Résumé
A priority for research on infectious disease is to understand how epidemiological and evolutionary processes interact to influence pathogen population dynamics and disease outcomes. However, little is understood about how population adaptation changes across time, how sexual vs. asexual reproduction contribute to the spread of pathogens in wild populations and how diversity measured with neutral and selectively important markers correlates across years. Here, we report results from a long-term study of epidemiological and genetic dynamics within several natural populations of theLinum marginale-Melampsora liniplant-pathogen interaction. Using pathogen isolates collected from three populations of wild flax (L.marginale) spanning 16 annual epidemics, we probe links between pathogen population dynamics, phenotypic variation for infectivity and genomic polymorphism. Pathogen genotyping was performed using 1567 genome-wide SNP loci and sequence data from two infectivity loci (AvrP123,AvrP4). Pathogen isolates were phenotyped for infectivity using a differential set. Patterns of epidemic development were assessed by conducting surveys of infection prevalence in one population (Kiandra) annually. Bayesian clustering analyses revealed host population and ecotype as key predictors of pathogen genetic structure. Despite strong fluctuations in pathogen population size and severe annual bottlenecks, analysis of molecular variance revealed that pathogen population differentiation was relatively stable over time. Annually, varying levels of clonal spread (0-44.8%) contributed to epidemics. However, within populations, temporal genetic composition was dynamic with rapid turnover of pathogen genotypes, despite the dominance of only four infectivity phenotypes across the entire study period. Furthermore, in the presence of strong fluctuations in population size and migration, spatial selection may maintain pathogen populations that, despite being phenotypically stable, are genetically highly dynamic.
Author summary Melampsora liniis a rust fungus that infects native flax,Linum marginalein south-eastern Australia where its epidemiology and evolution have been intensively studied since 1987. Over that time, substantial diversity in the pathotypic structure ofM.linihas been demonstrated but an understanding of how genetic diversity in pathogen populations is maintained through space and time is lacking. Here we integrated phenotypic, genotypic and epidemiological datasets spanning 16 annual epidemics across three host populations to examine long-term pathogen genetic dynamics. The results show that host ecotype is the dominant selective force in the face of strong bottlenecks and annual patterns of genetic turnover. Results from previous studies indicate that in this geographic region,M.linilacks the capacity to reproduce sexually-we thus expected to find limited genetic diversity and evidence for strong clonality influencing genetic dynamics within growing seasons. However, the breadth of genomic coverage provided by the SNP markers revealed high levels of genotypic variation withinM.linipopulations. This discovery contrasts with observed phenotypic dynamics as the epidemics of this pathogen were largely dominated by four pathotypes across the study period. Based on a detailed assessment and comparison of pathotypic and genotypic patterns, our study increases the understanding of how genetic diversity is generated and maintained through space and time within wild pathogen populations. The implications for the management of resistance to pathogens in agricultural or conservation contexts are significant: the appearance of clonality may be hiding high levels of pathogen diversity and recombination. Understanding how this diversity is generated could provide new and unique ways to mitigate or suppress the emergence of infectious strains, allowing to efficiently combat harmful diseases.