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In the Bateson–Dobzhansky–Muller model of genetic incompatibilities post-zygotic gene-flow barriers arise by fixation of novel alleles at interacting loci in separated populations. Many such incompatibilities are polymorphic in plants, implying an important role for genetic drift or balancing selection in their origin and evolution. Here we show that  NPR1  and  RPP5  loci cause a genetic incompatibility between the incipient species  Capsella grandiflora  and  C. rubella , and the more distantly related  C. rubella  and  C. orientalis . The incompatible  RPP5  allele results from a mutation in  C. rubella , while the incompatible  NPR1  allele is frequent in the ancestral  C. grandiflora . Compatible and incompatible  NPR1  haplotypes are maintained by balancing selection in  C. grandiflora , and were divergently sorted into the derived  C. rubella  and  C. orientalis . Thus, by maintaining differentiated alleles at high frequencies, balancing selection on ancestral polymorphisms can facilitate establishing gene-flow barriers between derived populations through lineage sorting of the alternative alleles.

Divergent sorting of a balanced ancestral polymorphism underlies the establishment of gene-flow barriers in Capsella