Antagonistic, synergistic, and social pleiotropy in microbial cheaters

Abstract Cooperation is widespread among microbes. One mechanism proposed to constrain cheating is antagonistic pleiotropy, wherein mutations that cause defection from cooperation, while potentially under positive selection for this effect, reduce fitness at other traits. The bacterium Myxococcus xanthus engages in pleiotropically connected complex multicellular behaviors, including motility, predation, and starvation-induced fruiting-body development. Sporulation during development is susceptible to cheating. Here we investigate pleiotropic impacts on how cheater spores respond to stressful environmental changes after development, relative to cooperator spores. A cheater with a mutation in the developmental-signaling gene asgB shows antagonistic pleiotropy under both heat and basic-pH stress, while a cheater mutated at csgA shows synergistic pleiotropy under basic-pH stress. Further, in a social form of pleiotropy, cooperator spores formed in mixture with the asgB cheater are less resilient under basic pH than those from pure groups; interaction of cooperators with cheaters reduces the cooperators’ physical robustness. Our results indicate that, depending on the mutation, pleiotropy can promote as well as limit cheating alleles. They additionally demonstrate that alleles can pleiotropically alter traits in organisms not carrying those alleles. Synergistic and social pleiotropy may contribute to shaping the evolutionary dynamics of cooperation and cheating in many social systems.