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

Evolutionary responses to sudden changes in the environment can, in theory, be rapid if they involve small shifts in allele frequencies at many loci. Such adaptation has proven hard to characterise in wild populations. We overcome these problems, in quantifying the genetic response of European ash trees ( Fraxinus excelsior ) to the strong selective challenge imposed by the invasive alien fungal pathogen Hymenoscyphus fraxineus , by exploiting a previous study that had estimated effect sizes for many single nucleotide polymorphism (SNP) loci associated with resistance to the fungus in large field trials. We ask if the selective response, in a new natural setting of a multigenerational wild ash woodland, involves allele frequency changes at the 10,000 loci which provided the best genomic prediction of resistance in the field trials. We conducted whole genome resequencing of each tree and calculated its genetic merit as a Genomic Estimated Breeding Value (GEBV), using the previous estimates of SNP effect sizes. The GEBV of trees established after the start of the epidemic were significantly higher than those of related adults from the pre-epidemic generation, with the size of the change in the alleles’ frequency corresponding to their effect sizes. To produce a GEBV shift of this magnitude, would require truncation selection eliminating at least 13% of the juvenile population. Thus, we document shifts in allele frequency at very many loci producing a heritable micro-evolutionary adaptive change over a single generation. Adaptation could be further accelerated by a breeding programme informed by genomic selection. Significance statement We demonstrate contemporary natural selection as European ash trees are exposed to the novel fungal epidemic of Hymenoscyphus fraxineus . We detect adaptive shifts in allele frequencies at thousands of loci. This mode of rapid evolution in a highly polygenic trait has been theorised since R. A. Fisher first proposed it, but has been hard to demonstrate in the wild. The approach we have applied could be widely used, where genomic prediction is possible in natural populations and there is a clear change in selective regime. The results for European ash trees indicate a degree of natural evolutionary rescue, after the fungus arrives. An effective practical application would be to accelerate this response by human-directed genomic selection. ### Competing Interest Statement The authors have declared no competing interest.