Congruent population genetic structures and divergence histories in anther-smut fungi and their host plants Silene italica and the S. nutans species complex

The study of population genetic structure congruence between hosts and pathogens gives important insights into their shared phylogeographic and coevolutionary histories. We studied the population genetic structure of castrating anther-smut fungi (Microbotryum genus) and of their host plants, the Silene nutans species complex, and the morphologically and genetically close S. italica, which can be found in sympatry. Phylogeographic population genetic structure related to persistence in separate glacial refugia has been recently revealed in the S. nutans plant species complex across Western Europe, identifying several distinct lineages. We genotyped 171 associated plant-pathogen pairs of anther-smut fungi and their host plant individuals using microsatellite markers and plant chloroplastic SNPs. We found clear differentiation between fungal populations parasitizing S. nutans and S. italica plants. The population genetic structure of fungal strains parasitizing the S. nutans plant species complex mirrored the host plant genetic structure, suggesting that the pathogen was isolated in glacial refugia together with its host and/or that it has specialized on the plant genetic lineages. Using random forest approximate Bayesian computation (ABC-RF), we found that the divergence history of the fungal lineages on S. nutans was congruent with the one previously inferred for the host plant and likely occurred with ancient but no recent gene flow. Genome sequences confirmed the genetic structure and the absence of recent gene flow between fungal genetic lineages. Our analyses of host-pathogen individual pairs contribute to a better understanding of co-evolutionary histories between hosts and pathogens in natural ecosystems, in which such studies are still scarce.