Combining population genomics and fitness QTLs to identify the genetics of local adaptation in <i>Arabidopsis thaliana</i>

Abstract

Evidence for adaptation to different climates in the model species <i>Arabidopsis thaliana</i> is seen in reciprocal transplant experiments, but the genetic basis of this adaptation remains poorly understood. Field-based quantitative trait locus (QTL) studies provide direct but low-resolution evidence for the genetic basis of local adaptation. Using high-resolution population genomic approaches, we examine local adaptation along previously identified genetic trade-off (GT) and conditionally neutral (CN) QTLs for fitness between locally adapted Italian and Swedish <i>A. thaliana</i> populations [Ågren J, et al. (2013) <i>Proc Natl Acad Sci USA</i> 110:21077-21082]. We find that genomic regions enriched in high <i>F</i>_<i>ST</i> SNPs colocalize with GT QTL peaks. Many of these high <i>F</i>_<i>ST</i> regions also colocalize with regions enriched for SNPs significantly correlated to climate in Eurasia and evidence of recent selective sweeps in Sweden. Examining unfolded site frequency spectra across genes containing high <i>F</i>_<i>ST</i> SNPs suggests GTs may be due to more recent adaptation in Sweden than Italy. Finally, we collapse a list of thousands of genes spanning GT QTLs to 42 genes that likely underlie the observed GTs and explore potential biological processes driving these trade-offs, from protein phosphorylation, to seed dormancy and longevity. Our analyses link population genomic analyses and field-based QTL studies of local adaptation, and emphasize that GTs play an important role in the process of local adaptation.