Multidimensional Profiling of Senescence in Eastern Honey Bee, Apis cerana (Hymenoptera: Apidae), Workers: Morphology, Microstructure, and Transcriptomics

Worker honey bees are crucial for colony stability and ecosystem pollination. However, the cross-scale aging features and underlying mechanisms in the Eastern honey bee (<i>Apis cerana</i>) remain poorly understood. This study systematically investigated age-related changes in <i>A. cerana</i> workers across youth (1~5 days post-emergence, dpe), middle age (29 dpe), and old age (50 dpe) through integrated morphological, ultrastructural, and transcriptomic analyses. With increasing age, the phenotypic deterioration in the old bees (OBs) was significant: the body color brightness decreased by 16.7% compared to the young bees (YBs) (<i>p</i> < 0.001), and the hair density of the head, thorax, and abdomen declined by 63.5%, 97.2%, and 91.5%, respectively (<i>p</i> < 0.0001). The wing wear index (WWI) increased to 96.7% (<i>p</i> < 0.0001). The locomotor performance declined sharply, with only 6.7% of the OBs successfully reaching the feeding platform within 15 s (<i>p</i> < 0.0001). Ultrastructural analysis revealed sensory organ abrasion, flattened thoracic bristles, thickened cuticle, and 90.4% increased mitochondrial damage (<i>p</i> < 0.0001). The autophagosomes showed dynamic changes, with 81.8% reduction versus those of mid-aged bees (MBs) (<i>p</i> < 0.001), which suggests that mitochondrial dysfunction and autophagy dysregulation may be the core driving factors behind aging. Transcriptomics identified 67 differentially expressed genes enriched in lifespan regulation, glutathione metabolism, and lysosomal pathways. Fifteen key aging-related genes were identified, such as <i>major royal jelly protein 3</i> (<i>MRJP3</i>), <i>synaptic vesicle glycoprotein 2A</i> (<i>SV2A</i>), and <i>apidermin 3</i> (<i>APD3</i>), whose expression dynamics have been shown to be closely related to nutritional metabolism, behavioral perception, and the decline of epidermal barrier function. This work establishes the first multidimensional aging evaluation system for <i>A. cerana</i>, providing critical insights into bee senescence mechanisms and colony health optimization.