The Natural Evolutionary Potential of Tree Populations to Cope with Newly Introduced Pests and Pathogens—Lessons Learned From Forest Health Catastrophes in Recent Decades

Abstract

Emerging diseases often originate from host shifts of introduced pests or pathogens. Genetic resistance of the host to such diseases might be limited or absent due to the lack of coevolutionary history. We review six examples of major disease outbreaks on native tree species caused by different introduced pests and pathogens that led to large ecological and economical losses. In all six cases, high tree mortality was observed in natural populations with some surviving individuals exhibiting varying levels of genetic resistance. The abundance and distribution of resistant individuals and the heritability of resistance traits varies substantially among the cases. While chestnut blight wilt combined with ink disease has virtually eliminated mature Castanea dentata trees from North America, other severe emerging diseases, such as the ash dieback, have left many surviving trees and genetic variation in resistance to such diseases has been documented. We argue that the evolutionary potential of tree species to respond to new emerging diseases should not be underestimated. However, the risk of increased levels of inbreeding and loss of genetic diversity caused by low population sizes is a major concern. Maintenance of broad genetic diversity is an important issue in conservation and forestry management. We expect that future research targeting the genetic background of biotic resistance towards emerging diseases and the role of endophytic communities in protecting trees will facilitate the informed and science-based guidance required to manage and maintain forests with high resilience. International cooperation on limiting disease spread and the provision of early invasive pest or pathogen detection systems are essential.

The susceptibility of Asian, European and North American Fraxinus species to the ash dieback pathogen Hymenoscyphus fraxineus reflects their phylogenetic history

“…It is still unknown if this is also the case for North American ashes. When facing a potential new pathogen, as broad a genetic base as possible should be deployed in the planted areas to improve the resilience of the plantings (Budde et al 2016).…”

The genetics of exapted resistance to two exotic pathogens in pedunculate oak

“…Moderate clonal repeatability values were obtained in both field and laboratory conditions, as reported in similar studies of disease response in mapping populations of forest trees: 0.54–0.94 for the poplar– Melampsora larici‐populina pathosystem in both controlled and natural conditions (Jorge et al , ), 0.59 for the Eucalyptus globulus – Mycosphaerella cryptica interaction in natural conditions (Freeman et al ., ), and 0.36–0.92 for various strains of Melampsora larici‐epitea on willow hybrids (Samils et al ., ). Heritability estimates were in the range expected for disease resistance in trees (Carson & Carson, ), including those observed in noncoevolved pathosystems (Budde et al ., ). However, heritability values depend on many factors, including the genetic variability of the host population tested, age at assessment, environmental conditions, and screening methods.…”

“…In a context of increasing forest damage due to emerging diseases world‐wide (Liebhold et al , ; Santini et al ., ), improving our understanding of the genetic basis of tree resistance to pathogens is a priority research topic. Genetic variation in susceptibility to pathogens will condition the ability of populations to evolve resistance, either in nature or through breeding programs (Ennos, ; Budde et al ., ). Interestingly, the recent sequencing of the oak ( Quercus robur ) genome suggested that the expansion of disease‐related gene families could be an important genomic feature associated with long lifespan in trees (Plomion et al ., ).…”

Environmentally induced changes in the distribution of disease susceptibility phenotypes inPinus radiata

“…Pitch canker was only recognized in California in 1986 (McCain, Koehler, & Tjosvold, 1987), and it appears to have been an introduction from the south-eastern United States (Wikler & Gordon, 2000), with no evidence that geographic ranges of host and pathogen overlapped prior to that. In the absence of selection pressure for resistance to pitch canker in P. radiata, variation in susceptibility may be attributable to a reservoir of neutral variation (Budde et al, 2016;Petit & Hampe, 2006), which is seen as integral to the capacity of tree species to respond effectively to challenges posed by exotic pathogens.…”

“…The vast extent of forested land, which presently covers approximately 27% of the terrestrial surface of the earth (Petit & Hampe, 2006), suggests that tree populations have the capacity to respond effectively to exotic pathogens. This capacity has been attributed to a deep reservoir of genetic diversity in the form of large populations and extensive gene flow (Budde, Nielsen, Ravn, & Kjaer, 2016).…”