Hybrid inferiority and genetic incompatibilities drive divergence of fungal pathogens infecting the same host

Agro-ecosystems provide environments that are conducive for rapid evolution and dispersal of plant pathogens. Previous studies have demonstrated that hybridization of crop pathogens can give rise to new lineages with altered virulence profiles. Currently, little is known about either the genetics of fungal pathogen hybridization or the mechanisms that may prevent hybridization between related species. The fungus Pyrenophora teresis a global pathogen of barley. The pathogenic fungus P. teresexists as two distinct lineages P. teresf. teresand P. teresf. maculata(Pttand Ptm, respectively), which both infect barley but produce very distinct lesions and rarely interbreed. Interestingly, Pttand Ptmcan, by experimental mating, produce viable progenies. Here, we addressed the underlying genetics of reproductive barriers of P. teres. We hypothesize that Pttand Ptmdiverged in the past, possibly by adapting to distinct hosts, and only more recently colonized the same host in agricultural fields. Using experimental mating and in plantaphenotyping in barley cultivars susceptible to both P. teresforms, we demonstrate that hybrids produce mixed infection phenotypes but overall show inferior pathogenic fitness relative to the pure parents. Based on analyses of 104 hybrid genomes, we identify signatures of negative epistasis between parental alleles at distinct loci (Dobzhansky–Müller incompatibilities). Most DMI regions are not involved in virulence but certain genes are predicted or known to play a role in virulence. These results potentially suggest that divergent niche adaptation—albeit in the same host plant—contributes to speciation in P. teres.