Skip to main content
SpringerLink
Log in

Life extension and the position of the hormetic zone depends on sex and genetic background in Drosophila melanogaster

  • Research Article
  • Published:
Biogerontology Aims and scope Submit manuscript

Abstract

Hormesis, the beneficial effect of a mild stress, has been proposed as a means to prolong the period of healthy ageing as it can increase the average lifespan of a cohort. However, if we want to use hormesis therapeutically it is important that the treatment is beneficial on the individual level and not just on average at the population level. Long lived lines have been shown not to benefit from a, in other lines, hormesis inducing heat treatment in Drosophila melanogaster, D. buzzatii and mice. Also in many experiments hormesis has been reported to occur in one sex only, usually males but not in females. Here we investigated the interaction between the hormetic response and genetic background, sex and duration of a mild heat stress in D. melanogaster, using three replicate lines that have been selected for increased longevity and their respective control lines. We found that genetic background influences the position of the hormetic zone. The implication of this result could be that in a genetically diverse populations a treatment that is life prolonging in one individual could be life shortening in other individuals. However, we did find a hormetic response in all combinations of line and sex in at least one of the experiments which suggests that if it is possible to identify the optimal hormetic dose individually hormesis might become a therapeutic treatment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Bilde T, Maklakov AA, Meisner K, la Guardia L, Friberg U (2009) Sex differences in the genetic architecture of lifespan in a seed beetle: extreme inbreeding extends male lifespan. BMC Evol Biol 9. doi:3310.1186/1471-2148-9-33

  • Bubliy OA, Loeschcke V (2005) Correlated responses to selection for stress resistance and longevity in a laboratory population of Drosophila melanogaster. J Evol Biol 18:789–803. doi:10.1111/j.1420-9101.2005.00928.x

    Article  PubMed  CAS  Google Scholar 

  • Burger JMS, Promislow DEL (2004) Sex-specific effects of interventions that extend fly life span. Sci Aging Knowl Environ 28:pe30

    Google Scholar 

  • Butov A, Johnson T, Cypser J, Sannikov I, Volkov M, Sehl M, Yashin A (2001) Hormesis and debilitation effects in stress experiments using the nematode worm Caenorhabditis elegans: the model of balance between cell damage and HSP levels. Exp Gerontol 37:57–66

    Article  PubMed  CAS  Google Scholar 

  • Calabrese EJ (2008) Hormesis and medicine. Br J Clin Pharmacol 66:594–617. doi:10.1111/j.1365-2125.2008.03243.x

    PubMed  CAS  Google Scholar 

  • Cypser JR, Johnson TE (2002) Multiple stressors in Caenorhabditis elegans induce stress hormesis and extended longevity. J Gerontol A Biol Sci Med Sci 57:B109–B114

    PubMed  Google Scholar 

  • Gomez FH, Bertoli CI, Sambucetti P, Scannapieco AC, Norry FM (2009) Heat-induced hormesis in longevity as correlated response to thermal-stress selection in Drosophila buzzatii. J Therm Biol 34:17–22. doi:10.1016/j.jtherbio.2008.09.003

    Article  Google Scholar 

  • Good TP, Tatar M (2001) Age-specific mortality and reproduction respond to adult dietary restriction in Drosophila melanogaster. J Insect Physiol 47:1467–1473

    Article  PubMed  CAS  Google Scholar 

  • Guedes NMP, Tolledo J, Correa AS, Guedes RNC (2010) Insecticide-induced hormesis in an insecticide-resistant strain of the maize weevil, Sitophilus zeamais. J Appl Entomol 134:142–148. doi:10.1111/j.1439-0418.2009.01462.x

    Article  CAS  Google Scholar 

  • Heidler T, Hartwig K, Daniel H, Wenzel U (2010) Caenorhabditis elegans lifespan extension caused by treatment with an orally active ROS-generator is dependent on DAF-16 and SIR-2.1. Biogerontology 11:183–195. doi:10.1007/s10522-009-9239-x

    Article  PubMed  CAS  Google Scholar 

  • Hercus MJ, Hoffmann AA (2000) Maternal and grandmaternal age influence offspring fitness in Drosophila. Proc R Soc Lond B Biol Sci 267:2105–2110

    Article  CAS  Google Scholar 

  • Hercus MJ, Loeschcke V, Rattan SIS (2003) Lifespan extension of Drosophila melanogaster through hormesis by repeated mild heat stress. Biogerontology 4:149–156

    Article  PubMed  CAS  Google Scholar 

  • Hoffmann AA, Dagher H, Hercus M, Berrigan D (1997) Comparing different measures of heat resistance in selected lines of Drosophila melanogaster. J Insect Physiol 43:393–405

    Article  PubMed  CAS  Google Scholar 

  • Ikeya T, Broughton S, Alic N, Grandison R, Partridge L (2009) The endosymbiont Wolbachia increases insulin/IGF-like signalling in Drosophila. Proc R Soc Lond B Biol Sci 276:3799–3807. doi:10.1098/rspb.2009.0778

    Article  CAS  Google Scholar 

  • Iliadi KG, Iliadi NN, Boulianne GL (2009) Regulation of Drosophila life-span: effect of genetic background, sex, mating and social status. Exp Gerontol 44:546–553. doi:10.1016/j.exger.2009.05.008

    Article  PubMed  Google Scholar 

  • Kuether K, Arking R (1999) Drosophila selected for extended longevity are more sensitive to heat shock. Age 22:175–180

    Article  Google Scholar 

  • Le Bourg E (2009) Hormesis, aging and longevity. Biochim Biophys Acta 1790:1030–1039. doi:10.1016/j.bbagen.2009.01.004

    PubMed  CAS  Google Scholar 

  • Le Bourg E, Minois N, Bullens P, Baret P (2000) A mild stress due to hypergravity exposure at young age increases longevity in Drosophila melanogaster males. Biogerontology 1:145–155

    Article  PubMed  CAS  Google Scholar 

  • Le Bourg E, Valenti P, Lucchetta P, Payre F (2001) Effects of mild heat shocks at young age on aging and longevity in Drosophila melanogaster. Biogerontology 2:155–164

    Article  PubMed  CAS  Google Scholar 

  • Le Bourg E, Toffin E, Masse A (2004) Male Drosophila melanogaster flies exposed to hypergravity at young age are protected against a non-lethal heat shock at middle age but not against behavioral impairments due to this shock. Biogerontology 5:431–443

    Article  PubMed  Google Scholar 

  • Le Bourg E, Massou I, Gobert V (2009) Cold stress increases resistance to fungal infection throughout life in Drosophila melanogaster. Biogerontology 10:613–625. doi:10.1007/s10522-008-9206-y

    Article  PubMed  CAS  Google Scholar 

  • Liao CY, Rikke BA, Johnson TE, Diaz V, Nelson JF (2010) Genetic variation in the murine lifespan response to dietary restriction: from life extension to life shortening. Aging Cell 9:92–95. doi:10.1111/j.1474-9726.2009.00533.x

    Article  PubMed  CAS  Google Scholar 

  • Maklakov AA, Simpson SJ, Zajitschek F, Hall MD, Dessmann J, Clissold F, Raubenheimer D, Bonduriansky R, Brooks RC (2008) Sex-specific fitness effects of nutrient intake on reproduction and lifespan. Curr Biol 18:1062–1066. doi:10.1016/j.cub.2008.06.059

    Article  PubMed  CAS  Google Scholar 

  • Maklakov AA, Hall MD, Simpson SJ, Dessmann J, Clissold FJ, Zajitschek F, Lailvaux SP, Raubenheimer D, Bonduriansky R, Brooks RC (2009) Sex differences in nutrient-dependent reproductive ageing. Aging Cell 8:324–330. doi:10.1111/j.1474-9726.2009.00479.x

    Article  PubMed  CAS  Google Scholar 

  • Minois N (2000) Longevity and aging: beneficial effects of exposure to mild stress. Biogerontology 1:15–29

    Article  PubMed  CAS  Google Scholar 

  • Moskalev A (2007) Radiation-induced life span alteration of Drosophila lines with genotype differences. Biogerontology 8:499–504. doi:10.1007/s10522-007-9090-x

    Article  PubMed  Google Scholar 

  • Moskalev A, Shaposhnikov M, Turysheva E (2009) Life span alteration after irradiation in Drosophila melanogaster strains with mutations of Hsf and Hsps. Biogerontology 10:3–11. doi:10.1007/s10522-008-9147-5

    Article  PubMed  CAS  Google Scholar 

  • Norry FM, Loeschcke V (2003) Heat-induced expression of a molecular chaperone decreases by selecting for long-lived individuals. Exp Gerontol 38:673–681

    Article  PubMed  CAS  Google Scholar 

  • Norry FM, Sambucetti P, Scannapieco AC, Loeschcke V (2006) Altitudinal patterns for longevity, fecundity and senescence in Drosophila buzzatii. Genetica 128:81–93. doi:10.1007/s10709-005-5537-7

    Article  PubMed  CAS  Google Scholar 

  • Onodera A, Yanase S, Ishii T, Yasuda K, Miyazawa M, Hartman PS, Ishii N (2010) Post-dauer life span of Caenorhabditis elegans dauer larvae can be modified by X-irradiation. J Radiat Res 51:67–71. doi:10.1269/jrr.09093

    Article  PubMed  Google Scholar 

  • Rattan SIS (2008) Principles and practice of hormetic treatment of ageing and age-related diseases. Hum Exp Toxicol 27:151–154. doi:10.1177/0960327107083409

    Article  PubMed  Google Scholar 

  • Rattan SIS, Clark BFC (2005) Understanding and modulating ageing. IUBMB Life 57:297–304. doi:10.1080/15216540500092195

    Article  PubMed  CAS  Google Scholar 

  • Sarup P, Sørensen P, Loeschcke V (in press) Flies selected for longevity retain a young gene expression profile. AGE

  • Sørensen JG, Kristensen TN, Kristensen KV, Loeschcke V (2007) Sex specific effects of heat induced hormesis in Hsf-deficient Drosophila melanogaster. Exp Gerontol 42:1123–1129. doi:10.1016/j.exger.2007.09.001

    Article  PubMed  Google Scholar 

  • Sørensen JG, Sarup P, Kristensen TN, Loeschcke V (2008) Temperature induced hormesis in Drosophila. In: Le Bourg E, Rattan SIS (eds) Mild stress and healthy aging. Springer-Verlag, Netherlands, pp 65–80

    Chapter  Google Scholar 

  • Sørensen JG, Holmstrup M, Sarup P, Loeschcke V (2010) Evolutionary theory and studies of model organisms predict a cautiously positive perspective on the therapeutic use of hormesis for healthy aging in humans. Dose Response 8:53–57. doi:10.2203/dose-response.09-040.Sorensen

    Article  Google Scholar 

  • Tricoire H, Battisti V, Trannoy S, Lasbleiz C, Pret AM, Monnier V (2009) The steroid hormone receptor EcR finely modulates Drosophila lifespan during adulthood in a sex-specific manner. Mech Ageing Dev 130:547–552. doi:10.1016/j.mad.2009.05.004

    Article  PubMed  CAS  Google Scholar 

  • Watson MJO, Hoffmann AA (1996) Acclimation, cross-generation effects, and the response to selection for increased cold resistance in Drosophila. Evolution 50:1182–1192

    Article  Google Scholar 

Download references

Acknowledgments

The authors are grateful to Doth Andersen for technical assistance, to Vanessa Kellermann and Janneke Wit for helpful comments on the MS, to the Danish Natural Sciences Research Council (frame and centre grant to V.L.), the Lundbeck foundation and Carlsberg foundations (stipend to P.S.) for financial support.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Ecology and Genetics, Aarhus Centre for Environmental Stress Research (ACES), Aarhus University, Ny Munkegade 114, 8000, Aarhus C, Denmark

    Pernille Sarup & Volker Loeschcke

Authors
  1. Pernille Sarup
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Volker Loeschcke
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pernille Sarup.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sarup, P., Loeschcke, V. Life extension and the position of the hormetic zone depends on sex and genetic background in Drosophila melanogaster . Biogerontology 12, 109–117 (2011). https://doi.org/10.1007/s10522-010-9298-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10522-010-9298-z

Keywords

Search

Navigation