Pathogen Population Biology Research can Reduce International Threats to Tree Health Posed by Invasive Fungi

Humankind owes much to trees, given their major role in sequestering carbon and providing oxygen, sugars and much of the energy on which ourselves and terrestrial ecosystems depend. Trees and forests are important culturally, economically, environmentally and socially. And yet, despite this, trees throughout the world are currently facing an increasing number of serious challenges. On a global scale, Curtis et al. (2018) report most forest loss is due to commodity driven deforestation through permanent conversion to nonforest land uses including agriculture (e.g. palm oil production), energy production and mining. The other main drivers of global forest loss, that might instead be considered less permanent and associated with subsequent regrowth, include forestry, shifting agriculture and wildfire. Additional threats to forests include those posed by climate change, and invasive biotic agents such as insect pests and pathogens. Most new tree disease outbreaks are due to introduction events, with a potential pathogen introduced from their endemic centres of origin (where they generally cause little or no disease on their plant host due to long-term coevolution) into a new geographic location, in which a naive host has not previously been exposed and can thus be highly susceptible. The incidence of such 'new encounter' diseases is increasing at an unprecedented rate due to globalisation with increased international trade in plants and travel, a scenario potentially exacerbated by a changing climate better suited to establishment of a pathogen once introduced. Identification of the centres of origin of fungal pathogens can be important for several reasons. First, given that the original host-fungus interaction will have typically stabilised over long periods of time, such geographic regions could be useful sources of host genetic resistance. Moreover, the longer time periods involved will have likely resulted in greater genetic diversity accruing in such endemic populations. More diverse pathogen populations have greater evolutionary potential, with increased genetic variation available for response to environmental change. This could enable host tolerance to be overcome, unexpected 'jumps' onto new hosts, increased risk of fungicide resistance, and better adaptability to changing environmental conditions (e.g. temperature). Thus, strategies to reduce introduction of additional genetic variation from source to sink regions can reduce tree health threats. In this article, such introduction events are considered in the context of three devastating tree diseases, namely ash dieback, Dutch Elm Disease (DED) and Dothistroma Needle Blight (DNB, mainly on pine). On all these tree hosts, multiple closely-related fungal species have now been associated with each of these different diseases. Such related species are often morphologically very similar or even indistinguishable by eye, and consequently this can result in taxonomic confusion and species misidentification, leading to delayed diagnosis of the true causal agent of a given disease outbreak. Research into such related species is important as they might pose very different plant health threats that require distinct disease management strategies. These differences might relate to pathogenicity, geographic distribution, host range, effectiveness of host resistance, sensitivity to fungicides, temperature optima, reproductive strategy and so on. Furthermore, when related fungal species come into physical contact with each other after a long period of separation, for instance via an introduction event, various outcomes are possible including: (1) replacement (and possible extinction) of one species by the other; (2) coexistence of the species; or (3) cross-species hybridisation. The remainder of this article focuses, using three major tree disease case histories, on how fundamental research on pathogen biology can provide new insights into the genetic structure of related pathogen populations that can be usefully applied to reduce the threat to tree health posed by invasive fungal species.