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Political philosophers have long drawn explicitly or implicitly on claims about the ways in which human behaviour is shaped by interactions within society. These claims have usually been based on introspection, anecdotes or casual empiricism, but recent empirical research has informed a number of early views about human nature. We focus here on five components of such views: (1) what motivates human beings; (2) what constraints our natural and social environments impose upon us; (3) what kind of society emerges as a result; (4) what constitutes a fulfilling life; and (5) what collective solutions can improve the outcome. We examine social contract theory as developed by some early influential political philosophers (Hobbes, Locke and Rousseau), who viewed the social contract as a device to compare the ‘natural’ state of humans with their behaviour in society. We examine their views in the light of recent cross-cultural empirical research in the evolutionary social sciences. We conclude that social contract theorists severely underestimated human behavioural complexity in societies lacking formal institutions. Had these theorists been more informed about the structure and function of social arrangements in small-scale societies, they might have significantly altered their views about the design and enforcement of social contracts.