Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity

Abstract

In most animals, longevity is achieved at the expense of fertility, but queen honey bees do not show this tradeoff. Queens are both long-lived and fertile, whereas workers, derived from the same genome, are both relatively short-lived and normally sterile. It has been suggested, on the basis of results from workers, that vitellogenin (Vg), best known as a yolk protein synthesized in the abdominal fat body, acts as an antioxidant to promote longevity in queen bees. We explored this hypothesis, as well as related roles of insulin-IGF-1 signaling and juvenile hormone. Vg was expressed in thorax and head fat body cells in an age-dependent manner, with old queens showing much higher expression than workers. In contrast, Vg expression in worker head was much lower. Queens also were more resistant to oxidative stress than workers. These results support the hypothesis that caste-specific differences in Vg expression are involved in queen longevity. Consistent with predictions from Drosophila, old queens had lower head expression of insulin-like peptide and its putative receptors than did old workers. Juvenile hormone affected the expression of Vg and insulin-IGF-1 signaling genes in opposite directions. These results suggest that conserved and species-specific mechanisms interact to regulate queen bee longevity without sacrificing fecundity.Apis mellifera ͉ lifespan ͉ social insect H oney bees (Apis mellifera) provide an attractive model to identify the molecular mechanisms regulating variation in lifespan. Workers and queens develop from the same genome, but queen lifespan is Ϸ10-fold longer (1). Moreover, queen longevity is achieved without the typical tradeoff between longevity and reproduction. Queens lay up to 2,000 eggs per day (2) and live for 1-3 years. Workers, in contrast, have limited fecundity and live for 3-6 weeks during spring and summer in temperate climates (1).Insulin-IGF-1 signaling (IIS) is a key integrative pathway regulating aging, fertility and other important biological processes in vertebrates and invertebrates. Down-regulation of IIS is associated with increased longevity and decreased fertility in Caenorhabditis elegans and Drosophila melanogaster (3). Although IIS functions are widely conserved, it is not known whether naturally occurring differences in longevity also are a result of variation in this pathway.Recent advances in insect molecular endocrinology have revealed connections between IIS and juvenile hormone (JH), a major insect hormone with diverse influences on growth, reproduction, and longevity in many species (4). Studies with Drosophila point to a connection between IIS and JH (5, 6). Because queens are both long-lived and reproductively active, the unique relationship between JH and vitellogenin (Vg) in honey bees has attracted attention (7). Honey bee Vg is a 180-kDa glycolipoprotein (8) synthesized in fat body cells and released to the hemolymph. Vg is best known as a yolk protein and is taken up by developing oocytes (9). JH is a gonadotropin and regulates vitellogenesis in ...

Senescence in the worker honey bee Apis Mellifera

“…It is possible that the concentration of hydrogen peroxide we used was too weak to induce much oxidative stress or stress-related mortality in our bees. This speculation is supported by the observation that paraquat (another free radical inducing agent) caused greater mortality in a comparable experiment (Corona et al, 2007). In that experiment, the median lifespan for worker bees 30 days of age was 33 h, compared to 66 h in our experiment.…”

“…Strikingly, the long life of social insect queens does not come at the cost of low reproduction: queens of many social insects lay hundreds or thousands of eggs per day throughout their adult life. Their ability to sustain both high reproductive effort and long life makes social insects particularly promising model systems for studies of aging (Parker et al, 2004;Seehus et al, 2006;Corona et al, 2005;Corona et al, 2007).…”

Weight of evidence evaluation of a network of adverse outcome pathways linking activation of the nicotinic acetylcholine receptor in honey bees to colony death

“…Vitellogenin is synthesized in fat body cells, released to the hemolymph (circulation), and taken up in developing oocytes (Corona et al, 2007). Mature honey bee queens, which lay~1000 eggs/day, continuously synthesize Vtg at high levels, including during periods when egg laying ceases (Seehuus et al, 2006;Corona et al, 2007).…”

“…Mature honey bee queens, which lay~1000 eggs/day, continuously synthesize Vtg at high levels, including during periods when egg laying ceases (Seehuus et al, 2006;Corona et al, 2007). However, in sterile worker bees, Vtg levels have been shown to change throughout their lives, with the highest levels observed in the long-lived winter bees and lowest in the short-lived summer foragers (Münch et al, 2015).…”

“…However, in sterile worker bees, Vtg levels have been shown to change throughout their lives, with the highest levels observed in the long-lived winter bees and lowest in the short-lived summer foragers (Münch et al, 2015). In addition to the role Vtg plays as an egg yolk protein, it has a role in oxidative stress resistance (Corona et al, 2007;Seehuus et al, 2006;Amdam et al, 2004). …”