Abstract

The lifespan of Drosophila melanogaster can be extended substantially by inducing reproductive dormancy (also known as diapause) by lowered temperature and short days. This increase of longevity is accompanied by lowered metabolism and increased stress tolerance. We ask here whether behavioral senescence is ameliorated during adult dormancy. To study this we kept flies for seven or more weeks in normal rearing conditions or in diapause conditions and compared to 1-week-old flies in different behavioral assays of sleep, negative geotaxis and exploratory walking. We found that the senescence of geotaxis and locomotor behavior seen under normal rearing conditions was negligible in flies kept in dormancy. The normal senescence of rhythmic activity and sleep patterns during the daytime was also reduced by adult dormancy. Investigating the morphology of specific neuromuscular junctions (NMJs), we found that changes normally seen with aging do not take place in dormant flies. To monitor age-associated changes in neuronal circuits regulating activity rhythms, sleep and walking behavior we applied antisera to tyrosine hydroxylase (TH), serotonin and several neuropeptides to examine changes in expression levels and neuron morphology. In most neuron types the levels of stored neuromodulators decreased during normal aging, but not in diapause treated flies. No signs of neurodegeneration were seen in either condition. Our data suggest that age-related changes in motor neurons could be the cause of part of the behavioral senescence and that this is ameliorated by reproductive diapause. Earlier studies established a link between age-associated decreases in neuromodulator levels and behavioral decline that could be rescued by overexpression of neuromodulator. Thus, it is likely that the retained levels of neuromodulators in dormant flies alleviate behavioral senescence.

Highlights

  • Organismal lifespan is dependent on genetic and environmental factors such as diet and exposure to xenobiotics or other stressors, and can be extended experimentally in several model organisms via the manipulation of nutrient sensing and stress response signaling pathways

  • Use the term dormancy, and not diapause, for the physiological condition of the flies, since it may be argued that in laboratory strains of D. melanogaster dormancy is not induced in advance of aversive environmental conditions, but is triggered by them (Tauber et al, 2007)

  • When comparing the climbing ability of aging flies, dormant flies and flies that recovered from 3 weeks diapause (Figure 1D), we found that diapause-exposed flies performed significantly better than 5–7 weeks old flies and the recovered flies showed better climbing ability than similar aged flies reared under normal conditions

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Summary

Introduction

Organismal lifespan is dependent on genetic and environmental factors such as diet and exposure to xenobiotics or other stressors, and can be extended experimentally in several model organisms via the manipulation of nutrient sensing and stress response signaling pathways (reviewed in Guarente and Kenyon, 2000; Kenyon, 2005; Fontana et al, 2010). Dietary restriction and the genetic down regulation of the nutrientsensing insulin-IGF-like signaling (IIS) and target of rapamycin (TOR) networks are the most well studied means of extending lifespan in model organisms (Guarente and Kenyon, 2000; Clancy et al, 2001; Tatar et al, 2001; Broughton et al, 2005; Jones et al, 2009; Fontana et al, 2010). The effect of increased lifespan on agingrelated decline of neuronal function in the brain and associated behavioral and cognitive senescence is poorly understood. This is an important issue in modern society where life expectancy increases and thereby the incidence of various forms of dementia becomes increasingly problematic (Price et al, 1998; Metaxakis et al, 2014)

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