Honey robbing, as an extreme adaptive response of honey bee colonies to resource scarcity, poses devastating threats to apiaries, yet the underlying molecular mechanisms remain poorly understood. We compared morphological traits and survival rates between robber bees and normal foragers and conducted proteomic sequencing of bee head samples. The results demonstrated that robber bees exhibited darker tergite coloration and significantly shortened lifespan. Proteomic analysis revealed that the darker coloration was primarily attributed to enhanced cuticular melanin deposition mediated by upregulated laccase-5, while the shortened lifespan mainly resulted from oxidative stress and immune suppression: the downregulation of heat shock protein 75 kDa and glutathione transferase weakened antioxidant capacity, and despite compensatory upregulation of the cytochrome P450 enzyme system, flavin-containing monooxygenases and other enzymes, oxidative damage continued to accumulate. Concurrently, downregulation of Defense protein 3 and C-type lectin 5 caused immune deficiency in robber bees. The results also showed metabolic and protein synthesis reprogramming in robber bees, specifically manifested by upregulated key enzymes in nicotinate and nicotinamide metabolism, the pentose phosphate pathway, and nucleotide metabolism, along with activation of protein synthesis-transport-export systems. We found that robber bees employ a “metabolic-synthetic co-enhancement” physiological strategy to boost short-term foraging efficiency, but this strategy simultaneously induces oxidative damage and immune suppression, ultimately shortening their lifespan. This study provides the first proteomic evidence revealing the physiological trade-offs underlying this behavior at the molecular level, offering novel insights into the physiological costs of behavioral adaptation in animals.

Honey robbing, as an extreme adaptive response of honeybee colonies to resource scarcity, poses devastating threats to apiaries, yet the underlying molecular mechanisms remain poorly understood. We compared morphological traits and survival rates between robber bees and normal foragers and conducted proteomic sequencing of bee head samples. The results indicated that: (1) Darker tergite coloration, largely attributed to enhanced cuticular melanin deposition mediated by upregulated laccase-5; (2) Significantly shortened lifespan, primarily resulting from oxidative stress and immune suppression: Downregulation of heat shock protein 75 kDa and glutathione transferase weakened antioxidant capacity, and despite compensatory upregulation of cytochrome P450 enzyme system, flavin-containing monooxygenases, and other enzymes, oxidative damage still accumulated; Concurrently, downregulation of Defense protein 3 and C-type lectin 5 caused immune deficiency; (3) Metabolic and protein synthesis reprogramming, specifically manifested by upregulated key enzymes in nicotinate and nicotinamide metabolism, pentose phosphate pathway, and Nucleotide metabolism, along with activation of protein synthesis-transport-export systems. We found that robber bees employ a "metabolic-synthetic co-enhancement" physiological strategy to boost short-term foraging efficiency, but this simultaneously induces oxidative damage and immune suppression, ultimately shortening their lifespan. This study provides the first proteomic evidence revealing the physiological trade-offs underlying the behavior at the molecular level, offering novel insights into the physiological costs of behavioral adaptation in animals.