Local climate adaptation in a widespread fungal tree pathogen

Background/Question/Methods

Fungi are key components of forest and agricultural systems with direct influence on plant health and productivity and ecosystem carbon and nutrient cycling. Rapid evolutionary change has the potential to structure species responses to changing climate, yet the potential for fungi to adapt to novel climate regimes is largely unknown. Here we examine climate adaptation in a widespread pathogenic fungus (Neonectria faginata) that infects American beech trees (Fagus grandifolia) as part of the beech bark disease (BBD) complex. Importantly, forest stands with older BBD infections occur in colder climates (northeastern USA) with consistent spatiotemporal spread of the disease to the south and west over the last 130 years, setting up a potential natural experiment in local climate adaptation. We performed genome resequencing of 59 isolates across seven sites (sequencing of an additional 63 isolates from six additional sites is underway), calculated population differentiation metrics, and performed genome scans to ask: 1) whether N. faginata displays trends in isolation by distance or population structure consistent with spatiotemporal spread of BBD indicating recent dispersal to warmer climate regimes; and 2) whether there are signals of local climate adaptation in the genome of N. faginata, and if so, which genes are under selection?

Results/Conclusions

An initial sequencing experiment included fungal single-spore isolates from sites ranging from the northeastern US (Maine), the Great Lakes region (Michigan), and southeastern US (North Carolina) representing a broad climatic sample of the range of American beech. We did not detect strong evidence for genetically differentiated populations of N. faginata (i.e., population structure; STRUCTURE and ADMIXTURE algorithms). Instead, there was evidence for genetic isolation by distance (Mantel r = 0.54, P = 0.007). Furthermore, patterns of genetic diversity indicated greater genetic differentiation (negative Tajima’s D) in sites with older BBD infection and population contraction or founder effects (positive Tajima’s D) in sites with younger infections (infection duration versus Tajima’s D, R2 = 0.64, P = 0.03). Genome scans and latent factor mixed modeling identified several genomic regions with elevated levels of diversification correlated with climate (growing degree days and annual precipitation). Patterns of isolation by distance and decreased genetic diversity in sites with younger BBD infections support spatiotemporal dispersal of N. faginata in conjunction with spread of BBD as opposed to a broader historic range. Together with the identification of putative genomic markers for climate adaptation, these results indicate that N. faginata has undergone rapid local adaptation to warmer climates.