Long-lasting coexistence of multiple asexual lineages alongside their sexual counterparts in a fungal plant pathogen

Cases of sexual to asexual transitions within species are key to understanding the evolution of reproductive modes, yet the coexistence of both modes in the same environment is poorly documented. Here, we reported this transition in a plant pathogen species coexisting in the same geographical environment. Our biological model is the poplar rust fungus Melampsora larici-populina, which displays a complex life cycle typical of rust fungi (Pucciniales). It alternates between two unrelated hosts to complete an obligate sexual life cycle once a year. We conducted a comprehensive population genetic analysis, utilizing 21 microsatellite markers and data from 2,122 individuals gathered over 30 years from various locations in France. Our results demonstrate the existence of many distinct lineages that reproduce asexually through the years, skipping the sexual phase. A clustering analysis identified a group of multilocus lineages that displayed all hallmarks of the genetic consequences of asexual reproduction, including highly negative and large variance among loci of the inbreeding coefficient (FIS). This indirect evidence for asexual reproduction was confirmed by the direct observation of these asexual lineages being repeatedly sampled across multiple years. This result demonstrates the coexistence of these lineages with their sexual counterparts in the same ecological niche, challenging conventional assumptions about geographical sorting of reproductive modes. These considerations are of paramount importance for understanding the contemporary evolution of major pathogen species. This switch from sexual to asexual reproduction has contributed to devastating epidemics worldwide.