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

Abstract Sexual-to-asexual transitions within species are crucial for understanding reproductive evolution, yet the coexistence of both modes of fungal species in the same environment is poorly documented. Here, we report this transition in a plant pathogen species that coexists within 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, using 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. 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. Competing Interest Statement The authors have declared no competing interest. Footnotes In this revised version, the figures and analysis workflow have been updated. A life cycle schematic has been added and is now presented as the main figure. Additional figures showing the silhouette analysis and the sampling collection strategy have also been included. The R code has been updated to improve clarity, reproducibility, and execution.