Rapid diversification of wild social groups driven by toxin-immunity loci on mobile genetic elements

Many species form distinct social groups that provide fitness advantages to individuals. However, the evolutionary processes that generate new social groups are not well understood. Here we examined recently diverged natural isolates of the model social bacterium, Myxococcus xanthus, to probe the genetic mechanisms and evolutionary processes of kin discrimination that occurred naturally in soil. We show that social incompatibilities were formed from horizontal gene transfer of effectors belonging to three distinct polymorphic toxin systems; outer membrane exchange, type VI secretion and rearrangement hotspot systems. Strikingly, the unique toxin effectors and their respective immunity genes that are responsible for social incompatibilities reside on mobile genetic elements, which make up nearly all of the genotypic variation between isolates within clades. By disrupting these three toxin systems, we engineered social harmony between strains that were originally incompatible. In addition, a horizontal allele swap of a single kin recognition receptor changed social interactions and competition outcomes. Our results provide a case study for how horizontal gene transfer led to social diversification in a natural context. Finally, we show how genomic information of kin discriminatory loci can be used to predict social interactions.