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

Abstract

AbstractIdentifying 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 ofArabidopsis thalianafrom Italy and Sweden, we examined the fitness consequences of a naturally occurring functional polymorphism inCBF2. 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 ofCBF2on 5-year mean fitness and fitness components at the native field sites by comparing near isogenic lines with alternate genotypes ofCBF2to their genetic background ecotypes. The effects ofCBF2were validated at the nucleotide level using gene edited lines in the native genetic backgrounds grown in simulated parental environments. The foreignCBF2genotype 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 thatCBF2encodes 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.