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

Abstract

Crozier's Paradox states that genetic kin recognition will select for its own demise, and theoretical analyses over the past few decades have supported this conclusion. However, empirical evidence is far more limited. Here we examine support for Crozier's Paradox in 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. We find that co-isolated amoebae, taken from just a few grams of soil, harbor highly diverged recognition alleles, indicating plentiful sequence variation for social decision-making on a micro-scale. tgrB1 and tgrC1 belong to a large gene family, whose members vary in their levels of polymorphism, strength of selection, and retention of polymorphism. We do not see strong evidence for the paradox, in the form of positive frequency-dependent selection, or its outcome, in the form of depleted genetic variation. Consistent with previous findings, we detect recombination among the duplicated tgrB and tgrC genes, which suggests a mechanism to generate novel alleles and replenish genetic variation. We suggest that the evolutionary dynamics of large gene families may be essential for rapidly generating novel variation that can prevent Crozier's Paradox from taking effect.