Allopatric divergence of cooperators confers cheating resistance and limits the effects of a defector mutation

Studies of microbial social defectors that ‘cheat’ on cooperative genotypes generally focus on interactions with their cooperative parents, yet in nature defectors may meet diverse cooperators. Genotype-by-genotype interactions may constrain the ranges of cooperators upon which particular defectors can cheat, limiting the cheaters’ spread and potentially the overall equilibrium frequency of cheaters. The bacterium Myxococcus xanthus undergoes cooperative multicellular development upon starvation, but some developmental defectors can cheat on cooperators, outcompeting them within mixed groups. We show that a defector disrupted at the signaling gene csgA has a narrow cheating range among diverse natural cooperators owing to antagonisms not specifically targeted at defectors. More strikingly, lab-evolved cooperators only slightly differentiated from the defector have allopatrically evolved beyond its cheating range by accumulating fewer than 20 mutations when development was not directly u...