Effects of load-lightening and delayed extrapair benefits on the fitness consequences of helping behavior

In most cooperative breeders, helping is directed at close kin, allowing helpers to gain indirect fitness benefits by increasing the reproductive success of close relatives, usually their parents. Extrapair paternity (EPP) occurs at high rates in some cooperative breeders, reducing the relatedness of helpers to the young they help raise. Even so, a son that helps is related to the brood by at least 0.25 through his mother and to within-pair young by 0.5, whereas a potential helper that has EPP in his own nest is related only to the offspring he sires and unrelated to any extrapair offspring. In birds, EPP often favors older males, which in the extreme case can result in sons being more closely related to young in their parents’ nest than to young in their own nests. The fitness benefit of helping will thus be enhanced if helping lightens the workload and increases survival of helpers and their fathers, enabling them to become old, hyper-successful extrapair sires. Here, we develop and analyze a proof-of-concept model, grounded in the western bluebird (Sialia mexicana) system, demonstrating the conditions under which high population levels of EPP can generate inclusive fitness benefits of helping behavior that outweigh the costs. This model provides a new perspective on the relationship between EPP and helping behavior in cooperative breeders and suggests a strong need for empirical work to gather unprecedented data on paternity over the lifetime of helpers and their parents.