Adaptive Introgression Facilitates Adaptation to High Latitudes in European Aspen (Populus tremula L.).

Martha Rendón-Anaya,Sæmundur Sveinsson,Dainis Ruņǵis,Pär K Ingvarsson,Jonathan Wilson,Aleksey Fedorkov,Kathryn M Robinson,Mark E S Bailey,Nathaniel R Street,Joan Cottrell,Christian Lexer,Stefan Jansson,Victoria Sork

doi:10.1093/molbev/msab229

Abstract

Understanding local adaptation has become a key research area given the ongoing climate challenge and the concomitant requirement to conserve genetic resources. Perennial plants, such as forest trees, are good models to study local adaptation given their wide geographic distribution, largely outcrossing mating systems, and demographic histories. We evaluated signatures of local adaptation in European aspen (Populus tremula) across Europe by means of whole-genome resequencing of a collection of 411 individual trees. We dissected admixture patterns between aspen lineages and observed a strong genomic mosaicism in Scandinavian trees, evidencing different colonization trajectories into the peninsula from Russia, Central and Western Europe. As a consequence of the secondary contacts between populations after the last glacial maximum, we detected an adaptive introgression event in a genome region of ∼500 kb in chromosome 10, harboring a large-effect locus that has previously been shown to contribute to adaptation to the short growing seasons characteristic of Northern Scandinavia. Demographic simulations and ancestry inference suggest an Eastern origin—probably Russian—of the adaptive Nordic allele which nowadays is present in a homozygous state at the north of Scandinavia. The strength of introgression and positive selection signatures in this region is a unique feature in the genome. Furthermore, we detected signals of balancing selection, shared across regional populations, that highlight the importance of standing variation as a primary source of alleles that facilitate local adaptation. Our results, therefore, emphasize the importance of migration–selection balance underlying the genetic architecture of key adaptive quantitative traits.

Highlights

Local adaptation, the means by which populations of a species genetically adjust to local environments, is a powerful process of evolution
Population Structure and Admixture In order to elucidate demographic and adaptive events that have accompanied the postglacial radiation of European aspen, we resequenced a large collection of individuals, covering a wide geographic range across the Eurasian continent
Sequencing reads for all individuals were mapped against the reference P. tremula v2.0 genome (Schiffthaler et al 2019) and obtained $20.8e6 single-nucleotide polymorphisms (SNPs) after several filtering steps

Summary

Introduction

The means by which populations of a species genetically adjust to local environments, is a powerful process of evolution. It occurs because multiple environmental factors imposing different selective pressures exist and the strength of each factor varies across habitats. Two fundamental genetic sources for local adaptation, in temperate forest trees that have large effective population size and low nucleotide substitution rates per unit of time, are standing variation and intra-/interspecies hybridization. Species capable of hybridization will have access to a larger pool of genetic variation that provides the raw material for selection and accelerated adaptation. At the same time, standing variation can be maintained through balancing selection (BS) within populations.

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