Whole-genome sequencing reveals recent and frequent genetic recombination between clonal lineages of Cryphonectria parasitica in western Europe.

Changes in the mode of reproduction are frequently observed in invasive fungal populations. The ascomycete Cryphonectria parasitica, which causes Chestnut Blight, was introduced to Europe from North America and Asia in the 20th century. Previous genotyping studies based on ten microsatellite markers have identified several clonal lineages which have spread throughout western Europe, suggesting that asexuality was the main reproductive mode of this species during colonization, although occasional sexual reproduction is not excluded. Based on the whole-genome sequences alignment of 46 C. parasitica isolates from France, North America and Asia, genealogy and population structure analyses mostly confirmed these lineages as clonal. However, one of these clonal lineages showed a signal of strong recombination, suggesting different strategies of reproduction in western Europe. Signatures of several recent recombination events within all the French clonal lineages studied here were also identified, indicating that gene flow is regular between these lineages. In addition, haplotype identification of seven French clonal lineages revealed that emergences of new clonal lineages during colonization were the result of hybridization between the main expanding clonal lineages and minor haplotypes non-sequenced in the present study. This whole-genome sequencing study underlines the importance of recombination events in the invasive success of these clonal populations, and suggests that sexual reproduction may be more frequent within and between the western European clonal lineages of C. parasitica than previously assumed using few genetic markers.

What was old is new again: thermal adaptation within clonal lineages during range expansion in a fungal pathogen.

Range-expanding species are expected to gain an increasing importance in the context of global change. They provide a great opportunity to study contemporary evolutionary changes and to unravel the mechanisms of evolution. Cryphonectria parasitica, the causal agent of chestnut blight, originating from Asia, has been spread since the beginning of the 20th century into different continents. We took advantage of the C. parasitica recent emergence in northern France to study the changes in population genetic structure and in phenotypic traits along this colonization and climatic gradient. Four hundred twenty-seven C. parasitica isolates were sampled in 47 chestnut sites in northern France. The C. parasitica outbreak in the north was found to be due to the expansion of five dominant clonal groups from southern France and to the emergence of a few rare recombined genotypes. The evolutionary changes during C. parasitica range expansion were studied by analysing phenotypic changes in isolates from the same clonal lineage, with or without a geographic shift. Growth rates were assessed in vitro, at four temperatures. The northern isolates grew faster at 12 and 15 °C and more slowly at 28 and 32 °C than the southern isolates. These results strongly suggest local adaptation to low temperatures in C. parasitica, with a trade-off of slower growth at high temperatures. They also reflect the high evolutionary potential of C. parasitica along a colonization gradient and show that clonal evolution is not a limitation for the rapid thermal adaptation of this invasive fungal species.