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The ecological stress theory of aging and hormesis: an energetic evolutionary model

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Abstract

Free-living organisms normally struggle to exist in harsh environments that are nutritionally and energetically inadequate, where evolutionary adaptation is challenged by internal stresses within organisms and external stresses from the environment. The incorporation of environmental variables into aging theories such as the free-radical and metabolic rate/oxidative stress theories, is the basis of the ecological stress theory of aging and hormesis. Environmental variation from optimum to lethal extremes gives a fitness-stress continuum, where energetic efficiency, or fitness, is inversely related to stress level; in the evolutionary context survival is a more direct measure of fitness for assessing aging than is lifespan. On this continuum, the hormetic zone is in the optimum region, while aging emphasizes survival towards lethal extremes. At the limits of survival, a convergence of physiological and genetical processes is expected under accumulating stress from Reactive Oxygen Species, ROS. Limited ecologically-oriented studies imply that major genes are important towards limits of survival compared with the hormetic zone. Future investigations could usefully explore outlier populations physiologically and genetically, since there is the likelihood that genetic variability may be lower in those cohorts managing to survive to extremely advanced ages as found in highly stressed ecological outlier populations. If so, an evolutionary explanation of the mortality-rate decline typical of cohorts of the extremely old emerges. In summary, an energetic evolutionary approach produces a general aging theory which automatically incorporates hormesis, since the theory is based on a fitness-stress continuum covering the whole range of possible abiotic environments of natural populations.

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References

  • Alonso-Alvarez C, Bertrand S, Deveney G, Prost J, Faivre B, Chastel O, Sorci G (2006) An experimental manipulation of life-history trajectories and resistance to oxidative stress. Evolution 60:1913–1924

    Article  PubMed  Google Scholar 

  • Ames BN (2004) Delaying the mitochondrial decay of aging. Ann NY Acad Sci 1019:406–411

    Article  PubMed  CAS  Google Scholar 

  • Arking R (1998) Biology of aging: observations and principles, 2nd edn. Sinauer Associates, Sunderland, Massachusetts

    Google Scholar 

  • Austad SN (1997) Why we age. John Wiley, New York

    Google Scholar 

  • Barja G (2004) Aging in vertebrates, and the effect of caloric restriction: a mitochondrial free radical production––DNA damage mechanism? Biol Rev 79:235–251

    Article  PubMed  Google Scholar 

  • Bernstein AM, Willcox BJ, Tamaki H, Kunishima N, Suziki M, Willcox DC, Yoo JS, Perls TT (2004) First autopsy study of an Okinawan centenarian: absence of many age related diseases. J Gerontol A Biol Sci Med Sci 59:1195–1199

    PubMed  Google Scholar 

  • Boulétreau-Merle J, Fouillet P, Terrier O (1992) Clinical and seasonal variations in initial retention of virgin Drosophila melanogaster females as a strategy for fitness. Evol Ecol 6:223–242

    Article  Google Scholar 

  • Calabrese EJ (2006) The failure of dose-response models to predict low dose effects: a major challenge for biomedical, toxicological and aging research. Biogerontology 7:117–122

    Article  Google Scholar 

  • Calabrese EJ, Baldwin LA (2000) The effects of gamma rays on longevity. Biogerontology 1:309–319

    Article  PubMed  CAS  Google Scholar 

  • Caratero A, Courtade M, Bennet L, Planel H, Caratero C (1998) Effect of a continuous gamma irradiation at a very low dose on the life span of mice. Gerontology 44:272–276

    Article  PubMed  CAS  Google Scholar 

  • Carey J, Liedo P, Orozco D, Vaupel JW (1992) Slowing of mortality rates at older ages in large Medfly cohorts. Science 258:457–461

    Article  PubMed  CAS  Google Scholar 

  • Carnes BA, Olshansky SJ, Grahn D (2003) Biological evidence for limits to the duration of life. Biogerontology 4:31–45

    Article  PubMed  Google Scholar 

  • Curtsinger JW, Fukui RH, Townsend DR, Vaupel (1992) Demography of genotypes: failure of the limited life-span paradigm in Drosophila melanogaster. Science 258:461–462

    Article  PubMed  CAS  Google Scholar 

  • Darviri C, Tigani X, Demakakos P (2006) Healthy longevity of Greek Centenarians: a quantitative and qualitative exploration of exceptional longevity. 3rd International Conference on Healthy Ageing and Longevity. Melbourne, Abstract p92

  • Demetrius L (2005) Of mice and men. EMBO Reports 6:S39–S44

    Article  PubMed  CAS  Google Scholar 

  • Diamond JM, Hammond KA (1992) Intestinal determinants of muscle performance. Adv Biosciences 84:163–170

    Google Scholar 

  • Dissanayake C (2005) Of stones and health: medical geology in Sri Lanka. Science 309:883–885

    Article  PubMed  CAS  Google Scholar 

  • Dobzhansky T (1973) Nothing in biology makes sense except in the light of evolution. Am Biol Teach, March:125–129

  • Drenos F, Westendorp RGJ, Kirkwood TBL (2006) Trade-off mediated effects on the genetics of human survival caused by increasingly benign living conditions. Biogerontology 7:287–295

    Article  PubMed  Google Scholar 

  • Falkowski PG (2006) Tracing oxygen’s imprint on Earth’s metabolic evolution. Science 311:1724–1725

    Article  PubMed  CAS  Google Scholar 

  • Feinendegen LE (2005) Evidence for beneficial low level radiation effects and hormesis. Brit J Radiol 78:3–7

    Article  PubMed  CAS  Google Scholar 

  • Giess M-C, Planel H (1973) Influence de la radioprotection effectué á différents stades sur la longévité de Drosophila melanogaster. CR Acad Sci Paris 276:1029–1032

    CAS  Google Scholar 

  • Gruenewald TL, Seeman TE, Ryff CD, Karlamangla AS, Singer BH (2006) Combinations of biomarkers predictive of later life mortality. Proc Natl Acad Sci USA 103:14158–14163

    Article  PubMed  CAS  Google Scholar 

  • Heininger K (2001) The deprivation syndrome is the driving force of phylogeny, ontogeny and oncogeny. Rev Neurosciences 12:217–287

    CAS  Google Scholar 

  • Hekimi S, Guarente L (2003) Genetics and the specificity of the aging process. Science 299:1351–1354

    Article  PubMed  CAS  Google Scholar 

  • Hipkiss AR (2003) Errors, mitochondrial dysfunction and ageing. Biogerontology 4:397–400

    Article  PubMed  CAS  Google Scholar 

  • Jazwinski SM (1996) Longevity, genes and aging. Science 273:55–59

    Article  Google Scholar 

  • Jenkins NL, McColl G, Lithgow GJ (2004)Fitness cost and extended lifespan in Caenorhabditis elegans. Proc Roy Soc Lond B 271:2523–2526

    Article  Google Scholar 

  • Kerber RA, Boucher KM, Cawthon RM, O’Brien E (2006) Gene expression profiles predicting life expectancy in humans. 3rd International Conference on Healthy Ageing and Longevity Melbourne. Abstract, pp 76–77

  • Kerber RA, O’Brien E, Smith KR, Cawthon RA (2001) Familial excess longevity in Utah genealogies. J Gerontol Biol Sci 56A:B130–B139

    Google Scholar 

  • Kis-Papo T, Kirzhner V, Wasser SP, Nevo E (2003) Evolution of genomic diversity and sex at extreme environments. Fungal life under hypersaline Dead Sea stress. Proc Nat Acad Sci USA 100:14970–14975

    Article  PubMed  CAS  Google Scholar 

  • Kowald A (2002) Lifespan does not measure ageing. Biogerontology 3:187–190

    Article  PubMed  Google Scholar 

  • Lowenthal GC, Airey PL (2001) Practical applications of radioactivity and nuclear reactions. Cambridge University Press, Cambridge

    Google Scholar 

  • MacDonald IF, Kempster B, Zanette L, MacDougall-Shackleton SA (2006) Early nutritional stress impairs development of a song-control brain region in both male and female juvenile song sparrows (Melospiza melodia) at the onset of song learning. Proc Roy Soc B 273:2559–2564

    Article  Google Scholar 

  • Matheson AC, Parsons PA (1973) The genetics of resistance to long-term exposure to CO2 in Drosophila melanogaster: an environmental stress leading to anoxia. Theoret Appl Genet 43:261–268

    Google Scholar 

  • Meehan B, White NG (eds) (1990) Hunter-gatherer demography: past and present. University of Sydney, Sydney

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Miyazaki S, Nevo E, Grishkan I, Idleman U, Weinberg D, Bohnert HJ (2003) Oxidative stress responses in yeast strains, Saccharomyces cerevisiae, from ‘Evolution Canyon’, Israel. Monatschefte für Chemie 134:1465–1480

    CAS  Google Scholar 

  • Nevo E (2001) Evolution of genome-phenome diversity under environmental stress. Proc Natl Acad Sci USA 98:6233–6240

    Article  PubMed  CAS  Google Scholar 

  • Novoseltsev VN, Novoseltseva J, Yashin AI (2001) A homeostatic model of oxidative damage explains paradoxes observed in earlier experiments: a fusion and extension of older theories of aging. Biogerontology 2:127–138

    Article  PubMed  CAS  Google Scholar 

  • Olsen A, Vantipalli MC, Lithgow GJ (2006) Lifespan extension of Caenorhabditis elegans following repeated mild hormetic treatments. Biogerontology 7:221–230

    Article  PubMed  Google Scholar 

  • Olshansky SJ, Rattan SIS(2005) At the heart of aging: is it metabolic rate or stability? Biogerontology 6:291–295

    Article  PubMed  Google Scholar 

  • Parsons PA (1974) Genetics of resistance to environmental stresses in Drosophila populations. Ann Rev Genet 7:239–265

    Article  Google Scholar 

  • Parsons PA (1982) Adaptive strategies of colonizing animal species. Biol Rev 57:117–148

    Google Scholar 

  • Parsons PA (1992) Evolutionary adaptation and stress: the fitness gradient. Evol Biol 26:191–223

    Google Scholar 

  • Parsons PA (1995) Inherited stress resistance and longevity: a stress theory of ageing. Heredity 75:216–221

    PubMed  Google Scholar 

  • Parsons PA (2002a) Radiation hormesis: challenging LNT theory via ecological and evolutionary considerations. Health Physics 82:513–516

    Article  CAS  Google Scholar 

  • Parsons PA (2002b) Life span: does the limit to survival depend upon metabolic efficiency under stress? Biogerontology 3:233–241

    Article  CAS  Google Scholar 

  • Parsons PA (2003) Energy, stress and the invalid linear no-threshold premise: a generalization illustrated by ionizing radiation. Biogerontology 4:227–231

    Article  PubMed  Google Scholar 

  • Parsons PA (2004) From energy efficiency under stress to rapid development and a long life in natural populations. Biogerontology 5:201–210

    Article  PubMed  Google Scholar 

  • Parsons PA (2005) Environments and evolution: interactions between stress, resource inadequacy and energetic efficiency. Biol Rev 80:589–610

    Article  PubMed  Google Scholar 

  • Parsons PA (2006) Radiation, ecology and the invalid LNT model: the evolutionary imperative. Dose Response 4:191–200

    Article  CAS  PubMed  Google Scholar 

  • Parsons PA (2007a) Survival and longevity improvements at extreme ages: an interpretation assuming an ecological stress theory of aging. Biogerontology 8: (in press)

  • Parsons PA (2007b) Energetic efficiency under stress underlies positive genetic correlations between longevity and other fitness traits in natural populations. Biogerontology 8:55–61

    Article  Google Scholar 

  • Planel H, Soleilhavoup JP, Tixador R, Richoilley G, Conter A, Croute F et al (1987) Influence on cell proliferation of background radiation or exposure to very low chronic gamma-radiation. Health Phys 52:571–578

    Article  PubMed  CAS  Google Scholar 

  • Pollycove M, Feinendegen LE (2001) Biological responses to low doses of ionizing radiation: detriment versus hormesis Part 2. Dose responses of organisms. J Nuclear Medicine 42:26N–37N

    CAS  Google Scholar 

  • Rattan SIS (2004) Aging, anti-aging and hormesis. Mech Ageing Dev 123:285–289

    Article  CAS  Google Scholar 

  • Raymond J, Segre D (2006) The effect of oxygen on biochemical networks and the evolution of complex life. Science 311:1764–1767

    Article  PubMed  CAS  Google Scholar 

  • Rose MR, Rauser CL, Mueller LD, Benford G (2006) A revolution for aging research. Biogerontology 7:269–277

    Article  PubMed  Google Scholar 

  • Rosewell J, Shorrocks B (1987) The implication of survival rates in natural populations of Drosophila: capture-recapture experiments on domestic species. Biol J Linn Soc 32:373–384

    Google Scholar 

  • Snoke MS, Promislow DEL (2003) Quantitative genetic tests of recent senescence theory: age-specific mortality and male fertility in Drosophila melanogaster. Heredity 91:546–556

    Article  PubMed  CAS  Google Scholar 

  • Tubiana M, Aurengo A. Averbeck D, Bonnin A, Le Guen B, Masse R, Monier R, Valleron AJ, de Vathairel F (2005) Dose-effect relationships and estimation of the carcinogenic effect of low doses of ionizing radiation. Académie des Sciences-Académie National de Médecine, Paris, 94 pp

    Google Scholar 

  • Vaupel JW (1988) Inherited frailty and longevity. Demography 25:277–287

    Article  PubMed  CAS  Google Scholar 

  • Vaupel JW (1997) The remarkable improvements in survival at older ages. Proc R Soc Lond B 352:1799–1804

    Article  CAS  Google Scholar 

  • Vaupel JW, Carey JR, Christensen K, Johnson TE, Yashin AI, Holm NV et al (1998) Biodemographic trajectories of longevity. Science 280:855–860

    Article  PubMed  CAS  Google Scholar 

  • Walker DW, McColl G, Jenkins NL, Harris J, Lithgow GJ (2000) Evolution of lifespan in C. elegans. Nature 405:296–297

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Pot D, Kachman SD, Nuzhdin SV, Harshman LG (2006) A quantitative trait locus analysis of natural genetic variation for Drosophila melanogaster oxidative stress survival. J Heredity 97:355–366

    Article  CAS  Google Scholar 

  • Westerman JM, Parsons PA (1973) Variations in genetic architecture at different doses of γ-radiation as measured by longevity in Drosophila melanogaster. Can J Genet Cytol 15:289–298

    PubMed  CAS  Google Scholar 

  • White TCR (1993) The inadequate environment: nitrogen and the abundance of animals. Springer-Verlag, Berlin

    Google Scholar 

  • Willcox DC, Willcox BJ, Todoriki H, Curb JD, Suzuki M (2006a) Caloric restriction and human longevity: what can we learn from the Okinawans? Biogerontology 7:173–177

    Article  Google Scholar 

  • Willcox BJ, Willcox DC, He Q, Curd JD, Suzuki M (2006b) Siblings of Okinawan centenarians share lifelong mortality advantages. J. Gerontol ABiol Sci Med Sci 61:345-

    Google Scholar 

  • Yu BP, Chung HY (2001) Stress resistance by caloric restriction for longevity. NY Acad Sci 928:39–47

    Article  CAS  Google Scholar 

  • Zotin AI (1990) Thermodynamic bases of biological processes: physiological reactions and interactions. Walter de Gruyter, New York

    Google Scholar 

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Acknowledgements

I am grateful to Lee Ehrman for alerting me to some key references, and to Suresh Rattan for encouraging me to participate in the 3rd International Conference on Health Ageing and Longevity in Melbourne in late 2006, and to a reviewer whose comments improved the paper substantially.

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  1. Peter A. Parsons

    Present address: , P.O. Box 906, Unley, SA, 5061, Australia

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  1. La Trobe University, Bundoora, VIC, 3083, Australia

    Peter A. Parsons

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Parsons, P.A. The ecological stress theory of aging and hormesis: an energetic evolutionary model. Biogerontology 8, 233–242 (2007). https://doi.org/10.1007/s10522-007-9080-z

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