How to promote cooperative behavior is classically solved by incentives that lead self-interested individuals in socially desirable directions, but by now well-established laboratory results show that people often do act cooperatively, even at significant cost to themselves. These results suggest that cooperative dispositions might be an evolved part of human nature. Yet such dispositions appear inconsistent with the "Machiavellian intelligence" paradigm, which develops the idea that our brains have evolved, in substantial part, for capturing adaptive advantage from within-group competition. We use simulation to address the evolutionary relationship between basic Machiavellian capacities and cooperative dispositions. Results show that selection on such capacities can (1) permit the spread of cooperative dispositions even in cooperation-unfriendly worlds and (2) support transitions to populations with high mean cooperative dispositions. We distinguish between "rationality in action" and "rationality in design" - the adaptive fit between a design attribute of an animal and its environment. The combination of well-developed Machiavellian intelligence, modest mistrust, and high cooperative dispositions appears to be a rational design for the brains of highly political animals such as ourselves.
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