Tracking the Evolutionary Trajectory of a Young Hybrid Plant Pathogen

A common mechanism by which emerging plant pathogens gain the ability to infect new hosts is hybridization. Despite its widespread occurrence, the outcomes of hybridization remain largely unpredictable within current evolutionary frameworks, making empirical studies key for identifying patterns and establishing principles underlying hybrid evolution. Here, we track the evolutionary trajectory of Blumeria graminis forma specialis triticale (B.g. triticale), or triticale powdery mildew, a pathogen that emerged recently through hybridization of two powdery mildew forms specialized on wheat (B.g. tritici) and rye (B.g. secalis). Using a genomic dataset of 652 isolates from the three formae speciales, we show that they persist as three isolated lineages. Results from our infection assays and sampling suggest that B.g. triticale is not well adapted to infect wheat under field conditions, indicating that isolation between B.g. tritici and B.g. triticale may be maintained by partial niche separation. We investigated the genomic changes following hybridization and found that at least a third of the hybrid genome is fixed for B.g. tritici ancestry in contemporary populations, and around 1% is fixed for the B.g. secalis ancestry. We identified several loci to be under recent positive selection in B.g. triticale, most of which coincide with known genes and regions of fixed or nearly fixed local ancestry. Overall, we highlight the role of ecological isolation in preventing gene flow between B.g. triticale and its parental lineages. We reveal the rapid stabilization of its genome after hybridization and show that some of these changes were likely shaped by selection.