Oxytocin and the punitive hub — Dynamic spread of cooperation in human social networks

Human society operates on large-scale cooperation. However, individual differences in cooperativeness and incentives to free-ride on others’ cooperation make large-scale cooperation fragile and can lead to reduced social-welfare. Thus, how individual cooperation spreads through human social networks remains puzzling from ecological, evolutionary and societal perspectives. Here, we identify oxytocin and costly punishment as biobehavioral mechanisms that facilitate the propagation of cooperation in social networks. In three laboratory experiments (n = 870 human participants, 373 males and 497 females), individuals were embedded in heterogeneous networks and made repeated decisions with feedback in games of trust (n = 342), ultimatum bargaining (n = 324), and prisoner’s dilemma with punishment (n = 204). In each heterogeneous network, individuals at central positions (hub nodes) were given intranasal oxytocin (or placebo). Giving oxytocin (versus matching placebo) to central individuals increased their trust and enforcement of cooperation norms. Oxytocin-enhanced norm enforcement, but not elevated trust, explained the spreading of cooperation throughout the social network. Moreover, grounded in evolutionary game theory, we simulated computer agents that interacted in heterogeneous networks with central nodes varying in terms of cooperation and punishment levels. Simulation results confirmed that central cooperators’ willingness to punish non-cooperation allowed the permeation of the network and enabled the evolution of network cooperation. These results identify an oxytocin-initiated proximate mechanism explaining how individual cooperation facilitates network-wide cooperation in human society and shed light on the widespread phenomenon of heterogeneous composition and enforcement systems at all levels of life. Significance statement: Human society operates on large-scale cooperation. Yet because cooperation is exploitable by free-riding, how cooperation in social networks emerges remains puzzling from evolutionary and societal perspectives. Here we identify oxytocin and altruistic punishment as key factors facilitating the propagation of cooperation in human social networks. Individuals played repeated economic games in heterogeneous networks where individuals at central positions were given oxytocin or placebo. Oxytocin-enhanced cooperative norm enforcement, but not elevated trust, explained cooperation spreading throughout the social network. Evolutionary simulations confirmed that central cooperators’ willingness to punish non-cooperation allowed the permeation of the network and enabled the evolution of cooperation. These results identify an oxytocin-initiated proximate mechanism explaining how individual cooperation facilitates network-wide cooperation in human social networks.