Antioxidation Defenses of Apis mellifera Queens and Workers Respond to Imidacloprid in Different Age-Dependent Ways: Old Queens Are Resistant, Foragers Are Not

SIMPLE SUMMARY: Honey bees are unique for studies on aging because queens live 40-fold longer than workers. An efficient antioxidant defense (ADS) is thought to be pivotal for longevity, but not always. How were different ADSs shaped by evolution in young and old queens and workers? Honey bees, the essential pollinators, are facing depopulation due, at least in part, to pesticides, such as imidacloprid, an oxidative stressor. Is an evolutionarily shaped ADS still useful for contemporary young and old queens/workers? Answering these questions is important for emerging oxidative-stress ecology and protecting contemporary honey bees. The ADS activity was determined in 1-day-old, 20-day-old, and 2-year-old queens and in 1-day-old and 20-day-old workers (foragers) fed without (control) or with low or high imidacloprid (in bee food). ADS was upregulated in workers with age but downregulated in queens. However, imidacloprid oxidative stress suppressed the active ADS in workers, particularly 20-day-old foragers, but not in 1-day-old queens. Unexpectedly, poor ADS activity in 2-year-old queens was highly upregulated by imidacloprid. Thus, queen and worker ADSs respond to imidacloprid in opposite ways, and old queens were still resistant, but foragers were not. This may be unfavorable for foragers dwelling in ecosystems that expose them to pesticides. ABSTRACT: We investigated how different antioxidant defenses (ADSs) were shaped by evolution in young/old Apis mellifera workers and queens to broaden the limited knowledge on whether ADSs are effective in contemporary pesticide environments and to complete bee oxidative-aging theory. We acquired 1-day-old, 20-day-old, and 2-year-old queens and 1-day-old and 20-day-old workers (foragers) fed 0, 5, or 200 ppb imidacloprid, a pesticide oxidative stressor. The activities of catalase, glutathione peroxidase, glutathione S-transferase, and superoxide dismutase and the level of total antioxidant potential were determined in hemolymph. The ADS was upregulated in workers with age but downregulated in queens. Imidacloprid suppressed the ADS in all workers, particularly in foragers with an upregulated ADS, but it did not affect the ADS in 1-day-old queens. In contrast to foragers, the downregulated ADS of 2-year-old queens was unexpectedly highly upregulated by imidacloprid, which has not been previously shown in such old queens. The principal component analysis confirmed that queen and worker ADSs responded to imidacloprid in opposite ways, and ADS of 2-year-queens was markedly different from those of others. Thus, evolutionary shaped ADSs of older queens and workers may be of the limited use for foragers dwelling in pesticide ecosystems, but not for old queens.