Population genomic footprints of selection and associations with climate in natural populations of Arabidopsis halleri from the Alps.

Martin C Fischer,Kentaro K Shimizu,Rolf Holderegger,Andrew Tedder,Stefan Zoller,Alex Widmer,Felix Gugerli,Christian Rellstab

doi:10.1111/mec.12521

Abstract

Natural genetic variation is essential for the adaptation of organisms to their local environment and to changing environmental conditions. Here, we examine genomewide patterns of nucleotide variation in natural populations of the outcrossing herb Arabidopsis halleri and associations with climatic variation among populations in the Alps. Using a pooled population sequencing (Pool-Seq) approach, we discovered more than two million SNPs in five natural populations and identified highly differentiated genomic regions and SNPs using FST-based analyses. We tested only the most strongly differentiated SNPs for associations with a nonredundant set of environmental factors using partial Mantel tests to identify topo-climatic factors that may underlie the observed footprints of selection. Possible functions of genes showing signatures of selection were identified by Gene Ontology analysis. We found 175 genes to be highly associated with one or more of the five tested topo-climatic factors. Of these, 23.4% had unknown functions. Genetic variation in four candidate genes was strongly associated with site water balance and solar radiation, and functional annotations were congruent with these environmental factors. Our results provide a genomewide perspective on the distribution of adaptive genetic variation in natural plant populations from a highly diverse and heterogeneous alpine environment.

Highlights

Studies of genes and genomic regions underlying adaptation are at the heart of ecological genomics (Bergelson & Roux 2010; Ekblom & Galindo 2011), a dynamic research area that aims at understanding the genomic changes associated with the responses of organisms to their biotic and abiotic environment (Ungerer et al 2008)
In addition to counting the number of associations between environmental factors and individual single nucleotide polymorphisms (SNPs), we assessed the numbers of associations with particular genes, that is, those that could be annotated to the A. thaliana genome and for which we found at least one SNP being associated with a particular environmental factor
In a stepwise approach that included the identification of highly differentiated SNPs and genomic regions, environmental associations and Gene Ontology (GO) term analyses, we identified a set of candidate genes associated with climatic variation

Summary

Introduction

Studies of genes and genomic regions underlying adaptation are at the heart of ecological genomics (Bergelson & Roux 2010; Ekblom & Galindo 2011), a dynamic research area that aims at understanding the genomic changes associated with the responses of organisms to their biotic and abiotic environment (Ungerer et al 2008). Arabidopsis halleri grows in a wide range of habitats, typically at 600 m above sea level (asl) and higher, including mountain slopes at more than 2300 m asl, grassy meadows, forest margins and rocky crevices (Al-Shehbaz & O’Kane 2002) on soils with acidic, neutral and oligotrophic properties, and on soils with high natural or anthropogenic heavy metal content (Clauss & Koch 2006). It is a perennial, outcrossing and insect-pollinated herb that is distributed throughout Europe and eastern Asia. The ability of A. halleri to grow in a wide diversity of habitats and our increasing understanding of its biology make it an ideal study object for analyses of adaptation to different edaphic and climatic conditions

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