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 <i>Arabidopsis thaliana</i> from Italy and Sweden, we examined the fitness consequences of a naturally occurring functional polymorphism in <i>CBF2</i>. 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 <i>CBF2</i> on 5-y mean fitness and fitness components at the native field sites by comparing near-isogenic lines with alternate genotypes of <i>CBF2</i> to their genetic background ecotypes. The effects of <i>CBF2</i> were validated at the nucleotide level using gene-edited lines in the native genetic backgrounds grown in simulated parental environments. The foreign <i>CBF2</i> 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 <i>CBF2</i> 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.