Molecular signatures of adaptive heat tolerance in hybridized honey bee populations (Apis mellifera)

Thermal stress poses a major threat to insect fertility and survival, yet the molecular basis of thermal resilience remains poorly understood. We integrated population genomics and proteomics to investigate adaptive heat tolerance in two honey bee (Apis mellifera) populations: wild-derived Southern California (SoCal) bees and commercial bees from Northern California. Global and local ancestry inference revealed substantial African introgression in SoCal bees, contrasting with the European-dominated commercial population. Genome-wide SNP data showed that SoCal bees harbor significantly higher nucleotide diversity, especially in heat shock protein (HSP) gene regions. Protein expression profiling of drone reproductive tissue revealed significant population-level differences in HSP abundance, with commercial bees exhibiting higher expression, which potentially reflects compensatory upregulation in the face of less effective allelic variants. Protein–protein interaction networks showed distinct clustering of HSPs in sperm and seminal fluid, underscoring divergent regulatory architectures of HSPs in these tissues. Together, these molecular signatures suggest that adaptive introgression and elevated genetic diversity underlie enhanced thermal resilience in SoCal bees. Our findings highlight the value of hybridized populations for uncovering evolutionarily and agriculturally relevant stress-tolerance mechanisms in a changing climate.