Rapid and widespread de novo evolution of kin discrimination.

Diverse forms of kin discrimination, broadly defined as alteration of social behavior as a function of genetic relatedness among interactants, are common among social organisms from microbes to humans. However, the evolutionary origins and causes of kin-discriminatory behavior remain largely obscure. One form of kin discrimination observed in microbes is the failure of genetically distinct colonies to merge freely upon encounter. Here, we first use natural isolates of the highly social bacterium Myxococcus xanthus to show that colony-merger incompatibilities can be strong barriers to social interaction, particularly by reducing chimerism in multicellular fruiting bodies that develop near colony-territory borders. We then use experimental laboratory populations to test hypotheses regarding the evolutionary origins of kin discrimination. We show that the generic process of adaptation, irrespective of selective environment, is sufficient to repeatedly generate kin-discriminatory behaviors between evolved populations and their common ancestor. Further, we find that kin discrimination pervasively evolves indirectly between allopatric replicate populations that adapt to the same ecological habitat and that this occurs generically in many distinct habitats. Patterns of interpopulation discrimination imply that kin discrimination phenotypes evolved via many diverse genetic mechanisms and mutation-accumulation patterns support this inference. Strong incompatibility phenotypes emerged abruptly in some populations but strengthened gradually in others. The indirect evolution of kin discrimination in an asexual microbe is analogous to the indirect evolution of reproductive incompatibility in sexual eukaryotes and linguistic incompatibility among human cultures, the commonality being indirect, noncoordinated divergence of complex systems evolving in isolation.

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.