Becheler, R. | bioRxiv Science

bioRxiv2025

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

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.

evolutionary biology↗

bioRxiv2024

Reproductive modes of polyploid Ludwigia grandiflora subsp. hexapetala in western Europe: the effects of a late-acting self-incompatibility system and its absence on genetic diversity within populations

Reproductive mode, i.e., the proportion of individuals produced by clonality, selfing and outcrossing in populations, determines how hereditary material is transmitted through generations. It shapes genetic diversity and its structure over time and space, which can be used to infer reproductive modes. Ludwigia grandiflora subsp. hexapetala (Lgh) is a partially clonal, polyploid, hermaphroditic, and heteromorphic plant that recently colonized multiple countries worldwide. In western Europe, individuals are either self-incompatible caused by a late-acting self-incompatibility (LSI) system developing long-styled flowers, or self-compatible (SC), with short-styled flowers. In this study, we genotyped 53 long- and short-styled populations newly colonizing France and northern Spain using SNPs to estimate rates of clonality, selfing and outcrossing. We found that populations reproduced mainly clonally but with a high diversity of genotypes along with rates of sexuality ranging from 10% up to 40%. We also found evidence for local admixture between long- and short-styled populations in a background of genetic structure between floral morphs that was twice the level found within morphs. Long- and short-styled populations showed similar rates of clonality but short-styled populations presented significantly higher rates of selfing, as expected considering their breeding system, and despite the small rates of failure of the LSI system. Within the 53 studied populations, the 13 short-styled populations had fewer effective alleles, lower observed heterozygosity, and higher inbreeding coefficients, linkage disequilibrium and estimates of selfing than what was found in long-styled populations. These results emphasize the necessity to consider the variation of reproductive modes when managing invasive plant species. The overall maintenance of higher genetic diversity with the possibility of maintaining populations clonally in the absence of compatible partners may explain why long-styled individuals seem to be more prevalent in all newly expanding populations worldwide. Beyond Lgh, our methodological approach may inspire future studies to assess the reproductive modes in other autopolyploid populations.

evolutionary biology↗