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.

许多物种形成不同的社会群体，为个体提供健康优势。然而，产生新社会群体的进化过程还不是很清楚。在这里，我们检查了模型社会细菌Myxococcus xanthus 的最近发散的天然分离物，探讨土壤中自然发生的亲属歧视的遗传机制和进化过程。我们表明，社会不相容性是由属于三种不同多态性毒素系统的效应子的水平基因转移形成的；外膜交换、VI 型分泌和重排热点系统。引人注目的是，导致社会不相容性的独特毒素效应子及其各自的免疫基因存在于可移动的遗传元件上，它们构成了进化枝内分离株之间几乎所有的基因型变异。通过破坏这三种毒素系统，我们设计了原本不相容的菌株之间的社会和谐。此外，单个亲属识别受体的水平等位基因交换改变了社会互动和竞争结果。我们的结果为横向基因转移如何导致自然环境中的社会多样化提供了一个案例研究。最后，我们展示了如何使用亲属歧视位点的基因组信息来预测社会互动。