Honeybees are recognized as a model organism for understanding the basis of cognition (Menzel, 2012), especially their complex behavior. As eusocial insects, they form a hierarchical society consisting of queens, drones, and workers (Crespi and Yanega, 1995). They exhibit two sexes—males (drones) and females (queens and workers)—with the female caste further divided into reproductive queens and typically sterile workers specialized in colony maintenance (Johnson, 2003). The social organization is maintained through age polyethism among workers, in which tasks are sequentially assigned based on age (Robinson, 2009). For instance, newly emerged bees (0–3 days, cleaning brood cells), nurse bees (4–12 days, feeding larvae and the queen), middle-aged bees (12–20 days, comprehensive hive maintenance), and foragers (over 21 days, collecting resources) (Robinson, 2009, Seeley, 1982, Seeley and Kolmes, 1991). Nurse bees and middle-aged bees are often collectively referred to as nurse bees. Interestingly, some younger foragers may exhibit partial rejuvenation by reverting to nursing tasks under stress (Rascon et al., 2011), ensuring colony homeostasis when nurse bees are scare. Typically, healthy young bees care for the queen and brood, whereas older individuals are assigned to foraging tasks (Toth and Robinson, 2005). This plasticity is inherent to the superorganism nature of honeybee society (Seeley, 1989).

Stress factors that threaten bees are commonly classified as abiotic (e.g., environmental factors, pesticides) and biotic (e.g., pathogens, parasite and predator) (Li et al., 2018), and both of which can synergize with climate change, a major factor in Colony Collapse Disorder (CCD) (Le Conte and Navajas, 2008). Climate change induces fluctuations in environmental conditions, such as temperature, precipitation, and pollinators like honeybees are highly sensitive to these climatic factors (Petz et al., 2004). To maintain a stable nest environment during brood rearing, worker bees expend significant energy regulating temperature and humidity through complex behavior mechanisms (Heinrich and Esch, 1994, Egley and Breed, 2013, Kamboj et al., 2024). High developmental temperatures during the pupal stage accelerate physiological development and trigger precocious foraging (Becher et al., 2009), leading to abnormal growth patterns. Consequently, physiological changes in brood, reflected in caste transition rates, serve as an indirect indicator of colony health.

Caste transition is fundamentally linked to the aging, defined as the progressive accumulation of changes over time that increase an organism's susceptibility to disease and death (Harman, 1981). Therefore, both the chronological and biological ages of worker bees must be considered. Chronological age refers to the time elapsed since an organism’s birth, while biological age reflects the physiological changes occurring throughout its lifespan and is, by definition, influenced by external factors (Corby-Harris and Snyder, 2018).

This biological age is estimated based on biomarkers indicative of caste, reflecting the physiological specialization for caste‐specific tasks. As nutritional indicator organs, the hypopharyngeal glands (HGs), responsible for royal jelly synthesis, and the abdominal fat body, which accumulates lipids, exhibit age-specific development. Both show significant growth during the nurse phase and subsequent regression in the forager phase (Chan et al., 2011, Ahmad et al., 2021). Molecular markers such as AmGr10 and Vitellogenin (Vg) serve as indicators of these organ development and are closely linked to nutritional status (Corona et al., 2007, Paerhati et al., 2015), while ilp2 is also closely associated with nutritional status (Nilsen et al., 2011). Moreover, behavioral maturation-related genes, including ilp1, JH and TOR1, regulate caste transition via the insulin signaling pathway (IIS) (Corona et al., 2007, Ament et al., 2008). The enzyme involved in JH biosynthesis, Juvenile Hormone Acid Methyltransferase (JHAMT), exhibits changes in expression similar to JH titer and can serve as an alternative marker to JH, which cannot be directly measured because it is a sesquiterpenoid hormone.

These molecular markers exhibit caste-specific expression patterns, with ilp1 (Ament et al., 2008); TOR1 (Ament et al., 2008), and JH (Nelson et al., 2007), predominantly expressed in foragers, whereas AmGr10 (Paerhati et al., 2015, Lim et al., 2019); Vg (Nelson et al., 2007), and ilp2 (Nilsen et al., 2011) show higher expression in nurse bees. Additionally, in the case of heat stress response, hsp70 can serve as an indicator because, as a molecular chaperone, it plays a role in aging (Abou-Shaara, 2024).

Based on these insights, it becomes essential to develop reliable quantitative methods to assess the stress. Although the beekeeping industry is increasingly adopting IoT and AI-based predictive models (Jeong et al., 2024), robust models that utilize biological data are still underdeveloped. Notably, Alaux et al. (Alaux et al., 2018) made an initial attempt to utilize honeybee biological data in aging research. However, subsequent studies have been scarce. As climate change intensifies and CCD becomes increasingly prevalent, it is essential to integrate these approaches into honeybee research and advance the field.

In this study, we developed a mathematical model to estimate the effects of stress on caste transition (from nurse to forager) by assessing the acceleration of internal processes (biological age). The model was constructed using honeybees of varying ages collected during the flowering period and validated with individuals of the same chronological age sampled independently during the Flowering, Dearth, and Overwintering Periods. This approach quantifies the seasonal stress effects on biological age, providing insights into the mechanisms of maturation and aging in response to stress, and supporting strategies to enhance insect resilience.