Seasonal changes in ultrastructure and gene expression in the fat body of worker honey bees

The fat body of insects is a dynamic tissue involved in endocrine signaling and multiple metabolic functions, including lipid and carbohydrate metabolism, protein synthesis, amino acid and nitrogen metabolism, and detoxification of nitrogen metabolism. The fat body serves as a central nutrient storage facility for the synthesis and utilization of energy reserves. Energy reserves are stored as glycogen and triglycerides, which are degraded to glucose or fatty acids as fuel molecules on demand. Fatty acids also serve as precursors for the synthesis of eicosanoids, pheromones, phospholipids, and wax. Lipids constitute the main fat body component, and more than 90 % of the lipids are in the form of triglycerides, which are synthesized from dietary carbohydrates, fatty acids, or proteins (Arrese and Soulages, 2010).

During the summer, the spatiotemporal division of labor in worker honey bees is based on two main classes. Hive bees are young workers (0–21 days of age) who work inside the nest (0-3 days old bees are cell-cleaning specialists; 4-12 days old bees are called nurses as they nurse larvae and care for the brood nest; middle-aged bees (12-21 days) with task repertoire ranging from nest building and maintenance, to nectar receiving and processing, and to guarding the nest entrance); forager bees are the workers with an age of over 21 days, who venture outside the hive to collect food and water (Dixon et al., 2014, Johnson, 2010, Seeley and Kolmes, 1991). The transition between stages is associated with numerous physiological changes, such as a decrease in stored lipids and proteins, alteration in various tissues/organs such as the brain, fat bodies, pheromone-producing glands, and hypopharyngeal glands; the transition is also linked to rapid senescence. Until 10 days after the foraging transition, the mortality of foragers is approximately 20% but increases rapidly to almost 100% 20 days after the onset of foraging activity (Amdam, 2011). At the physiological level, the transitions are associated with changes in the titers of juvenile hormone (JH) and vitellogenin (Vg), both of which are key mediators of behavioral and physiological development of worker honey bees (Amdam et al., 2006). Vg is an egg yolk protein that is synthetized in fat body cells and released into the hemolymph, and its synthesis is positively correlated with the increased amount and quality of pollen in a protein-rich diet. JH is a crucial component of endocrine signaling and is linked to caste determination as well as the control of labor division in bees (Hartfelder, 2000, Elekonich et al., 2001). JH and Vg titers in honey bees are correlated negatively; JH titers are low in nurse bees and high in forager bees, and a decrease in Vg activity causes a rise in JH titers, which promotes behavioral development and initiates foraging. While Vg levels are believed to extend the lifespan of honey bees, JH acts as a pro-aging factor (Guidugli et al., 2005, Münch and Amdam, 2010).

Vg and JH titers change significantly throughout the year. JH levels peak during the summer and are lowest during the winter (Huang and Robinson, 1995), whereas Vg levels show the opposite pattern (Kunc et al., 2019, Koubová et al., 2021, Kodrík et al., 2022). Therefore, low JH and high Vg levels are observed in long-lived winter workers that are produced to sustain the colony throughout temperate winters. Winter workers, in contrast to summer workers, are task generalists who survive the cold season in a metabolically and physically active state by utilizing food resources and producing heat within thermoregulatory clusters (Stabentheiner et al., 2003, 2010). Winter workers gradually start to appear in the colonies at the end of summer and in early fall (Fluri et al., 1982, Fluri and Bogdanov, 1987), make up the majority of the hive population by mid-fall (Mattila et al., 2001), and maintain the colony until spring. A reduced photoperiod is believed to stimulate fat body mass, which leads to an increase in Vg levels and therefore lowers JH levels (Fluri and Bogdanov, 1987). Collectively, these results demonstrate that the fat body is a crucial component in controlling the nurse-forager transition and formation of the winter generation.

By analyzing structural changes in fat body cells combined with gene expression data, this study aimed to provide more details on the role of the fat body in the physiological settings of winter and summer workers, as well as differences between the youngest stage of hive bees and forager bees.

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