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Many researchers consider language to be definitionally unique to humans. However, increasing evidence suggests that language emerged via a series of adaptations to neural systems supporting earlier capacities for visuomotor integration and manual action. This paper reviews comparative neuroscience evidence for the evolutionary progression of these adaptations. An outstanding question is how to mechanistically explain the emergence of new capacities from pre-existing circuitry. One possibility is that human brains may have undergone selection for greater plasticity, reducing the extent to which brain organization is hard-wired and increasing the extent to which it is shaped by socially transmitted, learned behaviors. Mutations that made these new abilities easier or faster to learn would have undergone positive selection, and over time, the neural changes once associated with individual neural plasticity would tend to become heritable, innate, and fixed. Clearly, though, language is not entirely “innate;” it does not emerge without the requisite environmental input and experience. Thus, a mechanistic explanation for the evolution of language must address the inherent trade-off between the evolutionary pressure for underlying neural systems to be flexible and sensitive to environmental input vs. the tendency over time for continually adaptive behaviors to become reliably expressed in an early-emerging, canalized, less flexible manner.