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

Abstract

Deciphering how asexual lineages emerge and persist within otherwise sexual populations is central for understanding the evolution of reproductive modes. In addition to contributing to the long-standing debate about the respective advantages of sexual vs. asexual reproduction, cases of coexistence of both forms also raise ecological questions regarding differences in life-history strategies. Here, we focus on the poplar rust fungus Melampsora larici-populina, a plant pathogen species with a complex life cycle and a previously documented case of coexistence of sexual and asexual lineages. We conduct a population genetic study on more than 2,000 individuals sampled over a 30-year period across France to further monitor the persistence of asexual lineages and determine if they form a monophyletic group. Clustering analysis identifies a group of multilocus lineages showing the genetic hallmarks of clonality, including a strongly negative FIS value with high variance among loci. This indirect evidence is supported by the repeated resampling of asexual lineages that persist clonally across years. Notably, there is substantial variability within the asexual group, with several genetically distinct multilocus lineages, some of which are entangled with sexual lineages in the phylogenetic tree. The asexual lineages exhibit varying levels of abundance and persistence. One lineage predominates: it has persisted for over 30 years and is more widespread. Asexual lineages co-occur locally with their sexual counterparts, but their prevalence increases southward in France, which is consistent with milder winters being more favourable for asexual overwintering. Together, these results reveal a dynamic and ecologically structured process of repeated switches toward asexual survival with some events of long-lasting persistence. We discuss the consequences of these multiple transitions to asexuality, both in terms of evolutionary ecology and for the management of plant pathogen populations.