Co-infections by multiple pathogen strains are common in the wild. Theory predicts co-infections to have major consequences for both within- and between-host disease dynamics, but data are currently scarce. Here, using common garden populations of Plantago lanceolata infected by two strains of the pathogen Podosphaera plantaginis, either singly or under co-infection, we find the highest disease prevalence in co-infected treatments both at the host genotype and population levels. A spore-trapping experiment demonstrates that co-infected hosts shed more transmission propagules than singly infected hosts, thereby explaining the observed change in epidemiological dynamics. Our experimental findings are confirmed in natural pathogen populations—more devastating epidemics were measured in populations with higher levels of co-infection. Jointly, our results confirm the predictions made by theoretical and experimental studies for the potential of co-infection to alter disease dynamics across a large host–pathogen metapopulation.

Although they represent powerful genetic markers in many fields of biology, microsatellites have been isolated in few fungal species. The aim of this study was to assess whether obtaining microsatellite markers with an acceptable level of polymorphism is generally harder from fungi than in other organisms. We therefore surveyed the number, nature and polymorphism level of published microsatellite markers in fungi from the literature and from our own data on seventeen fungal microsatellite-enriched libraries, and in five other phylogroups (angiosperms, insects, fishes, birds and mammals). Fungal microsatellites indeed appeared both harder to isolate and to exhibit lower polymorphism than in other organisms. This appeared to be due, at least in part, to genomic specificities, such as scarcity and shortness of fungal microsatellite loci. A correlation was observed between mean repeat number and mean allele number in the published fungal microsatellite loci. The cross-species transferability of fungal microsatellites also appeared lower than in other phylogroups. However, microsatellites have been useful in some fungal species. Thus, the considerable advantages of these markers make their development worthwhile, and this study provides some guidelines for their isolation.

Clonal expansion has been observed in several invasive fungal plant pathogens colonizing new areas, raising the question of the origin of clonal lineages. Using microsatellite markers, we retraced the evolutionary history of introduction of the chestnut blight fungus, Cryphonectria parasitica, in North America and western Europe. Combining discriminant analysis of principal components and approximate Bayesian computation analysis, we showed that several introduction events from genetically differentiated source populations have occurred in both invaded areas. In addition, a low signal of genetic recombination among different source populations was suggested in North America. Finally, two genetic lineages were present in both invaded areas as well as in the native areas, suggesting the existence of genetic lineages with a high capacity to establish in diverse environments and host species. This study confirmed the importance of multiple introductions, but questioned the role of genetic admixture in the success of introduction of a fungal plant pathogen.

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Wild and cultivated plants represent very different habitats for pathogens, especially when cultivated plants bear qualitative resistance genes. Here, we investigated to what extent the population genetic structure of a plant pathogenic fungus collected on its wild host can be impacted by the deployment of resistant cultivars. We studied one of the main poplar diseases, poplar rust, caused by the fungus Melampsora larici-populina. A thousand and fifty individuals sampled from several locations in France were phenotyped for their virulence profile (ability to infect or not the most deployed resistant cultivar 'Beaupré'), and a subset of these was genotyped using 25 microsatellite markers. Bayesian assignment tests on genetic data clustered the 476 genotyped individuals into three genetic groups. Group 1 gathered most virulent individuals and displayed evidence for selection and drastic demographic changes resulting from breakdown of the poplar cultivar 'Beaupré'. Group 2 comprised individuals corresponding to ancestral populations of M. larici-populina naturally occurring in the native range. Group 3 displayed the hallmarks of strict asexual reproduction, which has never previously been demonstrated in this species. We discuss how poplar cultivation has influenced the spatial and genetic structure of this plant pathogenic fungus, and has led to the spread of virulence alleles (gene swamping) in M. larici-populina populations evolving on the wild host.

Trade-offs in life-history traits are a central tenet in evolutionary biology, yet their ubiquity and relevance to realized fitness of populations remains questioned. Trade-offs in pathogens are of particular interest because they may constrain the evolution and epidemiology of diseases. Here, studies that have measured life-history trade-offs in pathogens (fungi, oomycetes and viruses) of agricultural crops, as well as pathogens attacking wild host plants, are reviewed. The majority of studies report a penalty associated with high virulence as is evidenced by lower performance during subsequent life-history stages. However, costs are not pervasive, and the strength and even shape of life-history correlations can vary according to host genotype, and abiotic environment. Importantly, life-history trade-offs are shown to have profound epidemiological implications ranging from lower disease prevalence of strains harbouring unnecessary virulence, to increased extinction risk at the metapopulation level. From an evolutionary perspective, costs of virulence are shown to constrain the range of R genes, and hence host genotypes, a given strain can adapt to. Moreover, costs of virulence play an important role in limiting the host range of pathogens. Hence, analysis of pathogen life history plays a key role in identifying means of battling disease, from breeding durable resistance to epidemiological intervention strategies.

BACKGROUND: Complex III inhibitors are key compounds in the control of Plasmopara viticola. They are prone to the development of resistance, as demonstrated by the emergence of resistance to quinone-outside inhibitors. By using a combination of bioassays and molecular methods, we monitored sensitivity to amisulbrom and ametoctradin in P. viticola populations in French vineyards from 2012 to 2017. RESULTS:We found that the alternative oxidase (AOX)-related resistance mechanism was common in French P. viticola populations. Target-site resistance to ametoctradin was first detected in 2015 and is likely caused by a single point mutation in the cytochrome b gene, leading to the S34L substitution. The role of this substitution in resistance to ametoctradin was corroborated by another study using an experimental model. A molecular biology method has been developed to detect the mutant allele. To date, the frequency of this mutation is low in French P. viticola populations and it is often co-detected with the wild-type allele. CONCLUSION: Populations of P. viticola displaying evidence of AOX-related resistance were detected for every surveyed year, and their occurrence in French vineyards seems to be increasing over time. This resistance mechanism is currently threatening the efficacy of complex III inhibitors in the field. The low frequency of the S34L allele conferring resistance to ametoctradin, and the instability of resistant phenotypes in some populations, suggest that a fitness cost may be associated with the mutation.

The advent of molecular epidemiology has greatly improved our ability to identify the population sources and track the pathogen movement. Yet the wide spatial and temporal scales usually considered are useful only to infer historical migration pathways. In this study, Bayesian genetic assignments and a landscape epidemiology approach were combined to unravel genetic origin and annual spread during a single epidemic of a plant pathogen: the poplar rust fungus Melampsora larici-populina. The study focused on a particular area-the Durance River valley-which enabled inoculum sources to be identified and channelled spread of the epidemic along a one-dimensional corridor. Spatio-temporal monitoring of disease showed that the epidemic began in the upstream part of the valley and spread out downstream. Using genetic assignment tests, individuals collected at the end of the epidemic were sorted into two genetic groups; very few hybrids were detected, although individuals from both groups coexisted locally downstream in the valley. The epidemic originated from two genetically distinct inoculum sources. Individuals of each group then dispersed southwards along the Durance River and became mixed in poplar riparian stands. These two genetic groups were found previously at a wider spatial scale and proved to result from distinct evolutionary histories on either wild or cultivated poplars. This study showed that the two groups can mix during an epidemic but do not hybridize because they then reproduce asexually. In general, the methods employed here could be useful for elucidating the genetic origin and retracing the colonization history and migration pathways of recent epidemics.