Evolutionary dynamics of the tgr gene family in Dictyostelium allows escape from Crozier's Paradox

Crozier's Paradox states that genetic kin recognition will select for its own demise, and theoretical analyses over the past decades have supported this conclusion. Here we examine the molecular evolution of two kin recognition genes in the social amoeba Dictyostelium discoideum , tgrB1 and tgrC1 , which enable cells to recognize and reject unrelated cells during cooperative multicellular development. Our results reveal extraordinary polymorphism in these genes, placing them amongst the most rapidly evolving genes in the genome. Co-occurring amoebae, isolated from just a few grams of soil, show highly diverged recognition alleles, indicating plentiful sequence variation that can impact social decision-making on a micro-scale. Analyses of closely related gene duplicates show dynamic evolution of the gene family as a whole, suggesting a mechanism for replenishing genetic variation lost through Crozier's Paradox. Our results provide evidence that kin recognition loci can retain sufficient genetic variation in real-world settings and suggest that large gene families may be crucial to retaining genetic variation necessary to evade Crozier's paradox.