Modeling biological age to assess maturation and ageing (Apis mellifera)

Environmental stresses caused by climate change-especially fluctuations in temperature and humidity-affect the behavior and physiology of honeybees (Apis mellifera), a model organism with a complex social structure. Worker bees, the most numerous members of colonies, perform tasks based on age polyethism, with lifespans ranging from short-lived summer bees to long-lived winter bees. While regulating this aging process and understanding how stress influences maturation are crucial for colony survival, these mechanisms remain poorly understood. To address this issue, we analyzed two physiological traits (hypopharyngeal gland development and fat body lipid mass) and the expression of six genes (ilp1, ilp2, TOR1, JHAMT, AmGr10, and Vg) in marked workers across 11 age groups (0, 3, 6, 8, 10, 12, 14, 16, 18, 21, and 25 days) during the flowering period, under controlled environmental conditions and low DWV levels. Five genes (ilp1, ilp2, TOR1, JHAMT, and AmGr10) were identified as reliable age-related markers and were used to develop a predictive model of biological age. Validation on 14-day-old workers sampled during the Flowering, Dearth, and early Overwintering Periods demonstrated that seasonal stress affects biological aging, with predicted ages of 12.14 days (flowering), 14.64 days (dearth), and 28.17 days (early overwintering). The accelerated biological aging in overwintering bees, linked with disease presence and colony failure, confirmed the model's reliability. This study provides new insights into stress-induced aging in social insects and presents practical tools for monitoring colony health and resilience.