Skip to main content

Linking Pathogen Evolution and Epidemiology

Final Report Summary - PATHEVOL (Linking Pathogen Evolution and Epidemiology)

The goal of the research in PATHEVOL was to produce a comprehensive understanding of how evolutionary potential of pathogen populations interacts with epidemiological dynamics in natural populations. The empirical work was carried out with the specialist fungal pathogen Podosphaera plantaginis and its host plant Plantago lanceolata. During the project, I addressed the key theories of pathogen evolution, namely: life-history trade-offs, competition for resources under multiple infection, and the costs and benefits of sexual reproduction. This project benefitted from the exceptional research opportunities offered by the focal study species to test theories that have not been validated with respect to realized population dynamics and the persistence of pathogen populations.

The work was built around the unique epidemiological data that have been collected annually on the occurrence of the pathogen in a network of 4000 host populations since 2001. A recently completed de novo transcriptome sequencing offered molecular tools that were further developed during this project.

The first key questions were whether life-history trade-offs maintain variation in pathogen populations, and what are the links to epidemiological dynamics. Here, we made the following key discoveries: life-history trade-offs are expressed on allopatric host plants indicating that adaptation to host use alleviates these trade-offs. These trade-offs are reflected in the epidemiological dynamics of the pathogen; newly established pathogen populations are smaller and more prone to go extinct than older established populations. Furthermore, we discovered that rapid growth in the asexual life-history stage of this pathogen is traded off with low quality of resting spores that are produced sexually. Finally, we discovered that there are different strategies to becoming common, as the most common pathogen strains in this system exhibited contrasting life-history strategies. These results offer promising insight into disease control by means of virulence management.

The second key objective was to assess how dynamics under multiple infection drive virulence evolution. Here we discovered that coinfection was common across this pathosystem with strong spatial structure. Coinfection changed infection dynamics at the individual host and population levels. The mechanism for this is likely to be the increase in transmission which we quantified under controlled experiments. Coinfection dynamics were determined to be strongly mediated by the host, but with little evidence for effective and durable priming. These results highlight the importance of incorporating the probability of coinfection into predictive epidemiological modeling framework, and the limiting ability of priming to provide protection for the host to further pathogen attack.

Coinfection is also the pre-requisite for sexual outcrossing for many pathogens. We discovered the mating type genes form the transcriptome data, but contrary to expectations, found that this pathogen is capable of both haploid selfing and outcrossing. However, outcrossing appears to be common in the natural pathogen metapopulations and provides an immediate ecological benefit: populations with outcrossing have a higher probability of surviving the winter. The quality of resting spores produced in outcrossing were determined to be better than those produced in selfing. This is the first direct demonstrations of an ecological benefit of sex in a pathogen, a dilemma at the heart of disease biology.

Finally, our epidemiological analyses demonstrated overwintering to be the bottleneck for this pathosystem, with typically half of the local pathogen populations going extinct every winter. We discovered that this is highly sensitive to abiotic winter conditions, and with changing climate epidemiological dynamics are becoming more synchronized. Hence, climate change may alter epidemiological dynamics far beyond than what has been considered when only accounting for conditions during the growing season.