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.