Abstract
Progressive deterioration in performance with age is what we refer to as senescence or ageing. It varies greatly among species, but also among conspecific individuals because of the influence of genetic, environmental and stochastic factors. The recent emergence of long-term field studies has provided widespread evidence that animals in nature do senesce, a finding that has opened new horizons for research on causes and consequences of senescence. Empirical evidence is often supportive of the prediction that long-lived species produce less reactive species, have lower oxidative damage levels and antioxidants and have molecules more resistant to oxidative damage. However, full understanding of mechanisms underlying ageing is still elusive. This chapter reviews briefly the main mechanistic and evolutionary theories of senescence that may be linked to oxidative stress, and discusses comparative studies that tested the link between oxidative status parameters and senescence. The chapter ends with an examination of how mild doses of oxidative stress or other forms of stress experienced during sensitive windows of life may increase longevity through hormetic mechanisms.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abele D, Brey T, Philipp E (2009) Bivalve models of aging and the determination of molluscan lifespans. Exp Geront 44:307–315
Aledo JC, Li Y, De Magalhães JP, Ruíz-Camacho M, Pérez-Claros JA (2011) Mitochondrially encoded methionine is inversely related to longevity in mammals. Aging Cell 10:198–207
Andrews AB, Horvath TL (2009) Uncoupling protein-2 regulates lifespan in mice. Amer J Physiol Endocrinol Metab 296:E621–E627
Andziak B, O’Connor TB, Buffenstein R (2005) Antioxidants do not explain the disparate longevity between mice and the longest-living rodent, the naked mole rat. Mech Ageing Dev 126:1206–1212
Andziak B, O’Connor TP, Qi W, DeWaal EM, Pierce A, Chaudhuri AR, Van Remmen H, Buffenstein R (2006) High oxidative damage levels in the longest-living rodent, the naked mole rat. Aging Cell 5:463–471
Angelier F, Vleck CM, Holberton RL, Marra PP (2013) Telomere length, non-breeding habitat and return rate in male American redstarts. Funct Ecol 27:342–350
Archer CR, Sakaluk SK, Selman C, Royle NJ, Hunt J (2013) Oxidative stress and the evolution of sex differences in life span and ageing in the decorated cricket, Gryllodes sigillatus. Evolution 67:620–634
Argüelles S, García S, Maldonado M, Machado A, Ayala A (2004) Do the serum oxidative stress biomarkers provide a reasonable index of the general oxidative stress status? Biochim Biophys Acta 1674:251–259
Austad SN (1993) Retarded senescence in an insular population of Virginia opossums (Didelphis virginiana). J Zool 229:695–708
Barja G (2013) Updating the mitochondrial free radical theory of aging: an integrated view, key aspects and confounding concepts. Antioxid Redox Signal 19:1420–1445
Beaulieu M, Reichert S, Le Maho Y, Ancel A, Criscuolo F (2011) Oxidative status and telomere length in a long-lived bird facing a costly reproductive event. Funct Ecol 25:577–585
Beaulieu M, Thierry AM, González-Acuña D, Polito MJ (2013) Integrating oxidative ecology into conservation physiology. Conser Physiol 1:cot004
Beckman KB, Ames BN (1998) The free radical theory of aging matures. Physiol Rev 78:547–581
Begum S, Basova L, Strahl J, Sukhotin A, Heilmayer O, Philipp E, Brey T, Abele D (2009) A metabolic model for the ocean quahog Arctica islandica—Effects of animal mass and age, temperature, salinity and geography on respiration rate. J Shellfish Res 28:1–7
Bender A, Hajieva P, Moosmann B (2008) Adaptive antioxidant methionine accumulation in respiratory chain complexes explains the use of a deviant genetic code in mitochondria. Proc Natl Acad Sci USA 105:16496–16501
Bize P, Devevey G, Monaghan P, Doligez B, Christe P (2008) Fecundity and survival in relation to resistance to oxidative stress in a free-living bird. Ecology 89:2584–2593
Bize P, Criscuolo F, Metcalfe NB, Nasir L, Monaghan P (2009) Telomere dynamics rather than age predict life expectancy in the wild. Proc R Soc Lond B 276:1679–1683
Bjelland S, Seeberg E (2003) Mutagenicity, toxicity and repair of DNA base damage induced by oxidation. Mutat Res 531:37–80
Blanco MA, Sherman PW (2005) Maximum longevities of chemically protected and non-protected fishes, reptiles, and amphibians support evolutionary hypotheses of aging. Mech Ageing Dev 126:794–803
Bouwhuis S, Charmantier A, Verhulst S, Sheldon BC (2010) Individual variation in rates of senescence: natal origin effects and disposable soma in a wild bird population. J Anim Ecol 79:1251–1261
Brand MD (2000) Uncoupling to survive? The role of mitochondrial inefficiency in ageing. Exp Geront 35:811–820
Brand MD, Turner N, Ocloo A, Else PL, Hulbert AJ (2003) Proton conductance and fatty acyl composition of liver mitochondria correlates with body mass in birds. Biochem J 376:741–748
Brenner RR (1984) Effect of unsaturated fatty acids on membrane structure and enzyme kinetics. Prog Lipid Res 23:69–96
Brink TC, Demetrius L, Lehrach H, Adjaye J (2009) Age-related transcriptional changes in gene expression in different organs of mice support the metabolic stability theory of aging. Biogerontology 10:549–564
Brunet-Rossinni AK (2004) Reduced free-radical production and extreme longevity in the little brown bat (Myotis lucifugus) versus two non-flying mammals. Mech Ageing Dev 125:11–20
Buffenstein R (2005) The naked mole rat: a new long-living model for human aging research? J Geront Ser A 60:1369–1377
Butler PG Jr, Wanamaker AD, Scourse JD, Richardson CA, Reynolds DJ (2013) Variability of marine climate on the North Icelandic Shelf in a 1357-year proxy archived based on growth increments in the bivalve Arctica islandica. Palaeogeogr Palaeocl 373:141–151
Buttemer W, Battam H, Hulbert AJ (2008) Fowl play and the price of petrel: long-living Procellariformes have peroxidation resistant membrane composition compared with short-living Galliformes. Biol Lett 4:351–354
Buttemer W, Abele D, Costantini D (2010) From bivalves to birds: oxidative stress and longevity. Funct Ecol 24:971–983
Calabrese EJ (2013) Low doses of radiation can enhance insect lifespans. Biogerontology 14:365–381
Caratero A, Courtade M, Bonnet L, Planel H, Caratero C (1998) Effect of continuous gamma irradiation at a very low dose on the life span of mice. Gerontology 44:272–276
Carranza J, Alarcos S, Sánchez-Prieto CB, Valencia J, Mateos C (2004) Disposable-soma senescence mediated by sexual selection in an ungulate. Nature 432:215–218
Casagrande S, Dell’Omo G, Costantini D, Tagliavini J, Groothuis T (2011) Variation of a carotenoid-based trait in relation to oxidative stress and endocrine status during the breeding season in the Eurasian kestrel: a multi-factorial study. Comp Biochem Physiol Part A 160:16–26
Chaudhuri AR, de Waal EM, Pierce A, van Remmen H, Ward WF, Richardson A (2006) Detection of protein carbonyls in aging liver tissue: a fluorescence-based proteomic approach. Mech Ageing Dev 127:849–861
Clutton-Brock TH, Isvaran K (2007) Sex differences in ageing in natural populations of vertebrates. Proc R Soc Lond B 274:3097–3104
Cohen AA, McGraw KJ, Wiersma P, Williams JB, Robinson WD, Robinson TR, Brawn JD, Ricklefs RE (2008) Interspecific associations between circulating antioxidant levels and life-history variation in birds. Am Nat 172:178–193
Cohen AA, Milot E, Yong J, Seplaki CL, Fülöp T, Bandeen-Roche K, Fried LP (2013) A novel statistical approach shows evidence for multi-system physiological dysregulation during aging. Mech Ageing Dev 134:110–117
Costantini D, Dell’Omo G, De Filippis PS, Marquez C, Snell H, Snell H, Tapia W, Brambilla G, Gentile G (2009) Temporal and spatial covariation of gender and oxidative stress in the Galápagos land iguana Conolophus subcristatus. Physiol Biochem Zool 82:430–437
Costantini D (2010) Effects of diet quality on serum oxidative status and body mass in male and female pigeons during reproduction. Comp Biochem Physiol Part A 156:294–299
Costantini D, Marasco V, Moller AP (2011) A meta-analysis of glucocorticoids as modulators of oxidative stress in vertebrates. J Comp Physiol B 181:447–456
Costantini D, Ferrari C, Pasquaretta C, Cavallone E, Carere C, von Hardenberg A, Réale D (2012) Interplay between plasma oxidative status, cortisol and coping styles in wild alpine marmots, Marmota marmota. J Exp Biol 215:374–383
Costantini D, Monaghan P, Metcalfe N (2014) Prior hormetic priming is costly under environmental mismatch. Biol Lett (in press)
Cracraft J (1987) DNA hybridization and avian phylogenetics. Evol Biol 21:47–96
Criscuolo F, Font-Sala C, Bouillaud F, Poulin N, Trabalon M (2010) Increased ROS production: a component of the longevity equation in the male Mygalomorph, Brachypelma albopilosa. PLoS One 5:e13104
Csermely P, Soti C (2006) Cellular networks and the aging process. Arch Physiol Biochem 112:60–64
Cypser JR, Johnson TE (2002) Multiple stressors in Caenorhabditis elegans induce stress hormesis and extended longevity. J Gerontol A 57:B109–B114
Dagg AI (2009) The social behavior of older animals. The Johns Hopkins University Press, USA
De Coster G, De Neve L, Verhulst S, Lens L (2012) Maternal effects reduce oxidative stress in female nestlings under high parasite load. J Avian Biol 43:177–185
De Loof A, De Haes W, Boerjan B, Schoofs L (2013) The fading electricity theory of ageing: the missing biophysical principle? Ageing Res Rev 12:58–66
de Magalhães JP, Cabral JA, Magalhães D (2005) The influence of genes on the aging process of mice: a statistical assessment of the genetics of aging. Genetics 169:265–274
de Magalhães JP, Costa J, Church GM (2007) An analysis of the relationship between metabolism, developmental schedules, and longevity using phylogenetic independent contrasts. J Geront A 62:149–160
Descamps S, Boutin S, Berteaux D, Gaillard JM (2006) Best squirrels trade a long life for an early reproduction. Proc R Soc Lond B 273:2369–3237
Du C, Anderson A, Lortie M, Parsons R, Bodnar A (2013) Oxidative damage and cellular defense mechanisms in sea urchin models of aging. Free Radic Biol Med 63C:254–263
Epel ES, Blackburn EH, Lin J, Dhabhar FS, Adler NE, Morrow JD, Cawthon RM (2004) Accelerated telomere shortening in response to life stress. Proc Natl Acad Sci USA 101:17312–17315
Filho DW, Althoff SL, Dafré AL, Boveris A (2007) Antioxidant defenses, longevity and ecophysiology of South American bats. Comp Biochem Physiol Part C 146:214–220
Finch CE, Pike MC (1996) Maximum life span predictions from the Gompertz mortality model. J Gerontol A 51:B183–B194
Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408:239–247
Francis N, Gregg T, Owen R, Ebert T, Bodnar A (2006) Lack of age-associated telomere shortening in long-lived and short-lived species of sea urchins. FEBS Lett 580:4713–4717
Freeman-Gallant CR, Amidon J, Berdy B, Wein S, Taff CC, Haussmann MF (2011) Oxidative damage to DNA related to survivorship and carotenoid-based sexual ornamentation in the common yellowthroat. Biol Lett 7:429–432
Furness LJ, Speakman JR (2008) Energetics and longevity in birds. Age 30:75–87
Gems D, Guardia YD (2013) Alternative perspectives on aging in Caenorhabditis elegans: reactive oxygen species or hyperfunction? Antioxid Redox Signal 19:321–329
Gems D, Partridge L (2013) Genetics of longevity in model organisms: debates and paradigm shifts. Annu Rev Physiol 75:621–644
Gershman R, Gilbert DL, Nye F, Dwyer P, Fenw MV (1954) Oxygen poisoning and X-irradiation: a mechanism in common. Science 119:623–626
Gorbunova V, Seluanov A (2009) Coevolution of telomerase activity and body mass in mammals: from mice to beavers. Mech Ageing Dev 130:3–9
Guerra C, Zenteno-Savín T, Maeda-Martínez AN, Philipp EE, Abele D (2012) Changes in oxidative stress parameters in relation to age, growth and reproduction in the short-lived catarina scallop Argopecten ventricosus reared in its natural environment. Comp Biochem Physiol Part A 162:421–430
Hall ME, Nasir L, Daunt F, Gault EA, Croxall JP, Wanless S, Monaghan P (2004) Telomere loss in relation to age and early environment in long-lived birds. Proc R Soc Lond B 271:1571–1576
Han ES, Muller FL, Pérez VI, Qi W, Liang H, Xi L, Fu C, Doyle E, Hickey M, Cornell J, Epstein CJ, Roberts LJ, Van Remmen H, Richardson A (2008) The in vivo gene expression signature of oxidative stress. Physiol Genom 34:112–126
Harley CB, Futcher AB, Greider CW (1990) Telomeres shorten during ageing of human fibroblasts. Nature 345:458–460
Harman D (1956) Aging: a theory based on free radical and radiation chemistry. J Gerontol A 11:298–300
Harman D (1972) The biologic clock: the mitochondria? J Am Ger Soc 20:145–147
Harper JM, Wang M, Galecki AT, Ro J, Williams JB, Miller RA (2011) Fibroblasts from long-lived bird species are resistant to multiple forms of stress. J Exp Biol 214:1902–1910
Hatakeyama H, Nakamura KI, Izumiyama-Shimomura N, Ishii A, Tsuchida S, Takubo K, Ishikawa N (2008) The teleost Oryzias latipes shows telomere shortening with age despite considerable telomerase activity throughout life. Mech Ageing Dev 129:550–557
Haussmann MF, Winkler DW, Vleck CM (2005) Longer telomeres associated with higher survival in birds. Biol Lett 1:212–214
Haussmann MF, Winkler DW, Huntington CE, Nisbet ICT, Vleck CM (2007) Telomerase activity is maintained throughout the lifespan of long-lived birds. Exp Geront 42:610–618
Haussmann MF, Marchetto NM (2010) Telomeres: linking stress and survival, ecology and evolution. Curr Zool 56:714–727
Hayflick L (1965) The limited in vitro lifetime of human diploid cell strains. Exp Cell Res 37:614–636
Heidinger BJ, Blount JD, Boner W, Griffiths K, Metcalfe NB, Monaghan P (2012) Telomere length in early life predicts lifespan. Proc Natl Acad Sci USA 109:1743–1748
Herndon LA, Schmeissner PJ, Dudaronek JM, Brown PA, Listner KM, Sakano Y, Paupard MC, Hall DH, Driscoll M (2002) Stochastic and genetic factors influence tissue-specific decline in ageing C. elegans. Nature 419:808–814
Herrero A, Barja G (1997a) ADP-regulation of mitochondrial free radical production is different with complex I- and complex II-linked substrates: implications for the exercise paradox and brain hypermetabolism. J Bioener Biomembr 29:241–249
Herrero A, Barja G (1997b) Sites and mechanisms responsible for the low rate of free radical production of heart mitochondria in the long-lived pigeon. Mech Ageing Dev 98:95–111
Herrero A, Barja G (1998) H2O2 production of heart mitochondria and aging rate are slower in canaries and parakeets than in mice: sites of free radical generation and mechanisms involved. Mech Ageing Dev 103:133–146
Holman RT (1954) Autoxidation of fats and related substances. In: Holman RT, Lundberg WO, Malkin T (eds) Progress in chemistry of fats and other lipids, vol 2. Pergamon Press, London, pp 51–98
Hornsby PJ (2003) Replicative senescence of human and mouse cells in culture: significance for aging research. Mech Ageing Dev 124:853–855
Houben JMJ, Moonen HJJ, van Schooten FJ, Hageman GJ (2008) Telomere length assessment: biomarker of chronic oxidative stress? Free Rad Biol Med 44:235–246
Hulbert AJ (2005) On the importance of fatty acid composition of membranes for aging. J Theor Biol 234:277–288
Hulbert AJ (2008) Explaining longevity of different animals: is membrane fatty acid composition the missing link? Age 30:89–97
Hulbert AJ, Rana T, Couture P (2002a) The acyl composition of mammalian phospholipids: an allometric analysis. Comp Biochem Physiol Part B 132:515–527
Hulbert AJ, Faulks S, Buttemer WA, Else PL (2002b) Acyl composition of muscle membranes varies with body size in birds. J Exp Biol 205:3561–3569
Hulbert AJ, Faulks SC, Buffenstein R (2006) Oxidation-resistant membrane phospholipids can explain longevity differences among the longest-living rodents and similarly-sized mice. J Gerontol 61:1009–1018
Hulbert AJ, Pamplona R, Buffenstein R, Buttemer WA (2007) Life and death: metabolic rate, membrane composition, and life span of animals. Physiol Rev 87:1175–1213
Hulbert AJ, Beard LA, Grigg GC (2008) The exceptional longevity of an egg-laying mammal, the short-beaked echidna (Tachyglossus aculeatus) is associated with peroxidation-resistant membrane composition. Exp Geront 43:729–733
Ilmonen P, Kotrschal A, Penn DJ (2008) Telomere attrition due to infection. PLoS ONE 3:e2143
Isaksson C (2010) Pollution and its impact on wild animals: a meta-analysis on oxidative stress. EcoHealth 7:342–350
Isaksson C, While GM, Olsson M, Komdeur J, Wapstra E (2011) Oxidative stress physiology in relation to life history traits of a free-living vertebrate: the spotted snow skink, Niveoscincus ocellatus. Integr Zool 6:140–149
Issartel J, Hervant F, de Fraipont M, Clobert J, Voituron Y (2009) High anoxia tolerance in the subterranean salamander Proteus anguinus without oxidative stress nor activation of antioxidant defenses during reoxygenation. J Comp Physiol B 179:543–551
Jennings BJ, Ozanne SE, Dorling MW, Hales CN (1999) Early growth determines longevity in male rats and may be related to telomere shortening in the kidney. FEBS Lett 448:4–8
Jobson RW, Nabholz B, Galtier N (2010) An evolutionary genome scan for longevity-related natural selection in mammals. Mol Biol Evol 27:840–847
Jones DP (2006) Redefining oxidative stress. Antiox Redox Signal 8:1865–1879
Jones OR, Gaillard JM, Tuljapurkar S, Alho JS, Armitage KB, Becker PH, Bize P, Brommer J, Charmantier A, Charpentier M, Clutton-Brock T, Dobson FS, Festa-Bianchet M, Gustafsson L, Jensen H, Jones CG, Lillandt BG, McCleery R, Merilä J, Neuhaus P, Nicoll MA, Norris K, Oli MK, Pemberton J, Pietiäinen H, Ringsby TH, Roulin A, Saether BE, Setchell JM, Sheldon BC, Thompson PM, Weimerskirch H, Jean Wickings E, Coulson T (2008) Senescence rates are determined by ranking on the fast-slow life-history continuum. Ecol Lett 11:664–673
Jones OR, Scheuerlein A, Salguero-Gómez R, Camarda CG, Schaible R, Casper BB, Dahlgren JP, Ehrlén J, García MB, Menges ES, Quintana-Ascencio PF, Caswell H, Baudisch A, Vaupel JW (2014) Diversity of ageing across the tree of life. Nature 505:169–173
Kamper EF, Chatzigeorgiou A, Tsimpoukidi O, Kamper M, Dalla C, Pitychoutis PM, Papadopoulou-Daifoti Z (2009) Sex differences in oxidant/antioxidant balance under a chronic mild stress regime. Physiol Behav 98:215–222
Keipert S, Voigt A, Klaus S (2011) Dietary effects on body composition, glucose metabolism, and longevity are modulated by skeletal muscle mitochondrial uncoupling in mice. Aging Cell 10:122–136
Keipert S, Ost M, Chadt A, Voigt A, Ayala V, Portero-Otin M, Pamplona R, Al-Hasani H, Klaus S (2013) Skeletal muscle uncoupling-induced longevity in mice is linked to increased substrate metabolism and induction of the endogenous antioxidant defense system. Am J Physiol Endocrinol Metab 304:E495–E506
Kern B, Ivanina AV, Piontkivska H, Sokolov EP, Sokolova IM (2009) Molecular characterization and expression of a novel homolog of uncoupling protein 5 (UCP5) from the eastern oyster Crassostrea virginica (Bivalvia: Ostreidae). Comp Biochem Physiol Part D 4:121–127
Kirkwood TBL (1977) Evolution of ageing. Nature 270:301–304
Kirkwood TBL, Rose MR (1991) Evolution of senescence: late survival sacrificed for reproduction. Phil Trans R Soc Lond B 332:15–24
Kirkwood TBL, Feder M, Finch CE, Franceschi C, Globerson A, Klingenberg CP, LaMarco K, Omholt S, Westendorp RGJ (2005) What accounts for the wide variation in life span of genetically identical organisms reared in a constant environment? Mech Ageing Dev 126:439–443
Klepsatel P, Gáliková M, De Maio N, Ricci S, Schlötterer C, Flatt T (2013) Reproductive and post-reproductive life history of wild-caught Drosophila melanogaster under laboratory conditions. J Evol Biol 26:1508–1520
Koivula MJ, Kanerva M, Salminen JP, Nikinmaa M, Eeva T (2011) Metal pollution indirectly increases oxidative stress in great tit (Parus major) nestlings. Environ Res 111:362–370
Kotrschal A, Ilmonen P, Penn DJ (2007) Stress impacts telomere dynamics. Biol Lett 3:128–130
Kowald A, Kirkwood TBL (1996) A network theory of ageing: the interactions of defective mitochondria, aberrant proteins, free radicals and scavengers in the ageing process. Mutat Res 316:209–236
Kowald A (2002) Lifespan does not measure ageing. Biogerontology 3:187–190
Lagisz M, Hector KL, Nakagawa S (2013) Life extension after heat shock exposure: assessing meta-analytic evidence for hormesis. Ageing Res Rev 12:653–660
Lambert AJ, Boysen HM, Buckingham JA, Yang T, Podlutsky A, Austad SN, Kunz TH, Buffenstein R, Brand MD (2007) Low rates of hydrogen peroxide production by isolated heart mitochondria associate with long maximum lifespan in vertebrate homeotherms. Aging Cell 6:607–618
Lanner RM, Connor KF (2001) Does bristlecone pine senesce? Exp Geront 36:675–685
Le Bourg E (2005) Hormetic protection of Drosophila melanogaster middle-aged male flies from heat stress by mildly stressing them at young age. Naturwissenschaften 92:293–296
Lebovitz RM, Zhang H, Vogel H, Cartwright J, Dionne L, Lu N, Huang S, Matzuk MM (1996) Neurodegradation, myocardial injury, and perinatal death in mitochondrial superoxide dismutase-deficient mice. Proc Natl Acad Sci USA 93:9782–9787
Lionaki E, Markaki M, Tavernarakis N (2013) Autophagy and ageing: insights from invertebrate model organisms. Ageing Res Rev 12:413–428
Lopez-Torres M, Perez-Campo R, Rojas C, Cadenas S, Barja G (1993) Maximum lifespan in vertebrates: relationship with liver antioxidant enzymes, glutathione system, ascorbate, urate, sensitivity to peroxidation, true malondialdehyde, in vivo H2O2, and basal and maximum aerobic capacity. Mech Ageing Dev 70:177–199
Loschen G, Flohé L, Chance B (1971) Respiratory chain linked H2O2 production in pigeon heart mitochondria. FEBS Lett 18:261–264
Losdat S, Helfenstein F, Blount JD, Marri V, Maronde L, Richner H (2013) Nestling erythrocyte resistance to oxidative stress predicts fledging success but not local recruitment in a wild bird. Biol Lett 9:20120888
Lund TC, Glass TJ, Tolar J, Blazar BR (2009) Expression of telomerase and telomere length are unaffected by either age or limb regeneration in Danio rerio. PLoS ONE 4:e7688
Maklakov AA, Fricke C, Arnqvist G (2007) Sexual selection affects lifespan and aging in the seed beetle. Aging Cell 6:739–744
Maklakov AA, Lummaa V (2013) Evolution of sex differences in lifespan and aging: causes and constraints. BioEssays 35:717–724
Martin JG, Festa-Bianchet M (2011) Age-independent and age-dependent decreases in reproduction of females. Ecol Lett 14:576–581
Martinez DE (1998) Mortality patterns suggest lack of senescence in hydra. Exp Geront 33:217–225
Medawar PB (1952) An unsolved problem of biology. HK Lewis and Co
Melov S, Schneider JA, Day BJ, Hinerfeld D, Coskun P, Mirra SS, Crapo JD, Wallace DC (1998) A novel neurological phenotype in mice lacking mitochondrial manganese superoxide dismutase. Nat Genet 18:159–163
Melov S, Coskun P, Patel M, Tuinstra R, Cottrell B, Jun AS, Zastawny TH, Dizdaroglu M, Goodman SI, Huang TT, Miziorko H, Epstein CJ, Wallace DC (1999) Mitochondrial disease in superoxide dismutase 2 mutant mice. Proc Natl Acad Sci USA 96:846–851
Miquel J, Economos AC, Fleming J, Johnson JE Jr (1980) Mitochondrial role in cell aging. Exp Geront 15:579–591
Moe B, Rønning B, Verhulst S, Bech C (2009) Metabolic ageing in individual zebra finches. Biol Lett 5:86–89
Møller AP (2006) Sociality, age at first reproduction and senescence: comparative analyses of birds. J Evol Biol 19:682–689
Møller AP (2008) Relative longevity and field metabolic rate in birds. J Evol Biol 21:1379–1386
Møller AP, de Lope F, Saino N (2005) Reproduction and migration in relation to senescence in the barn swallow Hirundo rustica: a study of avian ‘centenarians’. Age 27:307–318
Monaghan P, Haussmann MF (2006) Do telomere dynamics link lifestyle and lifespan? Trends Ecol Evol 21:47–53
Monaghan P, Charmantier A, Nussey DH, Ricklefs RE (2008) The evolutionary ecology of senescence. Funct Ecol 22:371–378
Monaghan P (2010) Telomeres and life histories: the long and the short of it. Ann NY Acad Sci 1206:130–142
Montgomery MK, Hulbert AJ, Buttemer WA (2011) The long life of birds: the rat-pigeon comparison revisited. PLoS ONE 6:e24138
Montgomery MK, Hulbert AJ, Buttemer WA (2012) Does the oxidative stress theory of aging explain longevity differences in birds? I. Mitochondrial ROS production. Exp Geront 47:203–210
Moosmann B, Behl C (2008) Mitochondrially encoded cysteine predicts animal lifespan. Aging Cell 7:32–46
Munro D, Pichaud N, Paquin F, Kemeid V, Blier PU (2013) Low hydrogen peroxide production in mitochondria of the long-lived Arctica islandica: underlying mechanisms for slow aging. Aging Cell 12:584–592
Munshi-South J, Wilkinson GS (2006) Diet influences life span in parrots. Auk 123:108–118
Nabholz B, Glémin S, Galtier N (2008) Strong variations of mitochondrial mutation rate across mammals—the longevity hypothesis. Mol Biol Evol 25:120–130
Nakagawa S, Gemmell NJ, Burke T (2004) Measuring vertebrate telomeres: applications and limitations. Mol Ecol 13:2523–2533
Noguera JC, Kim S-Y, Velando A (2011) Pre-fledgling oxidative damage predicts recruitment in a long-lived bird. Biol Lett 8:61–63
Norte AC, Ramos JA, Araújo PM, Sousa JP, Sheldon BC (2008) Health-state variables and enzymatic biomarkers as survival predictors in nestling great tits (Parus major): effects of environmental conditions. Auk 125:1–11
Nussey DH, Kruuk LEB, Donald A, Fowlie M, Clutton-Brock TH (2006) The rate of senescence in maternal performance increases with early-life fecundity in red deer. Ecol Lett 9:1342–1350
Nussey DH, Kruuk LEB, Morris A, Clutton-Brock TH (2007) Environmental conditions in early life influence ageing rates in a wild population of red deer. Curr Biol 17:R1000–R1001
Nussey DH, Coulson T, Festa-Bianchet M, Gaillard JM (2008) Measuring senescence in wild animal populations: towards a longitudinal approach. Funct Ecol 22:393–406
Nussey DH, Kruuk LE, Morris A, Clements MN, Pemberton JM, Clutton-Brock TH (2009) Inter- and intrasexual variation in aging patterns across reproductive traits in a wild red deer population. Am Nat 174:342–357
Nussey DH, Froy H, Lemaitre J-F, Gaillard J-M, Austad SN (2013) Senescence in natural populations of animals: widespread evidence and its implications for bio-gerontology. Ageing Res Rev 12:214–225
O’Connor TP, Lee A, Jarvis JU, Buffenstein R (2002) Prolonged longevity in naked mole rats: age-related changes in metabolism, body composition and gastrointestinal function. Comp Biochem Physiol Part A 133:835–842
Ogburn CE, Carlberg K, Ottinger MA, Holmes DJ, Martin GM, Austad SN (2001) Exceptional cellular resistance to oxidative damage in long-lived birds requires active gene expression. J Gerontol A 56:468–474
Pamplona R (2008) Membrane phospholipids, lipoxidative damage and molecular integrity: a causal role in aging and longevity. Biochim Biophys Acta-Bioenerg 1777:1249–1262
Pamplona R, Barja G (2003) Aging rate, free radical production, and constitutive sensitivity to lipid peroxidation: insights from comparative studies. In: Van Zglinicki T (ed) Biology of aging and its modulation series. Aging at the molecular level, vol 1. Kluwer Academic Publisher, New York, pp 47–64
Pamplona R, Costantini D (2011) Molecular and structural antioxidant defences against oxidative stress in animals. Am J Physiol 301:R843–R863
Pamplona R, Barja G, Portero-Otin M (2002) Membrane fatty acid unsaturation, protection against oxidative stress, and maximum life span: a homeoviscous-longevity adaptation? Ann NY Acad Sci 959:475–490
Pamplona R, Prat J, Cadenas S, Rojas C, Perez-Campo R, Lopez-Torres M, Barja G (1996) Low fatty acid unsaturation protects against lipid peroxidation in liver mitochondria from long-lived species: the pigeon and the human case. Mech Ageing Dev 86:53–66
Passos JF, Saretzki G, Ahmed S, Nelson G, Richter T, Peters H, Wappler I, Birket MJ, Harold G, Schaeuble K, Birch-Machin MA, Kirkwood TB, von Zglinicki T (2007) Mitochondrial dysfunction accounts for the stochastic heterogeneity in telomere-dependent senescence. PLoS Biol 5:e110
Pauliny A, Wagner RH, Augustin J, Szep T, Blomqvist D (2006) Age-independent telomere length predicts fitness in two bird species. Mol Ecol 15:1681–1687
Pearl R (1928) The rate of living. Alfred A. Knopf, New York
Pérez VI, Buffenstein R, Masamsetti V, Leonard S, Salmon AB, Mele J, Andziak B, Yang T, Edrey Y, Friguet B, Ward W, Richardson A, Chaudhuri A (2009) Protein stability and resistance to oxidative stress are determinants of longevity in the longest-living rodent, the naked mole rat. Proc Natl Acad Sci USA 106:3059–3064
Perez-Campo R, Lopez-Torres M, Rojas C, Cadenas S, Barja G (1994) Longevity and antioxidant enzymes, non-enzymatic antioxidants and oxidative stress in the vertebrate lung: a comparative study. J Comp Physiol B 163:682–689
Peterson RO, Vucetich JA, Fenton G, Drummer TD, Spencer Larsen C (2010) Ecology of arthritis. Ecol Lett 13:1124–1128
Philipp E, Brey T, Heilmayer O, Abele D, Pörtner HO (2006) Physiological ageing in a polar and a temperate swimming scallop. Mar Ecol Prog Ser 307:187–198
Philipp EER, Strahl J, Sukhotin AA (2012) Aging in marine animals. In: Abele D, Vázquez-Medina JP, Zenteno-Savín T (eds) Oxidative stress in aquatic ecosystems. Wiley-Blackwell, UK, pp 193–207
Porter RK, Brand MD (1993) Body mass dependence of H+ leak in mitochondria and its relevance to metabolic rate. Nature 362:628–630
Rattan SIS (2008) Hormesis in aging. Ageing Res Rev 7:63–78
Reed T, Kruuk LEB, Wanless S, Frederiksen M, Cunningham EJM, Harris MP (2008) Reproductive senescence in a long-lived seabird: rates of decline in late life performance are associated with varying costs of early reproduction. Am Nat 171:E89–E101
Reynolds RM, Phillips PC (2013) Natural variation for lifespan and stress response in the nematode Caenorhabditis remanei. PLoS ONE 8:e58212
Reznick D, Bryant M, Holmes D (2006) The evolution of senescence and post-reproductive lifespan in guppies (Poecilia reticulata). PLoS Biol 4:e7
Ricklefs RE (2010) Life-history connections to rates of aging in terrestrial vertebrates. Proc Natl Acad Sci USA 107:10314–10319
Robert KA, Brunet-Rossinni A, Bronikowski AM (2007) Testing the ‘free radical theory of aging’ hypothesis: physiological differences in long-lived and short-lived colubrid snakes. Aging Cell 6:395–404
Rodriguez M, Basten Snoek L, Riksen JAG, Bevers RP, Kammenga JE (2012) Genetic variation for stress-response hormesis in C. elegans lifespan. Exp Geront 47:581–587
Rose MR, Charlesworth B (1981) Genetics of life-history in Drosophila melanogaster. 2. Exploratory selection experiments. Genetics 97:187–196
Rottenberg H (2006) Longevity and the evolution of the mitochondrial DNA-coded proteins in mammals. Mech Ageing Dev 127:748–760
Rottenberg H (2007a) Coevolution of exceptional longevity, exceptionally high metabolic rates, and mitochondrial DNA-coded proteins in mammals. Exp Geront 42:364–373
Rottenberg H (2007b) Exceptional longevity in songbirds is associated with high rates of evolution of cytochrome b, suggesting selection for reduced generation of free radicals. J Exp Biol 210:2170–2180
Rubner M (1908) Das problem der lebensdauer und seine beziehunger zum wachstum und ernaibrung, Oldenburg, Munchen
Rubolini D, Colombo G, Ambrosini R, Caprioli M, Clerici M, Colombo R, Dalle-Donne I, Milzani A, Romano A, Romano M, Saino N (2012) Sex-related effects of reproduction on biomarkers of oxidative damage in free-living barn swallows (Hirundo rustica). PLoS One 7:e48955
Ruggiero C, Metter EJ, Melenovsky V, Cherubini A, Najjar SS, Ble A, Senin U, Longo DL, Ferrucci L (2008) High basal metabolic rate is a risk factor for mortality: the Baltimore longitudinal study of aging. J Geront A 63:698–706
Saino N, Caprioli M, Romano M, Boncoraglio G, Rubolini D, Ambrosini R, Bonisoli-Alquati A, Romano A (2011) Antioxidant defenses predict long-term survival in a passerine bird. PLoS ONE 6:e19593
Salmon AB, Marx DB, Harshman LG (2001) A cost of reproduction in Drosophila melanogaster: stress susceptibility. Evolution 55:1600–1608
Salmon AB, Leonard S, Masamsetti V, Pierce A, Podlutsky AJ, Podlutskaya N, Richardson A, Austad SN, Chaudhuri A (2009) The long lifespan of two bat species is correlated with resistance to protein oxidation and enhanced protein homeostasis. FASEB J 23:2317–2326
Salmon AB, Richardson A, Pérez VI (2010) Update on the oxidative stress theory of aging: does oxidative stress play a role in aging or healthy aging? Free Rad Biol Medic 48:642–655
Salomons HM, Mulder GA, van de Zande L, Haussmann MF, Linskens MH, Verhulst S (2009) Telomere shortening and survival in free-living corvids. Proc R Soc Lond B 276:3157–3165
Salway KD, Gallagher EJ, Page MM, Stuart JA (2011) Higher levels of heat shock proteins in longer-lived mammals and birds. Mech Ageing Dev 132:287–297
Samuels DC (2005) Life span is related to the free energy of mitochondrial DNA. Mech Ageing Dev 126:1123–1129
Sanz A, Pamplona R, Barja G (2006) Is the mitochondrial free radical theory of aging intact? Antiox Redox Sign 8:582–599
Sasaki T, Unno K, Tahara S, Shimada A, Chiba Y, Hoshino M, Kaneko T (2008) Age-related increase of superoxide generation in the brains of mammals and birds. Aging Cell 7:459–469
Schriner SE, Linford NJ, Martin GM, Treuting P, Ogburn CE, Emond M, Coskun PE, Ladiges W, Wolf N, Van Remmen H, Wallace DC, Rabinovitch PS (2005) Extension of murine life span by overexpression of catalase targeted to mitochondria. Science 308:1909–1911
Selman C, McLaren JS, Collins AR, Duthie GG, Speakman JR (2008) The impact of experimentally elevated energy expenditure on oxidative stress and lifespan in the short-tailed field vole Microtus agrestis. Proc R Soc Lond B 275:1907–1916
Snell TW, Fields AM, Johnston RK (2012) Antioxidants can extend lifespan of Brachionus manjavacas (Rotifera), but only in a few combinations. Biogerontology 13:261–275
Sohal RS, Mockett RJ, Orr WC (2002) Mechanisms of aging: an appraisal of the oxidative stress hypothesis. Free Rad Biol Med 33:575–586
Sohal RS, Orr WC (2012) The redox stress hypothesis of aging. Free Rad Biol Med 52:539–555
Soltow QA, Jones DP, Promislow DEL (2010) A network perspective on metabolism and aging. Integr Comp Biol 50:844–854
Sørensen JG, Kristensen TN, Kristensen KV, Loeschcke V (2007) Sex specific effects of heat induced in Hsf-deficient Drosophila melanogaster. Exp Gerontol 42:1123–1129
Sosnowska D, Richardson C, Sonntag WE, Csiszar A, Ungvari Z, Ridgway I (2014) A heart that beats for 500 years: age-related changes in cardiac proteasome activity, oxidative protein damage and expression of heat shock proteins, inflammatory factors, and mitochondrial complexes in Arctica islandica, the longest-living noncolonial animal. J Gerontol A (in press)
Southworth LK, Owen AB, Kim SK (2009) Aging mice show a decreasing correlation of gene expression within genetic modules. PLoS Genet 5:e1000776
Speakman JR (2005a) Body size, energy metabolism and lifespan. J Exp Biol 208:1717–1730
Speakman JR (2005b) Correlations between physiology and lifespan–two widely ignored problems with comparative studies. Aging Cell 4:167–175
Speakman JR, Talbot DA, Selman C, Snart S, McLaren JS, Redman P, Krol E, Jackson DM, Johnson MS, Brand MD (2004) Uncoupled and surviving: individual mice with high metabolism have greater mitochondrial uncoupling and live longer. Aging Cell 3:87–95
Stadtman ER, Moskovitz J, Berlett B, Levine RL (2002) Cyclic oxidation and reduction of protein methionine residues is an important antioxidant mechanism. Mol Cell Biochem 234–235:3–9
Storer JB (1967) Relation of lifespan to brain weight, body weight and metabolic rate among inbred mouse strains. Exp Geront 2:173–182
Strecker V, Mai S, Muster B, Beneke S, Bürkle A, Bereiter-Hahn J, Jendrach M (2010) Aging of different avian cultured cells: lack of ROS-induced damage and quality control mechanisms. Mechan Ageing Dev 131:48–59
Talbot DA, Lambert AJ, Brand MD (2004) Production of endogenous matrix superoxide from mitochondrial complex I leads to activation of uncoupling protein 3. FEBS Lett 556:111–115
Tanaka Y (1993) A genetic mechanism for the evolution of senescence in Callosobruchus chinensis (the Azuki Bean Weevil). Heredity 70:318–321
Torres-Barceló C, Cabot G, Oliver A, Buckling A, MacLean RC (2013) A trade-off between oxidative stress resistance and DNA repair plays a role in the evolution of elevated mutation rates in bacteria. Proc R Soc Lond B 280:20130007
Tower J (2006) Sex-specific regulation of aging and apoptosis. Mech Ageing Dev 127:705–718
Trivers R (1985) Social evolution. Benjamin/Cummings Publishing, Menlo Park, California
Unterluggauer H, Hütter E, Voglauer R, Grillari J, Vöth M, Bereiter-Hahn J, Jansen-Dürr P, Jendrach M (2007) Identification of cultivation-independent markers of human endothelial cell senescence in vitro. Biogerontology 8:383–397
Valencak TG, Ruf T (2007) N-3 polyunsaturated fatty acids impair lifespan but have no role for metabolism. Aging Cell 6:15–25
Vaanholt LM, Daan S, Schubert KA, Visser GH (2009) Metabolism and aging: effects of cold exposure on metabolic rate, body composition, and longevity in mice. Physiol Biochem Zool 82:314–324
Vaanholt LM, Daan S, Garland T Jr, Visser GH (2010) Exercising for life? Energy metabolism, body composition, and longevity in mice exercising at different intensities. Physiol Biochem Zool 83:239–251
van de Crommenacker J (2011) Hard times in paradise? Oxidative status, physiology and fitness in the tropical Seychelles warbler. PhD Thesis, University of Groningen
Veskoukis AS, Nikolaidis MG, Kyparos A, Kouretas D (2009) Blood reflects tissue oxidative stress depending on biomarker and tissue studied. Free Rad Biol Med 47:1371–1374
Vina J, Gambini J, Lopez-Grueso R, Abdelaziz KM, Jove M, Borras C (2011) Females live longer than males: role of oxidative stress. Curr Pharm Des 17:3959–3965
Voituron Y, de Fraipont M, Issartel J, Guillaume O, Clobert J (2011) Extreme lifespan of the human fish (Proteus anguinus): a challenge for ageing mechanisms. Biol Lett 7:105–107
von Zglinicki T (2002) Oxidative stress shortens telomeres. Trends Biochem Sci 27:339–344
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 Hered 97:355–366
Wasser DE, Sherman PW (2010) Avian longevities and their interpretation under evolutionary theories of senescence. J Zool 280:103–155
Webb RE, Leslie DM Jr, Lochmiller RL, Masters RE (2005) Impact of food supplementation and methionine on high densities of cotton rats: support of the amino-acid-quality hypothesis? J Mammal 86:46–55
Weinert BT, Timiras PS (2003) Theories of aging. J Appl Physiol 95:1706–1716
Weirsma P, Nowak B, Williams JB (2012) Small organ size contributes to the slow pace of life in tropical birds. J Exp Biol 215:1662–1669
Weissman A (1889) Essays upon heredity and kindred biological problems. Clarendon Press, Oxford
Williams GC (1957) Pleiotropy, natural selection, and the evolution of senescence. Evolution 11:398–411
Wright WE, Shay JW (2001) Cellular senescence as a tumor-protection mechanism: the essential role of counting. Curr Opin Genet Dev 11:98–103
Xue H, Xian B, Dong D, Xia K, Zhu S, Zhang Z, Hou L, Zhang Q, Zhang Y, Han J-DJ (2007) A modular network model of aging. Mol Syst Biol 3:147
Yarian CS, Rebrin I, Sohal RS (2005) Aconitase and ATP synthase are targets of malondialdeyde modification and undergo an age-related decrease in activity in mouse heart mitochondria. Biochem Biophys Res Commun 330:151–156
Yu BP, Yang R (1996) Critical evaluation of the free radical theory of aging. A proposal for the oxidative stress hypothesis. Ann NY Acad Sci 786:1–11
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
Copyright information
© 2014 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Costantini, D. (2014). Integrating Oxidative Stress and Hormesis into Research on Senescence and Survival Perspectives. In: Oxidative Stress and Hormesis in Evolutionary Ecology and Physiology. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-54663-1_10
Download citation
DOI: https://doi.org/10.1007/978-3-642-54663-1_10
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-54662-4
Online ISBN: 978-3-642-54663-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)