Although the Prisoner’s dilemma is a leading metaphor for the evolution of sociality, only a few studies demonstrate that this game indeed operates in nature. We offer an alternative perspective, in which parasites and their hosts are used as a model system, suggesting that Prisoner’s dilemma may be rare due to different individuals experiencing variation in the payoffs they receive from alternative strategies. Ectoparasites (such as fleas) move stochastically between hosts, causing differential parasite burdens. The resulting variance in the need for cooperation – in this case cooperative allogrooming – means that payoffs for different strategies (e.g. cooperate and defect) are not fixed. Our simulations revealed that due to parasite dynamics, cooperation among hosts conforms to a mixture of two games: Mutualism and Cruel Bind, both of which are more likely to coerce individuals into mutual cooperation than Prisoner’s dilemma. Though interesting, Prisoner’s dilemma is in fact the least likely scenario. If payoff variation is common, the dominance of the Prisoner’s dilemma paradigm may have made us unnecessarily puzzled by cooperation in nature.