Promiscuity drives self-referent kin recognition

Kin selection theory has been one of the most significant advances in our understanding of social behavior. However, the discovery of widespread promiscuity has challenged the evolutionary importance of kin selection because it reduces the benefit associated with helping nestmates. This challenge would be resolved if promiscuous species evolved a self-referent kin-recognition mechanism that enables individuals to differentiate kin and nonkin. Here, we take advantage of an asymmetry in the level of promiscuity among males of alternative life histories in the bluegill sunfish (Lepomis macrochirus). We show that, as a consequence of this asymmetry, offspring of “parental” males have a high level of relatedness to nestmates, whereas offspring of “cuckolder” males have a low level of relatedness to nestmates. We find that offspring of parentals do not use a direct recognition mechanism to discriminate among nestmates, whereas offspring of cuckolders use kin recognition by self-referent phenotype matching to differentiate between kin and nonkin. Furthermore, we estimate that the cost of utilizing such self-referent kin recognition is equivalent to a relatedness (R) of at least 0.06. These results provide compelling evidence for adaptive use of kin recognition by self-referent phenotype matching and confirm the importance of kinship in social behavior.