Gene flow from the European wild apple and selection shaped the domesticated apple genome

Summary How selection and demography jointly shape the genomes of perennial crops remains an open question. Apple (M. domestica) is a compelling system because its domestication involved multiple wild progenitors and post-domestication admixture across Eurasia. We integrate 218 whole genomes (68 cultivated dessert/cider; 150 wild: M. sieversii, M. orientalis, M. sylvestris), RNA sequencing (RNA-seq), and a genome-wide association study of flowering time to resolve how these forces shaped the cultivated apple genome. Despite weak neutral differentiation and widespread admixture, dessert and cider apples form distinct gene pools that derive primarily from M. sieversii-M. orientalis rather than European M. sylvestris. We find no evidence of a domestication bottleneck, as expected in perennials. Demographic-aware selection scans reveal non-overlapping targets supported by RNA-seq; dessert shows more hard sweeps at fruit quality, disease resistance, and flowering genes, whereas cider shows proportionally more soft sweeps and balancing selection. Wild-to-crop introgression from M. sylvestris is extensive but heterogeneous; some introgressed tracts concentrate in hard-sweep regions and approach fixation (consistent with rapid, targeted uptake), whereas others persist at intermediate frequencies with soft-sweep signatures (consistent with diffuse, recurrent introgression of adaptive alleles). The lead chromosome 9 flowering-time association lies within an introgressed segment near a transposable element and is separated from sweep peaks, consistent with regulatory/polygenic control. Cultivated apples carry a lower deleterious load than wild relatives. These results provide a comprehensive genomic portrait of perennial fruit tree domestication, clarifying how selection and adaptive introgression shaped the cultivated apple genome and yielding actionable targets for breeding and conservation.