It has become somewhat of a platitude to call Aristotle the first epigenesist insofar as he thought form and structure emerged gradually from an unorganized, amorphous embryo. But modern biology now recognizes two senses of “epigenesis”. The first is this more familiar idea about the gradual emergence of form and structure, which is traditionally opposed to the idea of preformationism. But modern biologists also use “epigenesis” to emphasize the context-dependency of the process itself. Used in this sense development is not (...) simply the unfolding of a pre-determined sequence of changes specified in advance by the organism’s genotype. It is also sensitive to inputs from the internal and external environment, which help determine in real-time which of the many potential developmental pathways are actualized during the process. Within this paradigm developing embryos are viewed as dynamic and responsive systems that react to inputs from the internal and external environment ‘on the fly’. In this paper I argue that, while Aristotle was an epigenesist in the first sense, he would have rejected epigenesis in the more modern sense. First, Aristotle’s model of choice for a developing embryo is the automaton that executes a set of preset movements (GA 734b9-13, 741b7-15). The automatons he has in mind are not dynamic AI systems capable of modifying their behaviour on the fly in response to environmental cues but completely deterministic mechanisms whose movements are fixed by their original design. Second, given Aristotle’s views about the different kinds of causal powers there are, it looks like only intentional agents endowed with actual decision-making powers could be capable of the sort of plasticity at the core of a more dynamic epigenesis. For that kind of epigenesis requires powers for alternative outcomes, and Aristotle is explicit that such powers require rational desires (προαίρεσις) that control which of those alternatives to bring about. If I am right, then he could not have made sense of the idea of a developing embryo (as a non-intentional system) making adjustments to its phenotype on the fly in response to emerging problems and opportunities, given the conceptual resources available to him. (shrink)