Individuals that forgo their own reproduction in animal societies represent an evolutionary paradox because it is not immediately apparent how natural selection can preserve the genes that underlie non-breeding strategies. Cooperative breeding theory provides a solution to the paradox: non-breeders benefit by helping relatives and/or inheriting breeding positions; non-breeders do not disperse to breed elsewhere because of ecological constraints. However, the question of why non-breeders do not contest to breed within their group has rarely been addressed. Here, we use a wild population of clownfish (Amphiprion percula), where non-breeders wait peacefully for years to inherit breeding positions, to show non-breeders will disperse when ecological constraints (risk of mortality during dispersal) are experimentally weakened. In addition, we show non-breeders will contest when social constraints (risk of eviction during contest) are experimentally relaxed. Our results show it is the combination of ecological and social constraints that promote the evolution of non-breeding strategies. The findings highlight parallels between, and potential for fruitful exchange between, cooperative breeding theory and economic bargaining theory: individuals will forgo their own reproduction and wait peacefully to inherit breeding positions (engage in cooperative options) when there are harsh ecological constraints (poor outside options) and harsh social constraints (poor inside options).