The outcome of host-parasite interactions may depend not only on the genotypes of the species involved but also on environmental factors. We used the fungus Cryphonectria parasitica, the causal agent of chestnut blight, and its hyperparasitic virus, Cryphonectria hypovirus-1 (CHV1), to test for genotype-by-genotype-by-environment interactions in a host-parasite system. In C. parasitica, infection with CHV1 induces a hypovirulent phenotype with reduced virulence toward the chestnut tree (Castanea spp.) and thus controls chestnut blight in many European regions. In contrast, uninfected virulent C. parasitica have nearly eradicated the American chestnut in North America. We applied a full factorial design and assessed the fungal growth and sporulation of four C. parasitica strains, uninfected and infected with each of the four known CHV1 subtypes, at 12°, 18°, 24°, and 30°C. We found a significant (P ≤ .00001) genotype-by-genotype-by-environment interaction, demonstrating the potential for a selection mosaic. As a consequence, different host and parasite genotypes would be selected under different climatic conditions, affecting the coevolutionary dynamics of the host-parasite interaction and the course of chestnut blight epidemics. Genotype-by-genotype-by-environment interactions are essential to take into account when designing biological control strategies.

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We reconstructed the invasion history of the fungal virus Cryphonectria hypovirus 1 (CHV-1) in Europe, which infects the chestnut blight fungus Cryphonectria parasitica. The pattern of virus evolution was inferred based on nucleotide sequence variation from isolates sampled across a wide area in Europe at different points in time. Phylogeny and time estimates suggested that CHV-1 was introduced together with its fungal host to Europe and that it rapidly colonized the central range along the south facing slopes of the Alps and the north-east facing slopes of the Dinaric Alps. These central populations were the source for two waves of simultaneous invasions toward the southern Balkans and Turkey, as indicated by migration rates. Our results showed that the evolutionary scenarios for CHV-1 and C. parasitica were spatially congruent. As infection with CHV-1 reduces the pathogenicity of C. parasitica toward the chestnut tree, CHV-1 invasions of the newly established C. parasitica populations probably prevented the development of devastating chestnut blight epidemics in Europe. We propose that in this, and supposedly in other pathosystems, geographic, vegetation-related, demographic, economic, and political factors may help explain the correlated invasion pattern of a parasite and its host.

Cryphonectria hypovirus 1 hyperparasitizes the chestnut blight fungus Cryphonectria parasitica and acts as a biocontrol agent for this serious tree disease. The virus is transmitted cytoplasmatically between fungal individuals. However, highly virulent viruses strongly debilitate their host and, thus, reduce their own transmission probability. Furthermore, vegetative incompatibility between fungi is an important transmission barrier. Therefore, virulent viruses are expected to be strongly selected against in fungal populations with high levels of vegetative incompatibility, eventually leading to the erosion of biocontrol. To test this prediction, we assessed the virulence of the virus in four European C. parasitica populations with high diversity of vegetative compatibility types and in four populations with low diversity. We expected the degree of virus virulence to be lower in fungal populations with high levels of vegetative incompatibility. However, our results did not reveal such a trend. No significant differences in virus virulence between populations with low versus high diversity of vegetative compatibility types were observed. There was no evidence for an erosion of disease control due to the presence of these transmission barriers. Thus, the findings of this study are promising for the sustainability of Cryphonectria hypovirus 1 as a biocontrol agent for chestnut blight in Europe.

Virulent strains of the chestnut blight fungus Cryphonectria parasitica cause lethal bark cankers on chestnut trees. Infection of C. parasitica with Cryphonectria hypovirus 1 in Europe biologically controls this disease, leading to nonlethal and inactive cankers. Unexpectedly, virus-free C. parasitica strains have been isolated from inactive cankers. In this study, we compared the virulence of virus-infected and virus-free C. parasitica strains isolated from either inactive or active cankers on chestnut seedlings and sprouts. In the seedling experiment, we assessed canker growth and seedling mortality. In the sprout experiment, we also assessed canker growth and made fungal reisolations to determine virus infection and immigration of foreign vegetative compatibility (vc) types over a period of 13 years in a coppice forest. Overall, the virulence of virus-free C. parasitica strains isolated from inactive versus active cankers did not differ. Significant differences were only attributed to virus infection. Virus infection and fungal strain composition in cankers changed over time. Foreign vc types immigrated into cankers and virus-free cankers became virus-infected within a few years. Most of the cankers were callused over time and became inactive. However, we observed that the virus did not always persist in these cankers. This study demonstrates that virus spread occurs effectively in European chestnut forests and that this biocontrol system is highly dynamic.