Genetic mapping of adaptation reveals fitness tradeoffs in Arabidopsis thaliana

Significance Adaptation to local environmental conditions is common, but the genetic mechanisms of adaptation are poorly known. We produced recombinant inbred lines (RILs) of the model plant Arabidopsis thaliana by crossing populations that inhabit drastically different climates in Sweden and Italy, grew the RILs at the parental sites for 3 y, and genetically mapped quantitative trait loci (QTL) for fitness. The results demonstrate that surprisingly few QTL explain much of the adaptive divergence between the two plant populations. Moreover, we find strong evidence for tradeoffs (i.e., adaptation to one environment reduces performance elsewhere). The results shed light on processes governing the evolution of biological diversity and the potential for adaptive evolution in response to environmental change. Organisms inhabiting different environments are often locally adapted, and yet despite a considerable body of theory, the genetic basis of local adaptation is poorly understood. Unanswered questions include the number and effect sizes of adaptive loci, whether locally favored loci reduce fitness elsewhere (i.e., fitness tradeoffs), and whether a lack of genetic variation limits adaptation. To address these questions, we mapped quantitative trait loci (QTL) for total fitness in 398 recombinant inbred lines derived from a cross between locally adapted populations of the highly selfing plant Arabidopsis thaliana from Sweden and Italy and grown for 3 consecutive years at the parental sites (>40,000 plants monitored). We show that local adaptation is controlled by relatively few genomic regions of small to modest effect. A third of the 15 fitness QTL we detected showed evidence of tradeoffs, which contrasts with the minimal evidence for fitness tradeoffs found in previous studies. This difference may reflect the power of our multiyear study to distinguish conditionally neutral QTL from those that reflect fitness tradeoffs. In Sweden, but not in Italy, the local genotype underlying fitness QTL was often maladaptive, suggesting that adaptation there is constrained by a lack of adaptive genetic variation, attributable perhaps to genetic bottlenecks during postglacial colonization of Scandinavia or to recent changes in selection regime caused by climate change. Our results suggest that adaptation to markedly different environments can be achieved through changes in relatively few genomic regions, that fitness tradeoffs are common, and that lack of genetic variation can limit adaptation.