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
under selection. Cooperators might diversify not only with respect to
which defectors cheat on them, but also in the potential for a particular
mutation to reduce expression of cooperative trait or generate a cheating
phenotype. We tested this by constructing a new csgA mutation in several
highly diverged cooperators. The mutation generated very different
sporulation phenotypes – from a complete defect to no defect – indicating
that genetic background effects can limit the set of genomes for which a
given mutation creates a defector and potentiates cheating. Our results
suggest that natural populations feature geographic mosaics of cooperators
diversified in susceptibility to cheating by any given defector and in the
social phenotypes generated by any given mutation in a cooperation gene.