Abstract
Evolutionary relationships among fitness traits are considered in terms of the near-to-universal scenario of stressful environments leading to a resource-deficient and hence energy-deficient world. Fitness approximates to energetic (and metabolic) efficiency under this environmental model. When fitness is high, stress resistance (reducible to oxidative-stress resistance) and metabolic stability are maximal, and energy expenditure is minimal. Rapid development should then be favored followed by a long lifespan and high adult survival. Positive associations among diverse fitness or life-history traits are expected, controlled by stress-resistant ‘good genotypes’. Heterozygotes tend to show higher energetic efficiency and hence higher fitness than do corresponding homozygotes under extreme environments, and to give parallel associations among life-history traits. Energy budgets under abiotic environments are pivotal for integrative evolutionary studies of life histories in natural populations.
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References
Arking R (1998) Biology of aging: observations and principles, 2nd edn. Sinauer Associates, Sunderland, Massachusetts
Arking R, Buck S, Hwangbo DS, Lane M (2002) Metabolic alterations and shifts in energy allocations are corequisites for the expression of extended longevity genes in Drosophila. Ann NY Acad Sci 959:251–262
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
Criscuolo F, Gonzalez-Barroso M del M, Bouillard F, Ricquier D, Miroux B, Sorci G (2005) Mitochondrial uncoupling proteins: new perspectives for evolutionary ecologists. Am Nat 166:686–699
Demetrius L (2005) Of mice and men. EMBO Rep 6:S39–S44
Eldredge N (1999) The pattern of evolution. W H Freeman, New York
Falkowski PG (2006) Tracing oxygen’s imprint on Earth’s metabolic evolution. Science 311:1724–1725
Fisher RA (1930) The genetical theory of natural selection. Clarendon Press, Oxford
Hekimi S, Guarente L (2003) Genetics and the specificity of the aging process. Science 299:1351–1354
Hilliker AJ, Duyf B, Evans D, Phillips JP (1992) Urate-null rosy mutants of Drosophila melanogaster are hypersensitive to oxygen stress. Proc Natl Acad Sci USA 89:4243–4247
Kauffman SA (1993) The origins of order: self-organization and selection in evolution. Oxford Univ Press, New York
Koehn RK, Bayne BL (1989) Towards a physiological and genetical understanding of the stress response. Biol J Linn Soc 37:151–171
Kruuk LEB (2004) Estimating genetic parameters in natural populations using the animal model. Phil Trans Roy Soc Lond B359:873–890
Landis GN, Abdueva D, Skvortsov D, Yang J, Rabin BE, Carrick J, Tavaré S, Tower J (2004) Similar gene expression patterns characterize aging and oxidative stress in Drosophila melanogaster. Proc Natl Acad Sci USA 101:7663–7668
Margulis L, Sagan D (2002) Acquiring genomes: a theory of the origin of species. Basic Books, New York
Mauck RA, Huntingdon CE, Grubb TC Jr (2004) Age-specific reproductive success: evidence for the selection hypothesis. Evolution 58:880–885
Mitton JB (1993) Enzyme heterozygosity, metabolism and developmental variability. Genetica 89:47–63
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
Morowitz HJ (1992) Beginnings of cellular life: metabolism recaptures biogenesis. Yale Univ Press, New Haven
Myrand B, Tremblay R, Sévigny J-M (2002) Selection against blue mussels (Mytilus edulis L) homozygotes under various stressful conditions. J Hered 93:238–248
Nevo E (2001) Evolution of genome–phenome diversity under environmental stress. Proc Natl Acad Sci USA 98:6233–6240
Niewiarowski PH (2001) Energy budgets, growth rates, and thermal constraints: toward an integrative approach to the study of life-history variation. Am Nat 157:421–433
Olshansky SJ, Rattan SIS (2005) At the heart of aging: is it metabolic rate or stability? Biogerontology 6:291–295
Paolisso G, Tagliamonte MR, Risso MR, Manzella D, Gambardella A, Varrichio M (1998) Oxidative stress and advancing age: results in healthy centenarians. J␣Am Geriat Soc 46:833–838
Parsons PA (1971) Extreme-environment heterosis and genetic loads. Heredity 26:479–483
Parsons PA (1992) Evolutionary adaptation and stress: the fitness gradient. Evol Biol 26:191–223
Parsons PA (1995) Inherited stress resistance and longevity: a stress theory of ageing. Heredity 75:216–221
Parsons PA (1996) Rapid development and a long life: an association expected under a stress theory of aging. Experientia 53:643–646
Parsons PA (1998) Behavioral variability and limits to evolutionary adaptation under stress. Adv Study Behav 27:155–180
Parsons PA (2002) Life span: does the limit to survival depend upon metabolic efficiency under stress? Biogeronotology 3:233–241
Parsons PA (2004) From energy efficiency under stress to rapid development and a long life in natural populations. Biogerontology 5:201–210
Parsons PA (2005) Environments and evolution: interactions between stress, resource inadequacy and energetic efficiency. Biol Rev 80:589–610
Raymond J, Segre D (2006) The effect of oxygen on biochemical networks and the evolution of complex life. Science 311:1764–1767
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
Torres JL (1991) Natual selection and thermodynamic optimality. Il Nuovo Cimento 13:177–185
Van Voorhies WA, Fuchs J, Thomas S (2005) The longevity of Caenorhabditis elegans in soil. Biol Lett 1:247–249
Vernmeij GJ (2004) Nature: an economic history. Princeton Univ. Press, Princeton
Vorburger C (2005) Positive genetic correlations among major life-history traits related to ecological success in the aphid Myzus persicae. Evolution 59:1006–1015
Watt WB (1986) Power and efficiency as indexes of fitness in metabolic organization. Am Nat 127:629–653
Wedekind C (1994) Handicaps not obligatory in sexual selection for resistance genes. J Theor Biol 170:57–62
White TCR (1993) The inadequate environment: nitrogen and the abundance of animals. Springer-Verlag, Berlin
White TCR (2005) Why does the world stay green? Nutrition and survival of plant-eaters. CSIRO Publishing, Collingwood, Australia
Williams GC (1966) Adaptation and natural selection. Princeton University Press, Princeton
Zotin AI (1990) Thermodynamic bases of biological processes: physiological reactions and interactions. Walter de Gruyter, New York
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Parsons, P.A. Energetic efficiency under stress underlies positive genetic correlations between longevity and other fitness traits in natural populations. Biogerontology 8, 55–61 (2007). https://doi.org/10.1007/s10522-006-9028-8
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DOI: https://doi.org/10.1007/s10522-006-9028-8