Temporal regulation of kin recognition maintains recognition-cue diversity and suppresses cheating

Kin recognition, the ability to distinguish kin from non-kin, can facilitate cooperation between relatives. Evolutionary theory predicts that polymorphism in recognition cues, which is essential for effective recognition, would be unstable. Individuals carrying rare recognition cues would benefit less from social interactions than individuals with common cues, leading to loss of the genetic-cue diversity. We test this evolutionary hypothesis in Dictyostelium discoideum, which forms multicellular fruiting bodies by aggregation and utilizes two polymorphic membrane proteins to facilitate preferential cooperation. Surprisingly, we find that rare recognition variants are tolerated and maintain their frequencies among incompatible majority during development. Although the rare variants are initially excluded from the aggregates, they subsequently rejoin the aggregate and produce spores. Social cheating is also refrained in late development, thus limiting the cost of chimerism. Our results suggest a potential mechanism to sustain the evolutionary stability of kin-recognition genes and to suppress cheating.