Biochemistry (Moscow)

, Volume 82, Issue 12, pp 1435–1455 | Cite as

Sex and aging: A comparison between two phenoptotic phenomena

  • Giacinto LibertiniEmail author


Phenoptosis is a phenomenon that is genetically programmed and favored by natural selection, and that determines death or increased risk of death (fitness reduction) for the individual that manifests it. Aging, here defined as agerelated progressive mortality increase in the wild, if programmed and favored by natural selection, falls within the definition of phenoptosis. Sexual reproduction (sex), as for the involved individuals determines fitness reduction and, in some species, even certain death, also falls within the definition of phenoptosis. In this review, sex and aging are analyzed as phenoptotic phenomena, and the similarities between them are investigated. In particular, from a theoretical standpoint, the genes that cause and regulate these phenomena: (i) require analyses that consider both individual and supra-individual selection because they are harmful in terms of individual selection, but advantageous (that is, favored by natural selection) in particular conditions of supra-individual selection; (ii) determine a higher velocity of and greater opportunities for evolution and, therefore, greater evolutionary potential (evolvability); (iii) are advantageous under ecological conditions of K-selection and with finite populations; (iv) are disadvantageous (that is, not favored by natural selection) under ecological conditions of r-selection and with unlimited populations; (v) are not advantageous in all ecological conditions and, so, species that reproduce asexually or species that do not age are predicted and exist.


aging sex phenoptosis supra-individual selection K-selection r-selection 


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  1. 1.
    Pianka, E. R. (1970) On r- and K-selection, Am. Nat., 104, 592–597.CrossRefGoogle Scholar
  2. 2.
    Ghiselin, M. T. (1974) The Economy of Nature and the Evolution of Sex, University of California Press, Berkeley.Google Scholar
  3. 3.
    Williams, G. C. (1975) Sex and Evolution, Princeton University Press, Princeton.Google Scholar
  4. 4.
    Maynard Smith, J. (1978) The Evolution of Sex, Cambridge University Press, Cambridge.Google Scholar
  5. 5.
    Bell, G. (1982) The Masterpiece of Nature. The Evolution and Genetics of Sexuality, Croom Helm, London.Google Scholar
  6. 6.
    Ridley, M. (1993) The Red Queen. Sex and the Evolution of Human Nature, Penguin Books, London.Google Scholar
  7. 7.
    Barton, N. H., and Charlesworth, B. (1998) Why sex and recombination? Science, 281, 1986–1990.CrossRefPubMedGoogle Scholar
  8. 8.
    Agrawal, A. F. (2006) Evolution of sex: why do organisms shuffle their genotypes? Curr. Biol., 16, R696–R704.CrossRefPubMedGoogle Scholar
  9. 9.
    Hadany, L., and Comeron, J. M. (2008) Why are sex and recombination so common? Ann. N. Y. Acad. Sci., 1133, 26–43.CrossRefPubMedGoogle Scholar
  10. 10.
    Barton, N. H. (2009) Why sex and recombination? Cold Spring Harb. Symp. Quant. Biol., 74, 187–195.CrossRefPubMedGoogle Scholar
  11. 11.
    Otto, S. P. (2009) The evolutionary enigma of sex, Am. Nat., 174, S1–S14.CrossRefPubMedGoogle Scholar
  12. 12.
    Hartfield, M., and Keightley, P. D. (2012) Current hypotheses for the evolution of sex and recombination, Integr. Zool., 7, 192–209.CrossRefPubMedGoogle Scholar
  13. 13.
    McDonald, M. J., Rice, D. P., and Desai, M. M. (2016) Sex speeds adaptation by altering the dynamics of molecular evolution, Nature, 531, 233–236.PubMedCentralCrossRefPubMedGoogle Scholar
  14. 14.
    Sharp, N. P., and Otto, S. P. (2016) Evolution of sex: using experimental genomics to select among competing theories, Bioessays, 38, 751–757.CrossRefPubMedGoogle Scholar
  15. 15.
    Lewis-Pye, A. E., and Montalban, A. (2017) Sex versus asex: an analysis of the role of variance conversion, Theor. Popul. Biol., 114, 128–135.CrossRefPubMedGoogle Scholar
  16. 16.
    Ho, E. K. H., and Agrawal, A. F. (2017) Aging asexual lineages and the evolutionary maintenance of sex, Evolution, doi: 10.1111/evo.13260.Google Scholar
  17. 17.
    Weismann, A. (1889) Essays upon Heredity and Kindred Biological Problems, Translated by Poulton, E. B., Schonland, S., and Shipley, A. E., Clarendon Press, Oxford.Google Scholar
  18. 18.
    Guenther, C. (1906) Darwinism and the Problems of Life. A Study of Familiar Animal Life, Translated by McCabe, J. A., Owen, London.Google Scholar
  19. 19.
    Fisher, R. A. (1930) The Genetical Theory of Natural Selection, Oxford University Press, Oxford.CrossRefGoogle Scholar
  20. 20.
    Muller, H. J. (1932) Some genetic aspects of sex, Am. Nat., 66, 118–138.CrossRefGoogle Scholar
  21. 21.
    Muller, H. J. (1958) Evolution by mutation, Bull. Am. Math. Soc., 64, 137–160.CrossRefGoogle Scholar
  22. 22.
    Muller, H. J. (1964) The relation of recombination to mutational advance, Mutat. Res., 1, 2–9.CrossRefGoogle Scholar
  23. 23.
    Crow, J. F., and Kimura, M. (1965) Evolution in sexual and asexual populations, Am. Nat., 99, 439–450.CrossRefGoogle Scholar
  24. 24.
    Maynard Smith, J. (1968) Evolution in sexual and asexual populations, Am. Nat., 102, 469–473.CrossRefGoogle Scholar
  25. 25.
    Felsenstein, J. (1974) The evolutionary advantage of recombination, Genetics, 78, 737–756.PubMedCentralPubMedGoogle Scholar
  26. 26.
    Crow, J. F., and Kimura, M. (1969) Evolution in sexual and asexual populations: a reply, Am. Nat., 103, 89–91.CrossRefGoogle Scholar
  27. 27.
    Butcher, D. (1995) Muller’s ratchet, epistasis and mutation effects, Genetics, 141, 431–437.PubMedGoogle Scholar
  28. 28.
    Gordo, I., and Charlesworth, B. (2000) The degeneration of asexual haploid populations and the speed of Muller’s ratchet, Genetics, 154, 1379–1387.PubMedCentralPubMedGoogle Scholar
  29. 29.
    Keightley, P. D., and Otto, S. P. (2006) Interference among deleterious mutations favors sex and recombination in finite populations, Nature, 443, 89–92.CrossRefPubMedGoogle Scholar
  30. 30.
    Gordo, I., and Campos, P. R. (2008) Sex and deleterious mutations, Genetics, 179, 621–626.PubMedCentralCrossRefPubMedGoogle Scholar
  31. 31.
    Wardlaw, A. M., and Agrawal, A. F. (2012) Temporal variation in selection accelerates mutational decay by Muller’s ratchet, Genetics, 191, 907–916.PubMedCentralCrossRefPubMedGoogle Scholar
  32. 32.
    Williams, G. C. (1966) Adaptation and Natural Selection. A Critique of Some Current Evolutionary Thought, Princeton University Press, Princeton.Google Scholar
  33. 33.
    Emlen, J. M. (1973) Ecology: An Evolutionary Approach, Addison-Wesley, Reading.Google Scholar
  34. 34.
    Treisman, M. (1976) The evolution of sexual reproduction: a model which assumes individual selection, J. Theor. Biol., 60, 421–431.CrossRefPubMedGoogle Scholar
  35. 35.
    Dacks, J., and Roger, A. J. (1999) The first sexual lineage and the relevance of facultative sex, J. Mol. Evol., 48, 779–783.CrossRefPubMedGoogle Scholar
  36. 36.
    Hill, W. G., and Robertson, A. (1966) The effect of linkage on limits to artificial selection, Genet. Res., 8, 269–294.CrossRefPubMedGoogle Scholar
  37. 37.
    Case, T. J., and Taper M. L. (1986) On the coexistence and coevolution of asexual and sexual competitors, Evolution, 40, 366–387.CrossRefPubMedGoogle Scholar
  38. 38.
    Burt, A., and Bell, G. (1987) Mammalian chiasma frequencies as a test of two theories of recombination, Nature, 326, 803–805.CrossRefPubMedGoogle Scholar
  39. 39.
    Doncaster, C. P., Pound, G. E., and Cox, S. J. (2000) The ecological cost of sex, Nature, 404, 281–285.CrossRefPubMedGoogle Scholar
  40. 40.
    Song, Y., Drossel, B., and Scheu, S. (2011) Tangled Bank dismissed too early, Oikos, 120, 1601–1607.CrossRefGoogle Scholar
  41. 41.
    Van Valen, L. (1973) A new evolutionary law, Evol. Theory, 1, 1–30.Google Scholar
  42. 42.
    Hamilton, W. D. (1975) Gamblers since life began: barnacles, aphids, elms, Quart. Rev. Biol., 50, 175–180.CrossRefGoogle Scholar
  43. 43.
    Levin, D. A. (1975) Pest pressure and recombination systems in plants, Am. Nat., 109, 437–451.CrossRefGoogle Scholar
  44. 44.
    Charlesworth, B. (1976) Recombination modification in a fluctuating environment, Genetics, 83, 181–195.PubMedCentralPubMedGoogle Scholar
  45. 45.
    Glesener, R. R., and Tilman, D. (1978) Sexuality and the components of environmental uncertainty: clues from geographic parthenogenesis in terrestrial animals, Am. Nat., 112, 659–673.CrossRefGoogle Scholar
  46. 46.
    Glesener, R. R. (1979) Recombination in a simulated predator–prey interaction, Am. Zool., 19, 763–771.CrossRefGoogle Scholar
  47. 47.
    Bell, G., and Maynard Smith, J. (1987) Short-term selection for recombination among mutually antagonistic species, Nature, 328, 66–68.CrossRefGoogle Scholar
  48. 48.
    Peters, A. D., and Lively, C. M. (1999) The red queen and fluctuating epistasis: a population genetic analysis of antagonistic coevolution, Am. Nat., 154, 393–405.CrossRefPubMedGoogle Scholar
  49. 49.
    Peters, A. D., and Lively, C. M. (2007) Shortand long-term benefits and detriments to recombination under antagonistic coevolution, J. Evolution. Biol., 20, 1206–1217.CrossRefGoogle Scholar
  50. 50.
    Otto, S. P., and Nuismer, S. L. (2004) Species interactions and the evolution of sex, Science, 304, 1018–1020.CrossRefPubMedGoogle Scholar
  51. 51.
    Kouyos, R. D., Salathe, M., and Bonhoeffer, S. (2007) The Red Queen and the persistence of linkage-disequilibrium oscillations in finite and infinite populations, BMC Evol. Biol., 7,211.PubMedCentralCrossRefPubMedGoogle Scholar
  52. 52.
    Salathe, M., Kouyos, R. D., and Bonhoeffer, S. (2008) The state of affairs in the kingdom of the Red Queen, Trends Ecol. Evol., 23, 439–445.CrossRefPubMedGoogle Scholar
  53. 53.
    Liow, L. H., Van Valen, L., and Stenseth, N. C. (2011) Red Queen: from populations to taxa and communities, Trends Ecol. Evol., 26, 349–358.CrossRefPubMedGoogle Scholar
  54. 54.
    Brockhurst, M. A., Chapman, T., King, K. C., Mank, J. E., Paterson, S., and Hurst, G. D. (2014) Running with the Red Queen: the role of biotic conflicts in evolution, Proc. Biol. Sci., 281, pii: 20141382.PubMedCentralCrossRefPubMedGoogle Scholar
  55. 55.
    Voje, K. L., Holen, O. H., Liow, L. H., and Stenseth, N. C. (2015) The role of biotic forces in driving macroevolution: beyond the Red Queen, Proc. Biol. Sci., 282, 20150186.PubMedCentralCrossRefPubMedGoogle Scholar
  56. 56.
    Stanley, S. M. (1978) Clades versus clones in evolution: why we have sex? Science, 190, 382–383.CrossRefGoogle Scholar
  57. 57.
    Kondrashov, A. S. (1984) Deleterious mutations as an evolutionary factor. I. The advantage of recombination, Genet. Res., 44, 199–217.CrossRefPubMedGoogle Scholar
  58. 58.
    Charlesworth, B. (1990) Mutation selection balance and the evolutionary advantage of sex and recombination, Genet. Res., 55, 199–221.CrossRefPubMedGoogle Scholar
  59. 59.
    Barton, N. H. (1995) A general model for the evolution of recombination, Genet. Res., 65, 123–144.CrossRefPubMedGoogle Scholar
  60. 60.
    Otto, S. P., and Feldman, M. W. (1997) Deleterious mutations, variable epistatic interactions, and the evolution of recombination, Theor. Popul. Biol., 51, 134–147.Google Scholar
  61. 61.
    West, S. A., Lively, C. M., and Read, A. F. (1999) A pluralist approach to sex and recombination, J. Evol. Biol., 12, 1003–1012.CrossRefGoogle Scholar
  62. 62.
    Kondrashov, A. S. (1993) Classification of hypotheses on the advantage of amphimixis, J. Hered., 84, 372–387.CrossRefPubMedGoogle Scholar
  63. 63.
    Kondrashov, A. S., and Yampolsky, L. Y. (1996) Evolution of amphimixis and recombination under fluctuating selection in one and many traits, Genet. Res., 68, 165–173.CrossRefGoogle Scholar
  64. 64.
    Burger, R. (1999) Evolution of genetic variability and the advantage of sex and recombination in changing environments, Genetics, 153, 1055–1069.PubMedCentralPubMedGoogle Scholar
  65. 65.
    Palsson, S. (2002) Selection on a modifier of recombination rate due to linked deleterious mutations, J. Hered., 93, 22–26.CrossRefPubMedGoogle Scholar
  66. 66.
    Iles, M. M., Walters, K., and Cannings, C. (2003) Recombination can evolve in large finite populations given selection on sufficient loci, Genetics, 165, 2249–2258.PubMedCentralPubMedGoogle Scholar
  67. 67.
    Barton, N. H., and Otto, S. P. (2005) Evolution of recombination due to random drift, Genetics, 169, 2353–2370.PubMedCentralCrossRefPubMedGoogle Scholar
  68. 68.
    Martin, G., Otto, S. P., and Lenormand, T. (2006) Selection for recombination in structured populations, Genetics, 172, 593–609.PubMedCentralCrossRefPubMedGoogle Scholar
  69. 69.
    Tannenbaum, E. (2008) Comparison of three replication strategies in complex multicellular organisms: asexual replication, sexual replication with identical gametes, and sexual replication with distinct sperm and egg gametes, Phys. Rev. E Stat. Nonlin. Soft. Matter Phys., 77, 011915.PubMedGoogle Scholar
  70. 70.
    Otto, S. P., and Lenormand, T. (2002) Resolving the paradox of sex and recombination, Nat. Rev. Genet., 3, 252–261.CrossRefPubMedGoogle Scholar
  71. 71.
    Felsenstein, J., and Yokoyama, S. (1976) The evolutionary advantage of recombination, II. Individual selection for recombination, Genetics, 83, 845–859.Google Scholar
  72. 72.
    Felsenstein, J. (1965) The effect of linkage on directional selection, Genetics, 52, 349–363.PubMedCentralPubMedGoogle Scholar
  73. 73.
    Eshel, I., and Feldman, M. W. (1970) On the evolutionary effect of recombination, Theor. Pop. Biol., 1, 88–100.CrossRefGoogle Scholar
  74. 74.
    Karlin, S. (1973) Sex and infinity; a mathematical analysis of the advantages and disadvantages of recombination, in The Mathematical Theory of the Dynamics of Natural Populations (Bartlett, M. S., and Hiorns, R. W., eds.) Academic Press, London.Google Scholar
  75. 75.
    Armitage, P., Matthews, J. N. S., and Berry, G. (2001) Statistical Methods in Medical Research, Wiley-Blackwell, New York.Google Scholar
  76. 76.
    Libertini, G. (2012) Classification of phenoptotic phenomena, Biochemistry (Moscow), 77, 707–715.CrossRefGoogle Scholar
  77. 77.
    Zuk, M. (2016) Mates with benefits: when and how sexual cannibalism is adaptive, Curr. Biol., 26, R1230–R1232.CrossRefPubMedGoogle Scholar
  78. 78.
    Polis, G. A. (1981) The evolution and dynamics of intraspecific predation, Ann. Rev. Ecol. Syst., 51, 225–251.CrossRefGoogle Scholar
  79. 79.
    Foelix, R. A. (1982) Biology of Spiders, Harvard University Press, Cambridge (USA).Google Scholar
  80. 80.
    Bilde, T., Tuni, C., Elsayed, R., Pekar, S., and Toft, S. (2006) Death feigning in the face of sexual cannibalism, Biol. Lett., 2, 23–25.CrossRefPubMedGoogle Scholar
  81. 81.
    Fernandez-Montraveta, C., Gonzalez, J. M., and Cuadrado, M. (2014) Male vulnerability explains the occurrence of sexual cannibalism in a moderately sexually dimorphic wolf spider, Behav. Processes, 105, 53–59.CrossRefPubMedGoogle Scholar
  82. 82.
    Gerritson, J. (1980) Sex and parthenogenesis in sparse populations, Am. Nat., 115, 718–742.CrossRefGoogle Scholar
  83. 83.
    Maynard Smith, J. (1971) The origin and maintenance of sex, in Group Selection (Williams, G. C., ed.) AldineAtherton, Chicago.Google Scholar
  84. 84.
    Lehtonen, J., Jennions, M. D., and Kokko, H. (2012) The many costs of sex, Trends Ecol. Evol., 27, 172–178.CrossRefPubMedGoogle Scholar
  85. 85.
    Parker, G. A., Baker, R. R., and Smith, V. G. F. (1972) The origin and evolution of gamete dimorphism and the malefemale phenomenon, J. Theor. Biol., 36, 529–553.CrossRefPubMedGoogle Scholar
  86. 86.
    Bell, G. (1978) The evolution of anisogamy, J. Theor. Biol., 73, 247–270.CrossRefPubMedGoogle Scholar
  87. 87.
    Charlesworth, B. (1978) The population genetics of anisogamy, J. Theor. Biol., 73, 347–357.CrossRefPubMedGoogle Scholar
  88. 88.
    Zahavi, A. (1975) Mate selection–a selection for a handicap, J. Theor. Biol., 53, 205–214.CrossRefPubMedGoogle Scholar
  89. 89.
    Maynard Smith, J. (1976) Sexual selection and the handicap principle, J. Theor. Biol., 57, 239–242.CrossRefGoogle Scholar
  90. 90.
    Alan Grafen, A. (1990) Biological signals as handicaps, J. Theor. Biol., 144, 517–546.CrossRefGoogle Scholar
  91. 91.
    Libertini, G. (1988) An adaptive theory of the increasing mortality with increasing chronological age in populations in the wild, J. Theor. Biol., 132, 145–162.CrossRefPubMedGoogle Scholar
  92. 92.
    Comfort, A. (1979) The Biology of Senescence, Elsevier North Holland, New York.Google Scholar
  93. 93.
    Medvedev, Z. A. (1990) An attempt at a rational classification of theories of ageing, Biol. Rev. Camb. Philos. Soc., 65, 375–398.CrossRefPubMedGoogle Scholar
  94. 94.
    Weinert, B. T., and Timiras, P. S. (2003) Invited review: theories of aging, J. Appl. Physiol., 95, 1706–1716.CrossRefPubMedGoogle Scholar
  95. 95.
    Libertini, G. (2015) Non-programmed versus programmed aging paradigm, Curr. Aging Sci., 8, 56–68.CrossRefPubMedGoogle Scholar
  96. 96.
    Minot, C. S. (1907) The problem of age, growth, and death; a study of cytomorphosis, based on lectures at the Lowell Institute, March 1907, London.Google Scholar
  97. 97.
    Carrel, A., and Ebeling, A. H. (1921) Antagonistic growth principles of serum and their relation to old age, J. Exp. Med., 38, 419–425.CrossRefGoogle Scholar
  98. 98.
    Brody, S. (1924) The kinetics of senescence, J. Gen. Physiol., 6, 245–257.PubMedCentralCrossRefPubMedGoogle Scholar
  99. 99.
    Bidder, G. P. (1932) Senescence, Br. Med. J., 115, 5831–5850.Google Scholar
  100. 100.
    Lansing, A. I. (1948) Evidence for aging as a consequence of growth cessation, Proc. Natl. Acad. Sci. USA, 34, 304–310.PubMedCentralCrossRefPubMedGoogle Scholar
  101. 101.
    Lansing, A. I. (1951) Some physiological aspects of ageing, Physiol. Rev., 31, 274–284.CrossRefPubMedGoogle Scholar
  102. 102.
    Harman, D. (1972) The biologic clock: the mitochondria? J. Am. Geriatr. Soc., 20, 145–147.CrossRefPubMedGoogle Scholar
  103. 103.
    Croteau, D. L., and Bohr, V. A. (1997) Repair of oxidative damage to nuclear and mitochondrial DNA in mammalian cells, J. Biol. Chem., 272, 25409–25412.CrossRefPubMedGoogle Scholar
  104. 104.
    Beckman, K. B., and Ames, B. N. (1998) The free radical theory of aging matures, Physiol. Rev., 78, 547–581.CrossRefPubMedGoogle Scholar
  105. 105.
    Oliveira, B. F., Nogueira-Machado, J.-A., and Chaves, M. M. (2010) The role of oxidative stress in the aging process, Sci. World J., 10, 1121–1128.CrossRefGoogle Scholar
  106. 106.
    Bohr, V. A., and Anson, R. M. (1995) DNA damage, mutation and fine structure DNA repair in aging, Mutat. Res., 338, 25–34.Google Scholar
  107. 107.
    Miquel, J., Economos, A. C., Fleming, J., and Johnson, J. E., Jr. (1980) Mitochondrial role in cell aging, Exp. Gerontol., 15, 575–591.CrossRefPubMedGoogle Scholar
  108. 108.
    Trifunovic, A., Wredenberg, A., Falkenberg, M., Spelbrink, J. N., Rovio, A. T., Bruder, C. E., Bohlooly, Y. M., Gidlof, S., Oldfors, A., Wibom, R., Tornell, J., Jacobs, H. T., and Larsson, N. G. (2004) Premature ageing in mice expressing defective mitochondrial DNA polymerase, Nature, 429, 417–423.CrossRefPubMedGoogle Scholar
  109. 109.
    Balaban, R. S., Nemoto, S., and Finkel, T. (2005) Mitochondria, oxidants, and aging, Cell, 120, 483–495.Google Scholar
  110. 110.
    Sanz, A., and Stefanatos, R. K. (2008) The mitochondrial free radical theory of aging: a critical view, Curr. Aging Sci., 1, 10–21.CrossRefPubMedGoogle Scholar
  111. 111.
    Medawar, P. B. (1952) An Unsolved Problem in Biology, H. K. Lewis, London. Reprinted in: Medawar, P. B. (1957) The Uniqueness of the Individual, Methuen, London.Google Scholar
  112. 112.
    Hamilton, W. D. (1966) The moulding of senescence by natural selection, J. Theor. Biol., 12, 12–45.CrossRefPubMedGoogle Scholar
  113. 113.
    Edney, E. B., and Gill, R. W. (1968) Evolution of senescence and specific longevity, Nature, 220, 281–282.CrossRefPubMedGoogle Scholar
  114. 114.
    Mueller, L. D. (1987) Evolution of accelerated senescence in laboratory populations of Drosophila, Proc. Natl. Acad. Sci. USA, 84, 1974–1977.PubMedCentralCrossRefPubMedGoogle Scholar
  115. 115.
    Partridge, L., and Barton, N. H. (1993) Optimality, mutation and the evolution of ageing, Nature, 362, 305–311.Google Scholar
  116. 116.
    Williams, G. C. (1957) Pleiotropy, natural selection and the evolution of senescence, Evolution, 11, 398–411.Google Scholar
  117. 117.
    Rose, M. R. (1991) Evolutionary Biology of Aging, Oxford University Press, New York.Google Scholar
  118. 118.
    Kirkwood, T. B. (1977) Evolution of ageing, Nature, 270, 301–304.CrossRefPubMedGoogle Scholar
  119. 119.
    Kirkwood, T. B., and Holliday, R. (1979) The evolution of ageing and longevity, Proc. R. Soc. Lond. B Biol. Sci., 205, 531–546.CrossRefPubMedGoogle Scholar
  120. 120.
    Blagosklonny, M. V. (2006) Aging and immortality: quasiprogrammed senescence and its pharmacologic inhibition, Cell Cycle, 5, 2087–2102.CrossRefPubMedGoogle Scholar
  121. 121.
    Blagosklonny, M. V. (2013) MTOR-driven quasi-programmed aging as a disposable soma theory: blind watchmaker vs. intelligent designer, Cell Cycle, 12, 1842–1847.PubMedCentralCrossRefPubMedGoogle Scholar
  122. 122.
    De Magalhaes, J. P., and Toussaint, O. (2002) The evolution of mammalian aging, Exp. Gerontol., 37, 769–775.CrossRefPubMedGoogle Scholar
  123. 123.
    Skulachev, V. P. (1997) Aging is a specific biological function rather than the result of a disorder in complex living systems: biochemical evidence in support of Weismann’s hypothesis, Biochemistry (Moscow), 62, 1191–1195.Google Scholar
  124. 124.
    Bredesen, D. E. (2004) The non-existent aging program: how does it work? Aging Cell, 3, 255–259.CrossRefPubMedGoogle Scholar
  125. 125.
    Mitteldorf, J. (2004) Aging selected for its own sake, Evol. Ecol. Res., 6, 1–17.Google Scholar
  126. 126.
    Longo, V. D., Mitteldorf, J., and Skulachev, V. P. (2005) Programmed and altruistic ageing, Nat. Rev. Genet., 6, 866–872.CrossRefPubMedGoogle Scholar
  127. 127.
    Finch, C. E. (1990) Longevity, Senescence, and the Genome, The University of Chicago Press, Chicago.Google Scholar
  128. 128.
    Skulachev, V. P. (1999) Phenoptosis: programmed death of an organism, Biochemistry (Moscow), 64, 1418–1426.Google Scholar
  129. 129.
    Wallace, A. R. (1889) The action of natural selection in producing old age, decay and death (A note by Wallace written “some time between 1865 and 1870”) (Weismann, A., ed.).Google Scholar
  130. 130.
    Skulachev, V. P., and Longo, V. D. (2005) Aging as a mitochondria-mediated atavistic program: can aging be switched off? Ann. N.Y. Acad. Sci., 1057, 145–164.CrossRefPubMedGoogle Scholar
  131. 131.
    Weismann, A. (1892) Essays Upon Heredity and Kindred Biological Problems, Vol. II, Clarendon Press, Oxford.Google Scholar
  132. 132.
    Kirkwood, T. B., and Cremer, T. (1982) Cytogerontology since 1881: a reappraisal of August Weismann and a review of modern progress, Hum. Genet., 60, 101–121.CrossRefPubMedGoogle Scholar
  133. 133.
    Goldsmith, T. C. (2004) Aging as an evolved characteristic–Weismann’s theory reconsidered, Med. Hypotheses, 62, 304–308.CrossRefPubMedGoogle Scholar
  134. 134.
    Goldsmith, T. C. (2008) Aging, evolvability, and the individual benefit requirement; medical implications of aging theory controversies, J. Theor. Biol., 252, 764–768.PubMedGoogle Scholar
  135. 135.
    Mitteldorf, J., and Pepper, J. (2009) Senescence as an adaptation to limit the spread of disease, J. Theor. Biol., 260, 186–195.CrossRefPubMedGoogle Scholar
  136. 136.
    Skulachev, V. P. (1999) Mitochondrial physiology and pathology; concepts of programmed death of organelles, cells and organisms, Mol. Aspects Med., 20, 139–184.CrossRefPubMedGoogle Scholar
  137. 137.
    Skulachev, V. P. (2001) The programmed death phenomena, aging, and the Samurai law of biology, Exp. Gerontol., 36, 995–1024.PubMedGoogle Scholar
  138. 138.
    Olovnikov, A. M. (2003) The redusome hypothesis of aging and the control of biological time during individual development, Biochemistry (Moscow), 68, 2–33.CrossRefGoogle Scholar
  139. 139.
    Olovnikov, A. M. (2015) Chronographic theory of development, aging, and origin of cancer: role of chronomeres and printomeres, Curr. Aging Sci., 8, 76–88.PubMedGoogle Scholar
  140. 140.
    Leopold, A. C. (1961) Senescence in plant development, Science, 134, 1727–1732.CrossRefPubMedGoogle Scholar
  141. 141.
    Libertini, G. (1983) Evolutionary Arguments, Società Editrice Napoletana, Naples (Italy), English Edn., 2011, Evolutionary Arguments on Aging, Disease, and Other Topics, Azinet Press, Crownsville MD.Google Scholar
  142. 142.
    Libertini, G. (2006) Evolutionary explanations of the “actuarial senescence in the wild” and of the “state of senility”, Sci. World J., 6, 1086–1108.CrossRefGoogle Scholar
  143. 143.
    Libertini, G. (2008) Empirical evidence for various evolutionary hypotheses on species demonstrating increasing mortality with increasing chronological age in the wild, Sci. World J., 8, 183–193.CrossRefGoogle Scholar
  144. 144.
    Libertini, G. (2009) The role of telomere–telomerase system in age-related fitness decline, a tameable process, in Telomeres: Function, Shortening and Lengthening (Mancini, L., ed.) Nova Science Publ., New York, pp. 77–132.Google Scholar
  145. 145.
    Libertini, G. (2013) Evidence for aging theories from the study of a hunter-gatherer people (Ache of Paraguay), Biochemistry (Moscow), 78, 1023–1032.CrossRefGoogle Scholar
  146. 146.
    Travis, J. M. (2004) The evolution of programmed death in a spatially structured population, J. Gerontol. A Biol. Sci. Med. Sci., 59, 301–305.CrossRefPubMedGoogle Scholar
  147. 147.
    Martins, A. C. (2011) Change and aging senescence as an adaptation, PLoS One, 6, e24328.PubMedCentralCrossRefPubMedGoogle Scholar
  148. 148.
    Mitteldorf, J., and Martins, A. C. (2014) Programmed life span in the context of evolvability, Am. Nat., 184, 289–302.CrossRefPubMedGoogle Scholar
  149. 149.
    Kowald, A., and Kirkwood, T. B. (2016) Can aging be programmed? A critical literature review, Aging Cell, doi: 10.1111/acel.12510.Google Scholar
  150. 150.
    Ricklefs, R. E. (1998) Evolutionary theories of aging: confirmation of a fundamental prediction, with implications for the genetic basis and evolution of life span, Am. Nat., 152, 24–44.PubMedGoogle Scholar
  151. 151.
    Calabrese, E. J., and Baldwin, L. A. (1998) Hormesis as a biological hypothesis, Environ. Health Perspect., 106, 357–362.PubMedCentralCrossRefPubMedGoogle Scholar
  152. 152.
    Masoro, E. J. (2003) Subfield history: caloric restriction, slowing aging, and extending life, Sci. Aging Knowledge Environ., RE2.Google Scholar
  153. 153.
    Masoro, E. J. (2005) Overview of caloric restriction and ageing, Mech. Ageing Dev., 126, 913–922.CrossRefPubMedGoogle Scholar
  154. 154.
    Masoro, E. J. (2007) The role of hormesis in life extension by dietary restriction, Interdiscip. Top. Gerontol., 35, 1–17.PubMedGoogle Scholar
  155. 155.
    Calabrese, E. J. (2005) Toxicological awakenings: the rebirth of hormesis as a central pillar of toxicology, Toxicol. Appl. Pharmacol., 204, 1–8.CrossRefPubMedGoogle Scholar
  156. 156.
    Ribaric, S. (2012) Diet and aging, Oxid. Med. Cell Longev., 741468.Google Scholar
  157. 157.
    Lee, S. H., and Min, K. J. (2013) Caloric restriction and its mimetics, BMB Rep., 46, 181–187.PubMedCentralCrossRefPubMedGoogle Scholar
  158. 158.
    Skulachev, V. P. (2002) Programmed death phenomena: from organelle to organism, Ann. N.Y. Acad. Sci., 959, 214–237.CrossRefPubMedGoogle Scholar
  159. 159.
    Jones, O. R., Scheuerlein, A., Salguero-Gomez, R., Camarda, C. G., Schaible, R., Casper, B. B., Dahlgren, J. P., Ehrlen, J., Garcia, M. B., Menges, E. S., Quintana-Ascencio, P. F., Caswell, H., Baudisch, A., and Vaupel, J. W. (2014) Diversity of ageing across the tree of life, Nature, 505, 169–173.CrossRefPubMedGoogle Scholar
  160. 160.
    Libertini, G., Rengo, G., and Ferrara, N. (2017) Aging and aging theories, J. Geront. Geriatr., 1, 59–77.Google Scholar

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© Pleiades Publishing, Ltd. 2017

Authors and Affiliations

  1. 1.Independent researcher member of the Italian Society for Evolutionary BiologyRomeItaly

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