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

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.

Keywords: Pool-Seq; adaptation; environmental association; genome resequencing; pooled sequencing; population genomics.

Figure 1

(a) Location of the five sequenced populations of Arabidopsis halleri in Switzerland. (b) Principle component analysis of the five populations using five environmental factors (Table S1, Supporting information). Environmental factor coordinates (arrows) were multiplied by two for clarity. (c) The locations of the studied populations (black dots) in the south-eastern Swiss Alps (Digital Elevation Model DHM25 L2, reproduced by permission of swisstopo [JA100118]).

Figure 2

Results of the ten pairwise F_ST sliding-window analyses in Arabidopsis halleri along a 5 Mb stretch of A. thaliana chromosome 2. The solid line at 0.038 indicates the average differentiation across all SNPs, and the dotted line at 0.47 represents the 99.9% quantile threshold for strongly differentiated sliding windows.

Figure 3

Numbers of associations for the 4282 most strongly differentiated SNPs (black columns) and genes (grey columns) with five environmental factors (Table S1, Supporting information) in Arabidopsis halleri.

Figure 4

Population genomic evidence for adaptation to environmental variation in A. halleri for candidate gene P-GLYCOPROTEIN 1 (AT2G36910). (a) Pairwise F_ST values from highly differentiated sliding windows (lines) and SNPs (open circles). The dashed line at 0.038 indicates the mean F_ST across all SNPs, and the dotted line at 0.47 represents the 99.9% quantile threshold for strongly differentiated sliding windows. (b) Correlation between pairwise population differences in F_ST and solar radiation. r_PMT represents the correlation coefficient of the partial Mantel test. (c) Linear regression between major allele frequencies and solar radiation. Results for the remaining candidate genes are shown in Fig. S1 (Supporting information).