A large-effect fitness trade-off across environments is explained by a single mutation affecting cold acclimation

Abstract

Identifying the genetic basis of local adaptation and fitness trade-offs across environments is a central goal of evolutionary biology. Cold acclimation is an adaptive plastic response for surviving seasonal freezing, and costs of acclimation may be a general mechanism for fitness trade-offs across environments in temperate zone species. Starting with locally adapted ecotypes of Arabidopsis thaliana from Italy and Sweden, we examined the fitness consequences of a naturally occurring functional polymorphism in CBF2. This gene encodes a transcription factor that is a major regulator of cold-acclimated freezing tolerance and resides within a locus responsible for a genetic trade-off for long-term mean fitness. We estimated the consequences of alternate genotypes of CBF2 on 5-y mean fitness and fitness components at the native field sites by comparing near-isogenic lines with alternate genotypes of CBF2 to their genetic background ecotypes. The effects of CBF2 were validated at the nucleotide level using gene-edited lines in the native genetic backgrounds grown in simulated parental environments. The foreign CBF2 genotype in the local genetic background reduced long-term mean fitness in Sweden by more than 10%, primarily via effects on survival. In Italy, fitness was reduced by more than 20%, primarily via effects on fecundity. At both sites, the effects were temporally variable and much stronger in some years. The gene-edited lines confirmed that CBF2 encodes the causal variant underlying this genetic trade-off. Additionally, we demonstrated a substantial fitness cost of cold acclimation, which has broad implications for potential maladaptive responses to climate change.

Keywords: antagonistic pleiotropy; cold acclimation; genetic trade-off; local adaptation; plasticity.

Fig. 1.

Least squares mean estimates of fitness (number of fruits per seedling planted) of the SW and IT ecotypes and NILs over five individual 1-y experiments at the Swedish (A) and Italian (B) field sites. Error bars are 1 SE. The predominant color indicates the genetic background (SW ecotype = blue; IT ecotype = red). Hatching indicates the genotype of the introgression segment containing CBF2 in the NILs. Asterisks represent statistically significant contrasts between a NIL and its genetic background (***P < 0.001; **P < 0.01; ns, not significant).

Fig. 2.

Least squares mean estimates of fitness (number of fruits per seedling planted) of the ecotypes and NILs in each individual year at the Swedish (A) and Italian (B) field sites. Error bars are 1 SE. The predominant color indicates the genetic background (SW ecotype = blue; IT ecotype = red). Hatching indicates the genotype of the introgression segment containing CBF2 in the NILs as shown in Fig. 1. Asterisks denote significant contrasts between a NIL and its genetic background (***P < 0.001; **P < 0.01; ^†0.05 < P < 0.1; ns, not significant).

Fig. 3.

Least squares mean fitness (number of fruits per seedling planted) of the ecotypes and gene-edited lines in the “Swedish” (A) and “Italian” (B) growth chambers. Error bars are 1 SE. The predominant color indicates the genetic background (SW ecotype = blue; IT ecotype = red). Hatching indicates the genotype of CBF2 (capitals = functional copy, lower case = loss of function) in gene-edited lines. Asterisks represent statistically significant contrasts between a gene-edited line and its genetic background (***P < 0.001; **P < 0.01). Note that the scale of the y axis of fitness for the Italian growth chamber is double that of the Swedish growth chamber.

Fig. 4.

Fitness components of the SW and IT ecotypes and NILs over five individual one-year experiments at the Swedish and Italian field sites. Mean proportion survival (averaged over years) at the Swedish (A) and Italian (B) field sites. Least squares mean fecundity at the same sites (C and D). Colors and hatching as in other figures. Error bars for fecundity are 1 SE; no bars are given for survival because it was analyzed with a binomial error distribution. Asterisks represent statistically significant contrasts between a NIL and its genetic background (***P < 0.001; **P < 0.01; *P < 0.05; ^†0.05 < P <0.1; ns, not significant).