Positively Frequency-Dependent Interference Competition Maintains Diversity and Pervades a Natural Population of Cooperative Microbes

Positively frequency-dependent selection is predicted from theory to promote diversity in patchily structured populations and communities, but empirical support for this prediction has been lacking. Here, we investigate frequency-dependent selection among isolates from a local natural population of the highly social bacterium Myxococcus xanthus. Upon starvation, closely related cells of M. xanthus cooperate to construct multicellular fruiting bodies, yet recently diverged genotypes co-residing in a local soil population often antagonize one another during fruiting-body development in mixed groups. In the experiments reported here, both fitness per se and strong forms of interference competition exhibit pervasive and strong positive frequency dependence (PFD) among many isolates from a centimeter-scale soil population of M. xanthus. All strains that compete poorly at intermediate frequency are shown to be competitively dominant at high frequency in most genotype pairings during both growth and development, and strongly so. Interference competition is often lethal and appears to be contact dependent rather than mediated by diffusible compounds. Finally, we experimentally demonstrate that positively frequency-dependent selection maintains diversity when genotype frequencies vary patchily in structured populations. These results suggest that PFD contributes to the high levels of local diversity found among M. xanthus social groups in natural soil populations by reinforcing social barriers to cross-territory invasion and thereby also promotes high within-group relatedness. More broadly, our results suggest that potential roles of PFD in maintaining patchily distributed diversity should be investigated more extensively in other species.