Key message: Increasing human impacts on forests, including unintentional movement of pathogens, climate change, and large-scale intensive plantations, are associated with an unprecedented rate of new diseases. An evolutionary ecology perspective can help address these challenges and provide direction for sustainable forest management.Context: Forest pathology has historically relied on an ecological approach to understand and address the practical management of forest diseases. A widening of this perspective to include evolutionary considerations has been increasingly developed in response to the rising rates of genetic change in both pathogen populations and tree populations due to human activities.Aims: Here, five topics for which the evolutionary perspective is especially relevant are highlighted.Results: The first relates to the evolutionary diversity of fungi and fungal-like organisms, with issues linked to the identification of species and their ecological niches. The second theme deals with the evolutionary processes that allow forest pathogens to adapt to new hosts after introductions or to become more virulent in homogeneous plantations. The third theme presents issues linked to disease resistance in tree breeding programs (e.g., growth-defense trade-offs) and proposes new criteria and methods for more durable resistance. The last two themes are dedicated to the biotic environment of the tree–pathogen system, namely, hyperparasites and tree microbiota, as possible solutions for health management.Conclusion: We conclude by highlighting three major conceptual advances brought by evolutionary biology, i.e., that (i) “not everything is everywhere”, (ii) evolution of pathogen populations can occur on short time scales, and (iii) the tree is a multitrophic community. We further translate these into a framework for immediate policy recommendations and future directions for research.

Alder decline caused by Phytophthora alni has been one of the most important diseases of natural ecosystems in Europe during the last 20 years. The emergence of P. alni subsp. alni —the pathogen responsible for the epidemic—is linked to an interspecific hybridization event between two parental species: P. alni subsp. multiformis and P. alni subsp. uniformis. One of the parental species, P. alni subsp. uniformis, has been isolated in several European countries and, recently, in North America. The objective of this work was to assess the level of genetic diversity, the population genetic structure, and the putative reproduction mode and mating system of P. alni subsp. uniformis. Five new polymorphic microsatellite markers were used to contrast both geographical populations. The study comprised 71 isolates of P. alni subsp. uniformis collected from eight European countries and 10 locations in North America. Our results revealed strong differences between continental populations (Fst = 0.88; Rst = 0.74), with no evidence for gene flow. European isolates showed extremely low genetic diversity compared with the North American collection. Selfing appears to be the predominant mating system in both continental collections. The results suggest that the European P. alni subsp. uniformis population is most likely alien and derives from the introduction of a few individuals, whereas the North American population probably is an indigenous population.

Techniques based on high-throughput sequencing (HTS) of environmental DNA have provided a new way of studying fungal diversity. However, these techniques suffer from a number of methodological biases which may appear at any of the steps involved in a metabarcoding study. Air is one of the most important environments where fungi can be found, because it is the primary medium of dispersal for many species. Looking ahead to future developments, it was decided to test 20 protocols, including different passive spore traps, spore recovery procedures, DNA extraction kits, and barcode loci. HTS was performed with the Illumina MiSeq platform targeting two subloci of the fungal internal transcribed spacer. Multivariate analysis and generalized linear models showed that the type of passive spore trap, the spore recovery procedure, and the barcode all impact the description of fungal communities in terms of richness and diversity when assessed by HTS metabarcoding. In contrast, DNA extraction kits did not significantly impact these results. Although passive traps may be used to describe airborne fungal communities, a study using specific real-time PCR and a mock community showed that these kinds of traps are affected by environmental conditions that may induce losses of biological material, impacting diversity and community composition results.IMPORTANCEThe advent of high-throughput sequencing (HTS) methods, such as those offered by next-generation sequencing (NGS) techniques, has opened a new era in the study of fungal diversity in different environmental substrates. In this study, we show that an assessment of the diversity of airborne fungal communities can reliably be achieved by the use of simple and robust passive spore traps. However, a comparison of sample processing protocols showed that several methodological biases may impact the results of fungal diversity when assessed by metabarcoding. Our data suggest that identifying these biases is of paramount importance to enable a correct identification and relative quantification of community members.