Abstract
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 the Linum marginale-Melampsora lini plant-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.
Highlights
Evolution within pathogen populations poses ongoing risks for human health, agricultural productivity, and ecosystem structure and function
We investigated whether population differentiation by host ecotype is stable over time in genetic and phenotypic variation for 629 M. lini isolates collected between 1987 and 2010 from three populations (Table 1)
We found that genetic variation was maintained through time via among-population differentiation, and that pathogen populations are genetically and phenotypically dynamic
Summary
Evolution within pathogen populations poses ongoing risks for human health, agricultural productivity, and ecosystem structure and function. While there has been extensive theoretical work [2, 5,6,7] investigating pathogen evolution over time, most empirical studies have only assessed pathogen populations over a single growing season [8, 9], or more rarely a few growing seasons [10,11,12,13], and often attempt to infer evolutionary dynamics via spatial variation in genetic structure [14, 15] or patterns of local adaptation [16]. The forces that drive population dynamics within vs among epidemics may diverge due to temporal fluctuations in environment, different selection processes between years [17], at different phases of epidemics [11] and during off-season survival [18]
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