Human-mediated gene flow reshapes Apis mellifera diversity and erodes subspecies integrity in the Middle East

Abstract

Abstract In recent decades, human-mediated gene flow has profoundly reshaped Apis mellifera diversity across much of its native range, a process well documented in Europe but still poorly understood elsewhere. Here, we analyse whole-genome data from 423 individuals sampled across six countries, spanning six subspecies native to the Middle East and Egypt, together with 59 reference individuals. Genome-wide analyses of nuclear and mitochondrial variation inferred pervasive admixture driven by the importation of commercial queens and large-scale migratory beekeeping. Introgression from commercial A. m. ligustica , and, particularly from A. m. carnica , is widespread, reaching its highest estimates in A. m. meda (Iran) and A. m. syriaca (Jordan). Notably, the Egyptian A. m. lamarckii , itself introgressed, emerges as a major regional donor, substantially contributing to populations in Lebanon and Jordan and largely replacing the native A. m. jemenitica in the UAE. In contrast, admixture in Türkiye is dominated by gene flow among native subspecies, with A. m. anatoliaca contributing substantially to the gene pools of A. m. caucasia and A. m. meda , while receiving smaller reciprocal contributions. Nucleotide diversity is highest in Levantine admixed populations and declines significantly when estimated from individuals with high genetic integrity. Mitogenomic data broadly corroborate the nuclear findings, except in Türkiye and Iran, where all individuals clustered within the same branch as the C-lineage, thereby precluding inference of maternal introgression. Together, these findings indicate that modern apiculture is rapidly reshaping honeybee gene pools and eroding subspecies integrity across the Middle East.