Genetic mapping of adaptation reveals fitness tradeoffs in Arabidopsis thaliana

Abstract

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.

Keywords: QTL mapping; RIL population; divergent selection; genetic drift; inbreeding.

Fig. 1.

Distribution of RIL means for fitness (mean number of fruits per seedling planted) in field experiments established in Italy (A, C, and E) and Sweden (B, D, and F) in 2009, 2010, and 2011. Means for parental lines and associated 95% confidence intervals are indicated.

Fig. 2.

Fitness QTL detected in field experiments in Italy and Sweden in 2009, 2010, and 2011. Arrows indicate QTL position and the effect of the Swedish genotype (upward, fitness increased; downward, fitness decreased). The vertical line gives the 95% Bayesian credible interval. Of the 15 distinct QTL identified, 11 were detected in more than one site × year combination [indicated with light gray (QTL observed at just one site) and dark gray boxes (QTL shared across sites)]. Boxes specify the range of point estimates for distinct QTL detected more than once. The six fitness tradeoff QTL, where the local genotype was favored at each site, are underlined. LOD profiles are given in Fig. S2A.

Fig. 3.

Least-square mean number of fruits (±2 SE) of the Italian (closed symbol) and Swedish genotype (open symbol) at the six distinct fitness QTL (A–E) for which mapping results indicated a tradeoff between the Italian and Swedish sites across the 2009, 2010, and 2011 experiments. Least-square means were derived from an ANOVA including genotype at each of the 15 distinct QTL, site, year, and interactions as independent variables (Table S4). The five fitness QTL for which the ANOVA supported a tradeoff are indicated with an asterisk.