adaptive agents, hence not mere automata, but not cognitive agents.

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The computational metaphor of organisms as phenotypic automata controlled by a genetic programme has been replaced by the cognitive metaphor of organisms as intelligent agents making decisions about how to use their genomic and environmental resources. This metaphor facilitates novel ways of thinking about organisms that defy the assumptions of the old machine metaphor. But like all metaphors, the cognitive metaphor discloses important similarities at the expense of eclipsing significant dissimilarities. I argue that although cognitivism carries with it the crucial insight that living organisms are agents rather than mere automata, this metaphor distorts the nature of biological agency by over-intellectualizing, which risks eliminating the distinction between life and mind. I trace the Cartesian root of these metaphors and argue that it generates a dilemma between mechanism and intellectualism. To capture the middle path that most organisms occupy between these two extremes, I propose an ecological account of natural agency.

What is a biological individual? How are biological individuals individuated? How can we tell how many individuals there are in a given assemblage of biological entities? The individuation and differentiation of biological individuals are central to the scientific understanding of living beings. I propose a novel criterion of biological individuality according to which biological individuals are autonomous agents. First, I articulate an ecological–dynamical account of natural agency according to which, agency is the gross dynamical capacity of a goal‐directed system to bias its repertoire to respond to its conditions as affordances. Then, I argue that agents or agential dynamical systems can be agentially dependent on, or agentially autonomous from, other agents and that this agential dependence/autonomy can be symmetrical or asymmetrical, strong or weak. Biological individuals, I propose, are all and only those agential dynamical systems that are strongly agentially autonomous. So, to determine how many individuals there are in a given multiagent aggregate, such as multicellular organism, a colony, symbiosis, or a swarm, we first have to identify how many agential dynamical systems there are, and then what their relations of agential dependence/autonomy are. I argue that this criterion is adequate to the extent that it vindicates the paradigmatic cases, and explains why the paradigmatic cases are paradigmatic, and why the problematic cases are problematic. Finally, I argue for the importance of distinguishing between agential and causal dependence and show the relevance of agential autonomy for understanding the explanatory structure of evolutionary developmental biology.