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

Sexual to asexual transition is described as a process whereby asexual lineages emerge within sexual species. This phenomenon gives rise to many questions about the maintenance of sexual reproduction and the evolution of asexuality in these organisms. The poplar rust fungusMelampsora larici-populinahas a complex life cycle, which is typical of rust fungi (Pucciniales). It alternates between a sexual reproduction phase on larch trees (Larixspp.) and rounds of asexual multiplication on poplar trees (Populusspp.). This alternation between sexual and asexual reproduction shows some similarities with the cyclical parthenogenesis observed in aphids and daphnia. This study challenges the classic understanding of theM. larici-populinalife cycle. Our results demonstrate the existence of many distinct lineages that reproduce asexually through the years, skipping the sexual phase. We conducted a comprehensive population genetic analysis, utilizing 21 microsatellite markers and data from over 2000 individuals gathered over an extended period of time from various locations in France. 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 (F_IS). This indirect evidence for asexual reproduction was confirmed by the direct observation of these asexual lineages being repeatedly sampled over the years, confirming the findings of variations inM. larici-populinalife cycle with lineages that bypass the mandatory sexual phase. While sexual lineages are predominant throughout France, asexual lineages are more prevalent in the south of the country, due to possible environmental or ecological factors that allow the overwintering of asexual forms. The discovery of variations in the life cycle in this species offers insights into the evolution from sexual to asexual reproduction encountered in many pathogen species. It could serve as a model organism for studying the transition from sexual to asexual reproductive mode.