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).

In species with biparental care, conflict arises over how much each parent provides to their offspring because both parents benefit from shifting the burden of care to the other. Here, we tested alternative hypotheses for how parents will negotiate offspring care using a wild population of clownfish (Amphiprion percula). We experimentally handicapped parents by fin-clipping the female in 23 groups, the male in 23 groups, and neither parent in 23 groups and measured changes in indicators of female, male, and pair effort in response to handicapping. First, we found that handicapping resulted in a decrease in the number of eggs laid by fin-clipped females and a decrease in the amount of parental care by fin-clipped males. Second, contrary to predictions, female effort did not change in response to the male being handicapped, or vice versa. Finally, the number of embryos that matured to hatching, an indicator of pair effort, was not influenced by the manipulation, suggesting that although the handicap was effective, clownfish do not face the predicted “cost to conflict” when one parent is handicapped. Together, these results test the generality of theoretical predictions and uncover novel questions about whether and how negotiations operate in systems where interests are aligned.