Reproductive protein protects functionally sterile honey bee workers from oxidative stress

Abstract

Research on aging shows that regulatory pathways of fertility and senescence are closely interlinked. However, evolutionary theories on social species propose that lifelong care for offspring can shape the course of senescence beyond the restricted context of reproductive capability. These observations suggest that control circuits of aging are remodeled in social organisms with continuing care for offspring. Here, we studied a circuit of aging in the honey bee (Apis mellifera). The bee is characterized by the presence of a long-lived reproductive queen caste and a shorter-lived caste of female workers that are life-long alloparental care givers. We focus on the role of the conserved yolk precursor gene vitellogenin that, in Caenorhabditis elegans, shortens lifespan as a downstream element of the insulin͞insulin-like growth factor signaling cascade. Vitellogenin protein is synthesized at high levels in honey bee queens and is abundant in long-lived workers. We establish that vitellogenin gene activity protects worker bees from oxidative stress. Our finding suggests that one mechanistic explanation for patterns of longevity in bees is that a reproductive regulatory pathway has been remodeled to extend life. This perspective is of considerable relevance to research on longevity regulation that builds largely on inference from solitary model species.aging ͉ social evolution ͉ vitellogenin ͉ carbonylation ͉ RNA interference

Senescence in the worker honey bee Apis Mellifera

“…In that experiment, the median lifespan for worker bees 30 days of age was 33 h, compared to 66 h in our experiment. This observation is further supported by another experiment comparing paraquat-induced oxidative stress resistance in worker bees where complete mortality was reached within 60 hours of paraquat injection (Seehuus et al, 2006).…”

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

“…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). …”

“…Due to the antioxidant properties of Vtg, the unique localization of Vtg in fat cells of the thorax and brain, and the flexible aging patterns of bees, studies have been conducted to understand the role of Vtg throughout the lifespan (Seehuus et al, 2006;Corona et al, 2007;Münch et al, 2015). By studying Vtg levels in various tissues from drones, workers, and queens of different ages with knockdown technology, it has been demonstrated that Vtg is expressed at higher levels in both the thorax and head of queens, with negligible and decreasing levels found in the tissues of worker bees as they age (Corona et al, 2007).…”

“…By studying Vtg levels in various tissues from drones, workers, and queens of different ages with knockdown technology, it has been demonstrated that Vtg is expressed at higher levels in both the thorax and head of queens, with negligible and decreasing levels found in the tissues of worker bees as they age (Corona et al, 2007). Further, through evaluation of resistance to oxidative stress, studies show that Vtg plays a protective role in the bee by acting as a target of oxidative carbonylation and by scavenging free radicals (Seehuus et al, 2006). For example, Nelson et al (2007) demonstrated that knockdown of Vtg significantly reduced honey bee lifespan.…”