Heredity (1995) 75, 216–221; doi:10.1038/hdy.1995.126
Inherited stress resistance and longevity: a stress theory of ageing
Peter A Parsons1
1Department of Genetics and Human Variation, La Trobe University, Bundoora, Vic. 3083, Australia
Correspondence: Peter A Parsons, Faculty of Science and Technology, Griffith University, Qld. 4111, Australia
Received 20 December 1994.
Top of pageAbstract
Ageing is considered in the context of the abiotic stresses to which free-living organisms are normally exposed. Assuming that the primary target of selection of stress is at the level of energy carriers, trade-offs under the rate-of-living theory of ageing predict increased longevity from selection for stress resistance. Changes in longevity then become incidental to selection for stress resistance. I therefore suggest the reformulation of the rate-of-living theory to become a stress theory of ageing. This directly incorporates the characteristics of habitats in nature. Under this theory, the primary trait inherited is resistance to stress. Consequently, at extreme ages those with inherited resistance to abiotic stress should dominate. Furthermore, the reduction in homeostasis manifested by deteriorating ability to adapt to abiotic stress as ageing proceeds, should be slowest in those surviving longest.
Keywords:
abiotic stress, ageing, genetic variability, longevity, stress resistance, trade-off
Top of pageReferences
- Adelman, R, Saul, R L, and Ames, B N. 1988. Oxidation damage to DNA: relation to species metabolic rate and life span. Proc Natl Acad Sci USA, 85, 2706–2708. | Article | PubMed | ChemPort |
- Ames, B N, Shigenaga, M K, and Hagen, T M. 1993. Oxidants, antioxidants, and the degenerative diseases of aging. Proc Natl Acad Sci USA, 90, 7915–7922. | Article | PubMed | ChemPort |
- Arking, R. 1987. Genetic and environmental determinants of longevity in Drosophila. In: Woodhead, A. D. and Thompson, K. H. (eds) Evolution of Longevity in Animals, pp. 1–22. Plenum Press, New York.
- Arking, R, Buck, S, Berrios, A, Dwyer, S, and Baker, G T. III. 1991. Elevated paraquat resistance can be used as a bioassay for longevity in a genetically based long-lived strain of Drosophila. Devi Genet, 12, 362–370.
- Arking, R, and Wells, R A. 1990. Genetic alteration of normal aging processes is responsible for extended longevity in Drosophila. Devi Genet, 11, 141–148.
- Arthur, W. 1987. The Niche in Competition and Evolution. John Wiley, New York.
- Barros, A R, Sierra, L M, and Comendador, M A. 1991. Decreased metabolic rate as an acrolein resistance mechanism in Drosophila melanogaster. Behav Genet, 21, 445–451.
- Buck, S, Wells, R A, Dudas, S P, Baker, G T. III, and Arking, R. 1993. Chromosomal localization and regulation of the longevity determinant genes in a selected strain of Drosophila melanogaster. Heredity, 71, 11–22. | PubMed | ISI |
- Carey, J R, Liedo, P, Orozco, D, and Vaupel, J W. 1992. Slowing of mortality rates at older ages in large medfly cohorts. Science, 258, 457–460. | Article | PubMed | ISI | ChemPort |
- Clare, M J, and Luckinbill, L S. 1985. The effects of gene-environment interaction on the expression of longevity. Heredity, 55, 19–29. | PubMed | ISI |
- Crews, D E. 1993. Biological anthropology and human aging: some current directions in aging research. Ann Rev Anthrop, 22, 395–423.
- Cutler, R G. 1984. Antioxidants, aging, and longevity. In: Pryor, W. A. (ed.) Free Radicals in Biology, V, pp. 371–428. Academic Press, Orlando, FL.
- Diamond, J M, and Hammond, K A. 1992. Intestinal determinants of muscle performance. Adv Biosci, 84, 163–170.
- Dunson, W A, and Travis, J. 1991. The role of abiotic factors in community organization. Am Nat, 138, 1068–1091.
- Engström, G, Liuedahl, L-E, and Björklund, T. 1992. Expression of genetic and environmental variation during ageing 2. Selection for increased lifespan in Drosophila melanogaster. Theor Appl Genet, 85, 26–32.
- Hoffmann, A A, and Parsons, P A. 1989. Selection for increased desiccation resistance in Drosophila melanogaster: additive genetic control and correlated responses for other stresses. Genetics, 122, 837–845. | PubMed |
- Hoffmann, A A, and Parsons, P A. 1991. Evolutionary Genetics and Environmental Stress. Oxford University Press, Oxford.
- Hoffmann, A A, and Parsons, P A. 1993. Selection for adult desiccation resistance in Drosophila melanogaster. fitness components, larval resistance and stress correlations. Biol J Linn Soc, 48, 43–54. | Article |
- Homyk, T, Szidonya, J, and Suzuki, D T. 1980. Behavioral mutants of Drosophila melanogaster. III. Isolation and mapping of mutations by direct visual observations of behavioral phenotypes. Mol Gen Genet, 177, 553–565. | PubMed | ISI |
- Hughes, K A, and Charlesworth, B. 1994. A genetic analysis of senescence in Drosophila. Nature, 367, 64–66. | Article | PubMed | ISI | ChemPort |
- Kenyon, C, Chang, J, Gensch, E, Rudner, A, and Tabtiano, R. 1993. A C. elegans mutant that lives twice as long as wild type. Nature, 366, 461–464. | Article | PubMed | ISI | ChemPort |
- Kirkwood, T B L, and Holliday, R. 1979. The evolution of ageing and longevity. Proc R Soc B, 205, 531–546. | ChemPort |
- Koehn, R K, and Bayne, B I. 1989. Towards a physiological and genetical understanding of the energetics of the stress response. Biol J Linn Soc, 37, 157–171.
- Kohane, M J, and Parsons, P A. 1988. Domestication: evolutionary change under stress. Evol Biol, 23, 31–48.
- Kowald, A, and Kirkwood, T B L. 1994. Towards a network theory of ageing: a model combining the free radical theory and the protein error theory. J Theor Biol, 168, 75–94.
- Langridge, J. 1968. Thermal responses of mutant enzymes and temperature limits to growth. Mol Gen Genet, 103, 116–126. | Article | PubMed | ChemPort |
- Larsen, P L. 1993. Aging and resistance to oxidative damage in Caenorhabditis elegans. Proc Natl Acad Sci USA, 90, 8905–8909. | Article | PubMed | ChemPort |
- Lints, F A, Stoll, J, Gruwez, G, and Lints, C V. 1979. An attempt to select for increased longevity in Drosophila melanogaster. Gerontology, 25, 192–204.
- Luckinbill, L S, Graves, J L, Reed, A H, and Koetsawang, S. 1988. Localizing genes that defer senescence in Drosophila melanogaster. Heredity, 60, 367–374. | PubMed |
- Medvedev, Z A. 1990. An attempt at a rational classification of theories of ageing. Biol Rev, 65, 375–398.
- Miquel, J, Lundgren, P R, Bensch, K G, and Atlan, H. 1976. Effects of temperature on the life span, vitality and fine structure of Drosophila melanogaster. Mech. Ageing Devel, 5, 347–370.
- Naugler, C T, and Leech, S M. 1994. Fluctuating asymmetry and survival ability in the forest tent caterpillar moth Malacosoma disstria: implications for pest management. Entomologia exp appl, 70, 295–298.
- Overgaard, J. 1989. The current and potential role of hyperthermia in radiotherapy. Int J Radiat Oncol Biol Phys, 16, 535–549.
- Parsons, P A. 1978. The genetics of aging in optimal and stressful environments. Exp Geront, 13, 357–363.
- Parsons, P A. 1982. Evolutionary ecology of Australian Drosophila: a species analysis. Evol Biol, 14, 297–350.
- Parsons, P A. 1987. Evolutionary rates under environmental stress. Evol Biol, 21, 311–347.
- Parsons, P A. 1992. Fluctuating asymmetry: a biological monitor of environmental and genomic stress. Heredity, 68, 361–364. | PubMed | ISI |
- Parsons, P A. 1993. The importance and consequences of stress in living and fossil populations: from life-history variation to evolutionary change. Am Nat, 142, S5–S20
- Parsons, P A. 1994. Habitats, stress, and evolutionary rates. J Evol Biol, 7, 387–397.
- Phillips, J P, and Hilliker, A J. 1990. Genetic analysis of oxygen defense mechanisms in Drosophila melanogaster. Adv Genet, 28, 43–71.
- Pieri, C, Falasca, M, Recchioni, R, Moroni, F, and Marcheselli, F. 1992. Diet restriction: a tool to prolong lifespan of experimental animals. Models and current hypotheses of action. Comp Biochem Physiol, 103A, 551–554.
- Riddoch, B J. 1993. The adaptive significance of electro- phoretic mobility in phosphoglucose isomerase (PGI). Biol J Linn Soc, 50, 1–17.
- Rose, M R. 1991. Evolutionary Biology of Aging. Oxford University Press, New York.
- Rose, M R, and Charlesworth, B. 1980. A test of evolutionary theories of senescence. Nature, 287, 141–142. | Article | PubMed | ISI | ChemPort |
- Rose, M R, and Charlesworth, B. 1981. Genetics of life history in Drosophila melanogaster. II. Exploratory selection experiments. Genetics, 97, 187–196. | PubMed | ISI | ChemPort |
- Schächter, F, Faure-Delanef, L, Guénot, F, Rouger, H, Froguel, P, Ginot, L, and Cohen, D. 1994. Genetic associations with human longevity at the APOE and ACE loci. Nature Genetics, 6, 29–32. | Article | PubMed |
- Schnebel, E M, and Grossfield, J. 1988. Antagonistic pleio-tropy: an interspecific Drosophila comparison. Evolution, 42, 306–311.
- Sohal, R S. 1985. Aging in insects. In: Kerkut, G. A. and Gilbert, L. I. (eds) Comprehensive Insect Physiology, Biochemistry and Pharmacology, 10, pp. 595–631. Pergamon Press, Oxford.
- Sohal, R S. 1986. The rate of living theory: a contemporary interpretation. In: Collatz, K. G. and Sohal, R. S. (eds) Insect Aging, pp. 23–44. Springer-Verlag, Berlin.
- Templeton, A R, Crease, T J, and Shah, F. 1985. The molecular through ecological genetics of abnormal abdomen in Drosophila mercatorum. I. Basic genetics. Genetics, 111, 805–818. | PubMed | ChemPort |
- Thoday, J M. 1958. Homeostasis in a selection experiment. Heredity, 12, 401–415.
- Tyler, R H, Brar, H, Singh, M, Latorre, A, Graves, J L, Mueller, L D, Rose, M R, and Ayala, F J. 1993. The effect of superoxide dismutase alleles on aging in Drosophila. Genetica, 91, 143–149. | PubMed | ISI | ChemPort |
- Vanfleteren, J. 1993. Oxidative stress and aging in Caenorhabditis elegans. Biochem J, 292, 605–608. | PubMed | ISI | ChemPort |
- Vaupel, J W. 1988. Inherited frailty and longevity. Demography, 25, 277–287.
- Watt, W B. 1983. Adaptation at specific loci. II. Demographic and biochemical elements in the maintenance of the Colias PGI polymorphism. Genetics, 103, 691–724.
- Westerman, J M, and Parsons, P A. 1973. Variation in genetic architecture at different doses of
-radiation as measured by longevity in Drosophila melanogaster. Can J Genet Cytol, 15, 289–298. - White, E B, Debach, P, and Garber, M J. 1970. Artificial selection for genetic adaptation to temperature extremes in Aphytis lingnanensis (Hymenoptera: Aphelinidae). Hilgardia, 40, 161–192.
- Williams, G C. 1957. Pleiotropy, natural selection, and the evolution of senescence. Evolution, 11, 398–411. | Article | ISI |
- Yonemura, I, Motoyama, T, and Hasekura, H. 1989. Mode of inheritance of major genes controlling life span differences between two inbred strains of Drosophila melanogaster. Hereditas, 111, 207–214.