Population Genomics Reveals Genetic Diversity, Introgression, and Genetic Differentiation in Tianshan Mountains Western Honeybees ( Apis mellifera )

ABSTRACT The Tianshan Mountains, which host two native subspecies of western honeybees, represent the easternmost natural distribution limit of Apis mellifera . The managed Xinjiang black honeybee ( XJ ), introduced a century ago and designated as a Chinese National Animal Genetic Resource, has expanded rapidly under anthropogenic management. However, this expansion simultaneously threatens populations of native subspecies Apis mellifera sinisxinyuan and Apis mellifera pomonella . Herein, we performed the first whole‐genome resequencing of the XJ population and analyzed whole‐genome data from 19 XJ workers and 172 global A. mellifera samples to clarify the evolutionary history of XJ and evaluate its interactions with native bees. Population structure and phylogenomic analyses showed that XJ clustered within C lineage but formed a divergent clade distinct from other C lineage subspecies, with the closest affinity to Apis mellifera carnica (FST = 0.053). Despite higher inbreeding than other C lineage subspecies, XJ displayed comparatively higher genetic diversity (Θπ = 2.15 × 10 −3 ) and heterozygosity (0.0028) than other C lineage populations (0.0015), although XJ 's value falls within the global range of A. mellifera . This genetic pattern can be attributed to substantial introgression (~10%–15%) from the M lineage, specifically from the native A. m. sinisxinyuan . TreeMix and F‐branch analysis identified significant gene flow from A. m. sinisxinyuan into the ancestral population of the XJ . Functional enrichment analysis suggested that genes within introgressed regions are involved in cold adaptation and foraging efficiency, and independent transcriptome validation confirmed differential expression of key candidate genes (e.g., LOC552291/MCM4) within these introgressed regions. Overall, our findings indicate that XJ represents an introduced population that has undergone regional adaptation, facilitated by the introgression of potentially adaptive alleles from native taxa. This case underscores the need for conservation strategies balancing management of economically valuable populations with protection of native lineages from genetic swamping and ecological competition.