Aging and its modulation in a long-lived worker caste of the honey bee

Abstract

SUMMARYHighly social animals provide alternative aging models in which vastly different lifespan patterns are flexible, and linked to social caste. Research in these species aims to reveal how environment, including social cues, can shape the transition between shortlived and extremely long-lived phenotypes with negligible senescence. Among honey bee workers, short to intermediate lifespans are typical for summer castes, while the winter caste can live up to 10 times longer. For summer castes, experimental interventions could predictably accelerate, slow or revert functional senescence. In contrast, little is known about the particular conditions under which periods of negligible senescence in winter castes can be disrupted or sustained. We asked how manipulation of social environment in colonies with long-lived winter bees might alter the pace of functional senescence, measured as learning performance, as well as of cellular senescence, measured as lipofuscin accumulation. We show that behavioral senescence becomes rapidly detectable when the winter state is disrupted, and changes in social task behaviors and social environment (brood) are induced. Likewise, we found that cellular senescence was induced by such social intervention. However, cellular senescence showed marked regional differences, suggesting that particular brain regions age slower than others. Finally, by preventing post-winter colonies from brood rearing, behavioral senescence became undetectable, even after transition to the usually short-lived phenotypes had occurred. We envision that social regulation of negligible functional senescence and highly dynamic accumulation of a universal symptom of cellular aging (lipofuscin) offers rewarding perspectives to target proximate mechanisms of slowed aging. Supplementary material available online at

Vitellogenin in the honey bee brain: Atypical localization of a reproductive protein that promotes longevity

“…For worker bees, odor-learning capacity rapidly declines (within 2 weeks) in the shortest-lived foragers, while such decline remains undetectable for more than 6 months in the longest-lived winter bee worker type ('negligible senescence') (Behrends, Scheiner et al 2007, Münch, Kreibich et al 2013. Moreover, patterns of slowed, accelerated and also reversed behavioral aging can be experimentally evoked, when a change in the social environment pushes workers to transition from one worker-, and hence aging-type, to another Baker, Wolschin et al 2012, Münch, Kreibich et al 2013. The social cues that are experimentally coopted to "push" workers to change their tasks include those that convey the presence or absence of brood, or those cues that signal a skewed social demography in which colonies lack a certain worker type (Nelson 1927, Maurizio 1950.…”

“…Rapid, slowed or reversed behavioral senescence rates are linked to cellular changes in the brain, including: an altered abundance of synaptic and other signaling proteins (synapsin, protein kinase C), of proteins involved in cellular maintenance and lipid transport (heat shock proteins, peroxiredoxin, and fatty acid binding protein), the accumulation of residuals ('waste') from incomplete lysosomal degradation (lipofuscin), and changes in the brain's epigenetic state that differ between worker types (Baker, Wolschin et al 2012, Herb, Wolschin et al 2012, Münch, Kreibich et al 2013 review in, . Combined, these changes may contribute to learning decline.…”

Ageing and somatic maintenance in social insects

“…These bees engage in neither foraging nor brood care, but instead work to maintain colony temperature during the winter [23]. They have the longest life expectancy of the three worker behavioural castes, while foragers have the shortest [4,24 ].…”

“…In localised areas of the honeybee head, damaged proteins and lipids tend to be higher in foragers than in the nurses and winter bees. Lipofuscin levels in the hypopharyngeal glands and pars intercerebralis were found to be higher in foragers than in winter bees of similar age, while no difference was found between these castes in the calyx [24 ]. Seehuus et al [14] used staining and microscopy to investigate protein carbonyls and nitrotyrosine (an indicator of nitration damage to proteins) in three areas of the honeybee brain.…”

Vitellogenin family gene expression does not increase Drosophila lifespan or fecundity

“…Differential expression of Vg has also been associated with the differences in lifespan between different kinds of worker bees: higher expression is seen in "winter bees" which have a lifespan of 10 months to 1 year, and lower expression in "summer bees" with a lifespan of 30–50 days 16– 18 . RNAi knockdown of Vg expression in workers resulted in lower oxidative stress resistance 19 and shorter lifespan 20 .…”