Genomic Signature of Adaptation to Climate in Medicago truncatula

Abstract

Local adaptation and adaptive clines are pervasive in natural plant populations, yet the effects of these types of adaptation on genomic diversity are not well understood. With a data set of 202 accessions of Medicago truncatula genotyped at almost 2 million single nucleotide polymorphisms, we used mixed linear models to identify candidate loci responsible for adaptation to three climatic gradientsannual mean temperature (AMT), precipitation in the wettest month (PWM), and isothermality (ITH)-representing the major axes of climate variation across the species' range. Loci with the strongest association to these climate gradients tagged genome regions with high sequence similarity to genes with functional roles in thermal tolerance, drought tolerance, or resistance to herbivores of pathogens. Genotypes at these candidate loci also predicted the performance of an independent sample of plant accessions grown in climatecontrolled conditions. Compared to a genome-wide sample of randomly drawn reference SNPs, candidates for two climate gradients, AMT and PWM, were significantly enriched for genic regions, and genome segments flanking genic AMT and PWM candidates harbored less nucleotide diversity, elevated differentiation between haplotypes carrying alternate alleles, and an overrepresentation of the most common haplotypes. These patterns of diversity are consistent with a history of soft selective sweeps acting on loci underlying adaptation to climate, but not with a history of long-term balancing selection. L OCAL and clinal adaptation is widespread in natural populations (Clausen et al. 1941;Leimu and Fischer 2008), which, by definition, results from selection that varies across a species' range. Most methods to search for the targets of adaptation are designed to identify gene regions that have experienced "hard" selective sweeps, in which selection acts on new mutations that confer a selective advantage across the entire range of a sample (Maynard Smith and Haigh 1974;Nielsen 2005;Pritchard and Di Rienzo 2010;Kelly et al. 2013). These methods are not designed to identify targets of adaptation to selective environments that vary across the range of sampled populations. The targets of locally variable selection either may be maintained as stable polymorphisms or experience partial, or "soft," sweeps either because local adaptation involves fixation of different alleles in different portions of a species' range or because selection acts on standing variation (Hermisson and Pennings 2005;Pavlidis et al. 2012;Messer and Petrov 2013).Identifying the molecular targets of clinal adaptation offers an opportunity not only to identify functionally important genes, but also to further our understanding of adaptation itself. If the selective environment that drives clinal adaptation is stable, and alleles responsible for adaptation are at stable equilibria, then the loci responsible for adaptation may bear population genetic signatures of balancing selection: elevated differentiation between haplotypes linked to the ...

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