Tracking the evolutionary trajectory of a young hybrid plant pathogen

Abstract

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. Significance statementEmerging plant diseases pose serious risks to biodiversity and food production. A common mechanism by which fungal plant pathogens emerge on previously uncolonized hosts is hybridization. Hybridization brings together novel genetic combinations from different lineages that can facilitate adaptation to new environments. However, the evolutionary fate of hybrid pathogens is difficult to predict, and empirical studies of natural populations can help shed light on the dynamics of pathogen evolution following hybridization. Here, we use genomic data and infection assays to follow the evolutionary trajectory of a recently emerged hybrid plant pathogen. We show that the hybrid persists as an independent lineage distinct from both parents and analyze the genomic changes that have occurred in the few decades since initial hybridization.