Rapid polygenic adaptation in a wild population of ash trees under a novel fungal epidemic

Abstract

Large changes in quantitative traits through small shifts in allele frequencies at many genetic loci driven by natural selection lie at the heart of the neo-Darwinian synthesis [1,2] but are hard to fully demonstrate in the wild [3-6]. The spread of a natural pathogen into a new host population containing standing genetic variation for quantitative resistance provides an opportunity to demonstrate such shifts occurring in real time [7-10]. The invasive fungal pathogen (Hymenoscyphus fraxineus) causes ash dieback disease in European ash (Fraxinus excelsior) populations. The disease is frequently lethal [11,12], but larger trees persist longer [11,13], often with reduced reproductive output [13]. Here, using whole genome resequencing of an infected natural ash tree population in England, we measure allele frequencies at 7985 single nucleotide polymorphisms (SNPs) previously associated with resistance to the pathogen [14]. The average genetic merit for resistance of trees established after the start of the epidemic, calculated as Genomic Estimated Breeding Values (GEBV) from the 7985 loci, was higher than that of related adults from the pre-epidemic generation. We estimate that, to produce a GEBV shift of this magnitude, would require truncation selection eliminating at least 13% of the juvenile population. Even this rapid rate of change under natural selection may be insufficient for evolutionary rescue [15] of European ash populations, but change could be accelerated by a breeding programme informed by genomic selection. To this end, we show that for predicting the health of their offspring, the GEBVs of parent trees perform better than a phenotypic assessment of the ash dieback damage parent trees have suffered.

Discarded sequencing reads uncover natural variation in pest resistance inThlaspi arvense

“…With the decreasing cost of sequencing and increasing large-scale and single-species sequencing projects e.g. (37)(38)(39)(40)(41)(42)(43), the number of datasets suitable for such analyses is set to rapidly increase in the near future.…”

“…The goals of our study were thus two-fold: i) to contribute to a mechanistic understanding of pest resistance in Thlaspi arvense, and, more generally, ii) to explore whether non-target reads from plant sequencing can be used as proxies for studying plant biotic interactions. Considering that we are moving towards an increasingly sequencing-prone world, where more and larger datasets are being generated for many species (37)(38)(39)(40)(41)(42)(43), the use of non-target reads will likely have very broad potential.…”

Ash dieback: From Asia to Europe

“…The genetic basis for H. fraxineus resistance was subsequently published in 2019 (Stocks et al, 2019). Based on these findings, markers for breeding of resistance are now available and there is evidence that natural selection for resistance is already occurring (Metheringham et al, 2022;Plumb et al, 2020).…”

The challenge of demonstrating contemporary natural selection on polygenic quantitative traits in the wild

“…The success of Ashraf et al (2022) is that they can predict these small genetic effects with some accuracy. (for an example in trees see Metheringham et al, 2022). Perhaps one day this will extend to the genomic basis of speed in wolves and cheetahs.…”

“…While this slightly baffling situation is unlikely to replace easier‐to‐understand hypothetical examples of natural selection on wild animal quantitative traits in the popular literature, it represents a significant advance for the field. By pioneering genomic prediction methods in the exceptionally well‐studied Soay sheep population, this work opens up the way for more widespread searches for natural selection acting upon quantitative traits in other wild populations (for an example in trees see Metheringham et al, 2022 ). Perhaps one day this will extend to the genomic basis of speed in wolves and cheetahs.…”