Conserved transcriptional plasticity, not local adaptation, dominates early climate responses across wild and cultivated apples

Abstract

Perennial crops respond to climate change through phenotypic plasticity and local adaptation, yet how these responses are orchestrated at the molecular level and reshaped by domestication remains poorly understood. We grew 1,249 seedlings from five populations of M. domestica, M. orientalis, and M. sylvestris under four simulated European climates, quantified 12 phenotypic traits, performed RNA sequencing on 96 individuals, and integrated these data with previously published genome-wide polymorphism data from M. sylvestris to disentangle conserved climate responses from local adaptation. Climate was the dominant driver of phenotypic and transcriptional variation, revealing 344 conserved climate-responsive genes enriched for stress responses, nutrient metabolism, and cell wall biosynthesis. These genes are under strong purifying selection and carry fewer deleterious mutations. In contrast, genome-environment association analyses identified 217 loci associated with temperature and precipitation gradients, only a subset of which showed climate-responsive expression and elevated genomic differentiation. Population-level expression divergence closely mirrored neutral genetic differentiation, indicating that most transcriptomic divergence reflects demographic history rather than adaptive regulatory evolution. Domestication reshaped molecular diversity and mutation load without disrupting the conserved climate-response program. Climate responses in apple are primarily mediated by an evolutionarily conserved transcriptional program maintained by strong purifying selection, whereas local adaptation relies on largely distinct, population-specific loci. These findings reveal that conserved plasticity constitutes the dominant molecular response to climatic variation, whereas local adaptation contributes a secondary, population-specific layer of evolutionary change.