Gene flow from the European wild apple and selection shaped the domesticated apple (Malus domestica Borkh.) genome

How selection and demography shape genomes of long-lived crops remains largely unresolved. Using apple ( Malus domestica ) as a model, we integrate 218 whole genomes (68 cultivated dessert/cider; 150 wild: M. sieversii , M. orientalis , M. sylvestris ), RNA-seq, and a flowering-time GWAS to resolve how these forces forged 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 strong domestication bottleneck, as expected in perennials. Demography-aware selection scans reveal largely non-overlapping targets: dessert shows more hard sweeps at genes linked to fruit quality, disease resistance, and flowering, whereas cider shows proportionally more soft sweeps and balancing selection; RNA-seq differential expression supports these candidates. Wild-to-crop introgression from M. sylvestris is extensive but heterogeneous by context: 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). Extending to the phenotype, 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 predicted deleterious load than wild relatives. Together, these results provide one of the most comprehensive population genomic portraits of a perennial fruit tree domestication, clarifying how selection and adaptive introgression jointly shaped the cultivated apple genome architecture and yielding actionable targets for breeding and conservation.