Skip to main content
SpringerLink
Log in

Evolution of Longevity in Tetrapods: Safety Is More Important than Metabolism Level

  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

Various environmental morphological and behavioral factors can determine the longevity of representatives of various taxa. Long-lived species develop systems aimed at increasing organism stability, defense, and, ultimately, lifespan. Long-lived species to a different extent manifest the factors favoring longevity (gerontological success), such as body size, slow metabolism, activity of body’s repair and antioxidant defense systems, resistance to toxic substances and tumorigenesis, and presence of neotenic features. In continuation of our studies of mammals, we investigated the characteristics that distinguish long-lived ectotherms (crocodiles and turtles) and compared them with those of other ectotherms (squamates and amphibians) and endotherms (birds and mammals). We also discussed mathematical indicators used to assess the predisposition to longevity in different species, including standard indicators (mortality rate, maximum lifespan, coefficient of variation of lifespan) and their derivatives. Evolutionary patterns of aging are further explained by the protective phenotypes and life history strategies. We assessed the relationship between the lifespan and various studied factors, such as body size and temperature, encephalization, protection of occupied ecological niches, presence of protective structures (for example, shells and osteoderms), and environmental temperature, and the influence of these factors on the variation of the lifespan as a statistical parameter. Our studies did not confirm the hypothesis on the metabolism level and temperature as the most decisive factors of longevity. It was found that animals protected by shells (e.g., turtles with their exceptional longevity) live longer than species that have poison or lack such protective adaptations. The improvement of defense against external threats in long-lived ectotherms is consistent with the characteristics of long-lived endotherms (for example, naked mole-rats that live in underground tunnels, or bats and birds, whose ability to fly is one of the best defense mechanisms).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Abbreviations

CV:

coefficient of variation

LS:

life span

ROS:

reactive oxygen species

References

  1. Comfort, A. (1979) The Biology of Senescence, Churchill Livingstone, Edinburgh and London.

  2. Austad, S. N. (1997) Why We Age, John Wiley and Sons, New York.

  3. Finch, C. E. (2009) Update on slow aging and negligible senescence – a mini-review, Gerontology, 55, 307-313, https://doi.org/10.1159/000215589.

    Article  PubMed  Google Scholar 

  4. Medawar, P. B. (1952) An Unsolved Problem of Biology, H. C. Lewis & Co LTD, London.

  5. Williams, G. C. (1957) Pleiotropy, natural selection and the evolution of senescence, Evolution, 11, 398-411, https://doi.org/10.1111/j.1558-5646.1957.tb02911.x.

    Article  Google Scholar 

  6. Kirkwood, T. B. L. (1977) Evolution of ageing, Nature, 270, 301-304, https://doi.org/10.1038/270301a0.

    Article  ADS  CAS  PubMed  Google Scholar 

  7. Rando, T. A., and Chang, H. Y. (2012) Aging, rejuvenation, and epigenetic reprogramming: resetting the aging clock, Cell, 148, 46-57, https://doi.org/10.1016/j.cell.2012.01.003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Skulachev, M. V., and Skulachev, V. P. (2014) New data on programmed aging – slow phenoptosis, Biochemistry (Moscow), 79, 977-993, https://doi.org/10.1134/S0006297914100010.

    Article  CAS  PubMed  Google Scholar 

  9. Vaupel, J. W., Baudisch, A., Dölling, M., Roach, D. A., and Gampe, J. (2004) The case for negative senescence, Theor. Popul. Biol., 65, 339-351, https://doi.org/10.1016/j.tpb.2003.12.003.

    Article  PubMed  Google Scholar 

  10. Jones, O. R., Scheuerlein, A., Salguero-Gómez, R., Camarda, C. G., Schaible, R., Schaible, R., Casper, B. B., Dahlgren, J. P., Ehrlén, J., García, M. B., Menges, E., 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, https://doi.org/10.1038/nature12789.

    Article  ADS  CAS  PubMed  Google Scholar 

  11. Pascual-Torner, M., Carrero, D., Pérez-Silva, J. G., Álvarez-Puente, D., Roiz-Valle, D., Bretones, G., Rodríguez, D., Maeso, D., Mateo-González, E., Español, Y., Mariño, G., Acuña, J. L., Quesada, V., and López-Otín, C. (2022) Comparative genomics of mortal and immortal cnidarians unveils novel keys behind rejuvenation, Proc. Natl. Acad. Sci. USA, 119, e2118763119, https://doi.org/10.1073/pnas.2118763119.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Martínez, D. E. (1998) Mortality patterns suggest lack of senescence in hydra, Exp. Gerontol., 33, 217-225, https://doi.org/10.1016/s0531-5565(97)00113-7.

    Article  PubMed  Google Scholar 

  13. Bilinski, T., Bylak, A., and Zadrag-Tecza, R. (2016) Principles of alternative gerontology, Aging (Albany NY), 8, 589-602, https://doi.org/10.18632/aging.100931.

    Article  PubMed  Google Scholar 

  14. Bilinski, T., Bylak, A., Kukuła, K., and Zadrag-Tecza, R. (2021) Senescence as a trade-off between successful land colonisation and longevity: critical review and analysis of a hypothesis, PeerJ, 9, e12286, https://doi.org/10.7717/peerj.12286.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Shilovsky, G. A., Putyatina, T. S., and Markov, A. V. (2022) Evolution of longevity as a species-specific trait in mammals, Biochemistry (Moscow), 87, 1579-1599, https://doi.org/10.1134/S0006297922120148.

    Article  CAS  PubMed  Google Scholar 

  16. Martinez, D. E., and Levinton, J. S. (1992) Asexual metazoans undergo senescence, Proc. Natl. Acad. Sci. USA, 89, 9920-9923, https://doi.org/10.1073/pnas.89.20.9920.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  17. Healy, K., Ezard, T. H. G., Jones, O. R., Salguero-Gómez, R., and Buckley, Y. M. (2019) Animal life history is shaped by the pace of life and the distribution of age-specific mortality and reproduction, Nat. Ecol. Evol., 3, 1217-1224, https://doi.org/10.1038/s41559-019-0938-7.

    Article  PubMed  Google Scholar 

  18. Hoekstra, L. A., Schwartz, T. S., Sparkman, A. M., Miller, D. A. W., and Bronikowski, A. M. (2020) The untapped potential of reptile biodiversity for understanding how and why animals age, Funct. Ecol., 34, 38-54, https://doi.org/10.1111/1365-2435.13450.

    Article  PubMed  Google Scholar 

  19. Dart, A. (2022) Peto’s paradox put to the test, Nat. Rev. Cancer, 22, 129, https://doi.org/10.1038/s41568-022-00447-4.

    Article  CAS  PubMed  Google Scholar 

  20. De Magalhães, J. P., and Costa, J. (2009) A database of vertebrate longevity records and their relation to other life–history traits, J. Evol. Biol., 22, 1770-1774, https://doi.org/10.1111/j.1420-9101.2009.01783.x.

    Article  PubMed  Google Scholar 

  21. Martin, F. J., Amode, M. R., Aneja, A., Austine-Orimoloye, O., Azov, A. G., Azov, A. G., Barnes, I., Becker, A., Bennett, R., Berry, A., Bhai, J., Bhurji, S. K., Bignell, A., Boddu, S., Branco Lins, P. R., Brooks, L., Ramaraju, S. B., Charkhchi, M., Cockburn, A., Da Rin Fiorretto, L., Davidson, C., Dodiya, K., Donaldson, S., El Houdaigui, B., El Naboulsi, T., et al. (2023) Ensembl 2023, Nucleic Acids Res., 51, 933-941, https://doi.org/10.1093/nar/gkac958.

    Article  CAS  Google Scholar 

  22. Nielsen, J., Hedeholm, R. B., Heinemeier, J., Bushnell, P. G., Christiansen, J. S., Olsen, J., Ramsey, C. B., Brill, R. W., Simon, M., Steffensen, K. F., and Steffensen, J. F. (2016) Eye lens radiocarbon reveals centuries of longevity in the Greenland shark (Somniosus microcephalus), Science, 353, 702-704, https://doi.org/10.1126/science.aaf1703.

    Article  ADS  CAS  PubMed  Google Scholar 

  23. Congdon, J. D., Nagle, R. D., Kinney, O. M., van Loben Sels, R. C., Quinter, T., and Tinkle, D. W. (2003) Testing hypotheses of aging in long-lived painted turtles (Chrysemys picta), Exp. Gerontol., 38, 765772, https://doi.org/10.1016/s0531-5565(03)00106-2.

    Article  Google Scholar 

  24. Voituron, Y., De Fraipont, M., Issartel, J., Guillaume, O., and Clobert, J. (2011) Extreme lifespan of the human fish (Proteus anguinus): a challenge for ageing mechanisms, Biol. Lett., 7, 105107, https://doi.org/10.1098/rsbl.2010.0539.

    Article  Google Scholar 

  25. Kostanjšek, R., Diderichsen, B., Recknagel, H., Gunde-Cimerman, N., Gostinčar, C., Fan, G., Kordiš, D., Trontelj, P., Jiang, H., Bolund, L., and Luo, Y. (2022) Toward the massive genome of Proteus anguinus-illuminating longevity, regeneration, convergent evolution, and metabolic disorders, Ann. N. Y. Acad. Sci., 1507, 5-11, https://doi.org/10.1111/nyas.14686.

    Article  ADS  PubMed  Google Scholar 

  26. Voituron, Y., Guillaume, O., Dumet, A., Zahn, S., Criscuolo, F. (2023) Temperature-independent telomere lengthening with age in the long-lived human fish (Proteus anguinus), Proc. Biol. Sci., 290, 20230503, https://doi.org/10.1098/rspb.2023.0503.

    Article  CAS  PubMed  Google Scholar 

  27. Delhaye, J., Salamin, N., Roulin, A., Criscuolo, F., Bize, P., and Christe, P. (2016) Interspecific correlation between red blood cell mitochondrial ROS production, cardiolipin content and longevity in birds, Age (Dordr), 38, 433-443, https://doi.org/10.1007/s11357-016-9940-z.

    Article  CAS  PubMed  Google Scholar 

  28. Amir, Y., Insler, M., Giller, A., Gutman, D., and Atzmon, G. (2020) Senescence and longevity of sea urchins, Genes (Basel), 11, 573, https://doi.org/10.3390/genes11050573.

    Article  CAS  PubMed  Google Scholar 

  29. Medina-Feliciano, J. G., and García-Arrarás, J. E. (2021) Regeneration in echinoderms: molecular advancements, Front. Cell. Dev. Biol., 9, 768641, https://doi.org/10.3389/fcell.2021.768641.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Korotkova, D. D., Lyubetsky, V. A., Ivanova, A. S., Rubanov, L. I., Seliverstov, A. V., Zverkov, O. A., Martynova, N. Y., Nesterenko, A. M., Tereshina, M. B., Peshkin, L., and Zaraisky, A. G. (2019) Bioinformatics screening of genes specific for well-regenerating vertebrates reveals c-answer, a regulator of brain development and regeneration, Cell Rep., 29, 1027-1040.e6, https://doi.org/10.1016/j.celrep.2019.09.038.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Kolora, S. R. R., Owens, G. L., Vazquez, J. M., Stubbs, A., Chatla, K., Jainese, C., Seeto, K., McCrea, M., Sandel, M. W., Vianna, J. A., Maslenikov, K., Bachtrog, D., Orr, J. W., Love, M., and Sudmant, P. H. (2021) Origins and evolution of extreme life span in Pacific Ocean rockfishes, Science, 374, 842-847, https://doi.org/10.1126/science.abg5332.

    Article  ADS  CAS  PubMed  Google Scholar 

  32. Reinke, B. A., Cayuela, H., Janzen, F. J., Lemaître, J. F., Gaillard, J. M., Lawing, A. M., Iverson, J. B., Christiansen, D. G., Martínez-Solano, I., Sánchez-Montes, G., Gutiérrez-Rodríguez, J., Rose, F. L., Nelson, N., Keall, S., Crivelli, A. J., Nazirides, T., Grimm-Seyfarth, A., Henle, K., Mori, E., Guiller, G., Homan, R., Olivier, A., Muths, E., Hossack, B. R., Bonnet, X., et al. (2022) Diverse aging rates in ectothermic tetrapods provide insights for the evolution of aging and longevity, Science, 376, 1459-1466, https://doi.org/10.1126/science.abm0151.

    Article  ADS  PubMed  Google Scholar 

  33. Skulachev, V. P., Holtze, S., Vyssokikh, M. Y., Bakeeva, L. E., Skulachev, M. V., Markov, A. V., Hildebrandt, T. B., and Sadovnichii, V. A. (2017) Neoteny, prolongation of youth: From naked mole rats to “naked apes” (humans), Physiol. Rev., 97, 699-720, https://doi.org/10.1152/physrev.00040.2015.

    Article  PubMed  Google Scholar 

  34. Skulachev, V. P., Shilovsky, G. A., Putyatina, T. S., Popov, N. A., Markov, A. V., Skulachev, M. V., and Sadovnichii, V. A. (2020) Perspectives of Homo sapiens lifespan extension: focus on external or internal resources? Aging (Albany NY), 12, 5566-5584, https://doi.org/10.18632/aging.102981.

    Article  PubMed  Google Scholar 

  35. Wilkinson, P. M., Rainwater, T. R., Woodward, A. R., Leone, E. H., and Carter, C. (2016) Determinate growth and reproductive lifespan in the American alligator (Alligator mississippiensis): evidence from long-term recaptures, Copeia, 104, 843-852, https://doi.org/10.1643/CH-16-430.

    Article  Google Scholar 

  36. Moreira, M. O., Qu, Y. F., and Wiens, J. J. (2021) Large-scale evolution of body temperatures in land vertebrates, Evol. Lett., 5, 484-494, https://doi.org/10.1002/evl3.249.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Clarke, A., and Pörtner, H. O. (2010) Temperature, metabolic power and the evolution of endothermy, Biol. Rev., 85, 703-727, https://doi.org/10.1111/j.1469-185X.2010.00122.x.

    Article  PubMed  Google Scholar 

  38. Skulachev, M. V., Severin, F. F., and Skulachev, V. P. (2015) Aging as an evolvability-increasing program which can be switched off by organism to mobilize additional resources for survival, Curr. Aging Sci., 8, 95-109, https://doi.org/10.2174/1874609808666150422122401.

    Article  PubMed  Google Scholar 

  39. Skulachev, V. P., Vyssokikh, M. Y., Chernyak, B. V., Averina, O. A., Andreev-Andrievskiy, A. A., Zinovkin, R. A., Lyamzaev, K. G., Marey, M. V., Egorov, M. V., Frolova, O. J., Zorov, D. B., Skulachev, M. V., and Sadovnichii, V. A. (2023) Mitochondrion-targeted antioxidant SkQ1 prevents rapid animal death caused by highly diverse shocks, Sci. Rep., 13, 4326, https://doi.org/10.1038/s41598-023-31281-31289.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  40. Skulachev, V. P., Vyssokikh, M. Y., Chernyak, B. V., Mulkidjanian, A. Y., Skulachev, M. V., Shilovsky, G. A., Lyamzaev, K. G., Borisov, V. B., Severin, F. F., and Sadovnichii, V. A. (2023) Six functions of respiration: isn’t it time to take control over ROS production in mitochondria, and aging along with it? Int. J. Mol. Sci., 24, 12540, https://doi.org/10.3390/ijms241612540.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Patnaik, B. K. (1994) Ageing in reptiles, Gerontology, 40, 200-220, https://doi.org/10.1159/000213588.

    Article  CAS  PubMed  Google Scholar 

  42. Alvarez, J. A., and Vaupel, J. W. (2023) Mortality as a function of survival, Demography, 60, 327-342, https://doi.org/10.1215/00703370-10429097.

    Article  PubMed  Google Scholar 

  43. da Silva, R., Conde, D. A., Baudisch, A., and Colchero, F. (2022) Slow and negligible senescence among testudines challenges evolutionary theories of senescence, Science, 376, 1466-1470, https://doi.org/10.1126/science.abl7811.

    Article  ADS  CAS  PubMed  Google Scholar 

  44. Frýdlová, P., Mrzílková, J., Šeremeta, M., Křemen, J., Dudák, J., Žemlička, J., Minnich, B., Kverková, K., Němec, P., Zach, P., and Frynta, D. (2020) Determinate growth is predominant and likely ancestral in squamate reptiles, Proc. Biol. Sci., 287, 20202737, https://doi.org/10.1098/rspb.2020.2737.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Sparkman, A. M., Arnold, S. J., and Bronikowski, A. M. (2007) An empirical test of evolutionary theories for reproductive senescence and reproductive effort in the garter snake Thamnophis elegans, Proc. Biol. Sci., 274, 943-950, https://doi.org/10.1098/rspb.2006.0072.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Kara, T. C. (1994) Ageing in amphibians, Gerontology, 40, 161-173, https://doi.org/10.1159/000213585.

    Article  CAS  PubMed  Google Scholar 

  47. Jiang, Y., Zhao, L., Luan, X., and Liao, W. (2022) Geographical variation in body size and the Bergmann’s rule in Andrew’s toad (Bufo andrewsi), Biology (Basel), 11, 1766, https://doi.org/10.3390/biology11121766.

    Article  PubMed  Google Scholar 

  48. Miller, J. K. (2001) Escaping senescence: demographic data from the three-toed box turtle (Terrapene carolina triunguis), Exp. Gerontol., 36, 829-832.

    Article  CAS  PubMed  Google Scholar 

  49. Warner, D. A., Miller, D. A., Bronikowski, A. M., and Janzen, F. J. (2016) Decades of field data reveal that turtles senesce in the wild, Proc. Natl. Acad. Sci. USA, 113, 6502-6507, https://doi.org/10.1073/pnas.1600035113.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  50. Bronikowski, A. M., Hedrick, A. R., Kutz, G. A., Holden, K. G., Reinke, B., and Iverson, J. B. (2023) Sex-specific innate immunity and ageing in long-lived fresh water turtles (Kinosternon flavescens: Kinosternidae), Immun. Ageing, 20, 11, https://doi.org/10.1186/s12979-023-00335-x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Cayuela, H., Akani, G. C., Hema, E. M., Eniang, E. A., Amadi, N., Ajong, S. N., Dendi, D., Petrozzi, F., and Luiselli, L. (2019) Life history and age-dependent mortality processes in tropical reptiles, Biol. J. Linn. Soc. Lond., 128, 251-262, https://doi.org/10.1093/biolinnean/blz103.

    Article  Google Scholar 

  52. Shilovsky, G. A., Putyatina, T. S., Markov, A. V., and Skulachev, V. P. (2015) Contribution of quantitative methods of estimating mortality dynamics to explaining mechanisms of aging, Biochemistry (Moscow), 80, 1547-1559, https://doi.org/10.1134/S0006297915120020.

    Article  CAS  PubMed  Google Scholar 

  53. Shilovsky, G. A., Putyatina, T. S., Ashapkin, V. V., Luchkina, O. S., and Markov, A. V. (2017) Coefficient of variation of lifespan across the tree of life: is it a signature of programmed aging? Biochemistry (Moscow), 82, 1480-1492, https://doi.org/10.1134/S0006297917120070.

    Article  CAS  PubMed  Google Scholar 

  54. Gavrilova, N. S., Gavrilov, L. A., Severin, F. F., and Skulachev, V. P. (2012) Testing predictions of the programmed and stochastic theories of aging: comparison of variation in age at death, menopause, and sexual maturation, Biochemistry (Moscow), 77, 754-760, https://doi.org/10.1134/S0006297912070085.

    Article  CAS  PubMed  Google Scholar 

  55. Finch, C. E., and Tanzi, R. E. (1997) Genetics of aging, Science, 278, 407-411, https://doi.org/10.1126/science.278.5337.407.

    Article  ADS  CAS  PubMed  Google Scholar 

  56. Bronikowski, A. M. (2008) The evolution of aging phenotypes in snakes: a review and synthesis with new data, Age (Dordr), 30, 169-176, https://doi.org/10.1007/s11357-008-9060-5.

    Article  CAS  PubMed  Google Scholar 

  57. Robert, K. A., and Bronikowski, A. M. (2010) Evolution of senescence in nature: physiological evolution in populations of garter snake with divergent life histories, Am. Nat., 175, 147-159, https://doi.org/10.1086/649595.

    Article  PubMed  Google Scholar 

  58. Olsson, M., Wapstra, E., and Friesen, C. (2018) Ectothermic telomeres: it’s time they came in from the cold, Philos. Trans. R. Soc. Lond. B Biol. Sci., 373, 20160449, https://doi.org/10.1098/rstb.2016.0449.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Holtze, S., Gorshkova, E., Braude, S., Cellerino, A., Dammann, P., Hildebrandt, T. B., Hoeflich, A., Hoffmann, S., Koch, P., Terzibasi Tozzini, E., Skulachev, M., Skulachev, V. P., and Sahm, A. (2021) Alternative animal models of aging research, Front. Mol. Biosci., 8, 660959, https://doi.org/10.3389/fmolb.2021.660959.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Omotoso, O., Gladyshev, V. N., and Zhou, X. (2021) Lifespan extension in long-lived vertebrates rooted in ecological adaptation, Front. Cell. Dev. Biol., 9, 704966, https://doi.org/10.3389/fcell.2021.704966.

    Article  PubMed  PubMed Central  Google Scholar 

  61. Botha, J., Weiss, B. M., Dollman, K., Barrett, P. M., Benson, R. B. J., and Choiniere, J. N. (2023) Origins of slow growth on the crocodilian stem lineage, Curr. Biol., 8, 4261-4268.e3, https://doi.org/10.1016/j.cub.2023.08.057.

    Article  CAS  Google Scholar 

  62. Ripple, W. J., Newsome, T. M., Wolf, C., Dirzo, R., Everatt, K. T., Galetti, M., Hayward, M. W., Kerley, G. I., Levi, T., Lindsey, P. A., Macdonald, D. W., Malhi, Y., Painter, L. E., Sandom, C. J., Terborgh, J., and Van Valkenburgh, B. (2015) Collapse of the world’s largest herbivores, Sci. Adv., 1, e1400103, https://doi.org/10.1126/sciadv.1400103.

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  63. Fraser, D., Villasenor, A., Toth, A. B., Balk, M. A., Eronen, J. T., Andrew Barr, W., Behrensmeyer, A. K., Davis, M., Du, A., Tyler Faith, J., Graves, G. R., Gotelli, N. J., Jukar, A. M., Looy, C. V., McGill, B. J., Miller, J. H., Pineda-Munoz, S., Potts, R., Shupinski, A. B., Soul, L. C., and Kathleen Lyons, S. (2022) Late quaternary biotic homogenization of North American mammalian faunas, Nat. Commun., 13, 3940, https://doi.org/10.1038/s41467-022-31595-8.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  64. Stockdale, M. T., Benton, M. J. (2021) Environmental drivers of body size evolution in crocodile-line archosaurs, Commun. Biol., 4, 38, https://doi.org/10.1038/s42003-020-01561-5.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Legendre, L. J., Guénard, G., Botha-Brink, J., and Cubo, J. (2016) Palaeohistological evidence for ancestral high metabolic rate in archosaurs, Syst. Biol., 65, 989-996, https://doi.org/10.1093/sysbio/syw033.

    Article  PubMed  Google Scholar 

  66. Wiemann, J., Menéndez, I., Crawford, J. M., Fabbri, M., Gauthier, J. A., Hull, P. M., Norell, M. A., and Briggs, D. E. G. (2022) Fossil biomolecules reveal an avian metabolism in the ancestral dinosaur, Nature, 606, 522-526, https://doi.org/10.1038/s41586-022-04770-6.

    Article  ADS  CAS  PubMed  Google Scholar 

  67. Schmalhausen, I. I. (1982) Organism as a whole in its individual and historic development, in Izbrannye trudy (Selected works) [In Russian], Nauka, Moscow.

  68. Edmonds, D., Dreslik, M. J., Lovich, J. E., Wilson, T. P., and Ernst, C. H. (2021) Growing as slow as a turtle: unexpected maturational differences in a small, long-lived species, PLoS One, 16, e0259978, https://doi.org/10.1371/journal.pone.0259978.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Omeyer, L. C. M., Fuller, W. J., Godley, B. J., Snape, R. T. E., and Broderick, A. C. (2018) Determinate or indeterminate growth? Revisiting the growth strategy of sea turtles, Marine Ecol. Progr. Ser., 596, 199-211, https://doi.org/10.3354/meps12570.

    Article  ADS  Google Scholar 

  70. Hariharan, I. K., Wake, D. B., and Wake, M. H. (2015) Indeterminate growth: could it represent the ancestral condition? Cold Spring Harb. Perspect. Biol., 8, a019174, https://doi.org/10.1101/cshperspect.a019174.

    Article  PubMed  Google Scholar 

  71. Derocher, A. E., and Wiig, O. (2002) Postnatal growth in body length and mass of polar bears (Ursus maritimus) at Svalbard, J. Zool., 256, 343-349, https://doi.org/10.1017/S0952836902000377.

    Article  Google Scholar 

  72. McKenzie, J., Page, B., Goldsworthy, S. D., and Hindell, M. A. (2007) Growth strategies of New Zealand fur seals in southern Australia, J. Zool., 272, 377-389, https://doi.org/10.1111/j.1469-7998.2006.00278.x.

    Article  Google Scholar 

  73. Mumby, H. S., Chapman, S. N., Crawley, J. A. H., Mar, K. U., Htut, W., Soe, A. T., Aung, H. H., and Lummaa, V. (2015) Distinguishing between determinate and indeterminate growth in a long-lived mammal, BMC Evol. Biol., 15, 214, https://doi.org/10.1186/s12862-015-0487-x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Shine, R., and Charnov, E. L. (1992) Patterns of survival, growth, and maturation in snakes and lizards, Am. Naturalist, 139, 1257-1269, https://doi.org/10.1086/285385.

    Article  Google Scholar 

  75. Shine, R., and Iverson, J. B. (1995) Patterns of survival, growth and maturation in turtles, Oikos, 72, 343-348, https://doi.org/10.2307/3546119.

    Article  ADS  Google Scholar 

  76. Harris, R. J., and Arbuckle, K. (2016) Tempo and mode of the evolution of venom and poison in tetrapods, Toxins (Basel), 8, 193, https://doi.org/10.3390/toxins8070193.

    Article  CAS  PubMed  Google Scholar 

  77. Stark, G. (2022) Large and expensive brain comes with a short lifespan: the relationship between brain size and longevity among fish taxa, J. Fish. Biol., 101, 92-99, https://doi.org/10.1111/jfb.15074.

    Article  PubMed  PubMed Central  Google Scholar 

  78. Stark, G., and Pincheira-Donoso, D. (2022) The evolution of brain size in ectothermic tetrapods: large brain mass trades-off with lifespan in reptiles, Evol. Biol., 49, 180-188, https://doi.org/10.1007/s11692-022-09562-4.

    Article  Google Scholar 

  79. Yu, X., Zhong, M. J., Li, D. Y., Jin, L., Liao, W. B., and Kotrschal, A. (2018) Large-brained frogs mature later and live longer, Evolution, 72, 1174-1183, https://doi.org/10.1111/evo.13478.

    Article  PubMed  Google Scholar 

  80. 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.

    CAS  PubMed  Google Scholar 

  81. Lidsky, P. V., Yuan, J., Rulison, J. M., and Andino-Pavlovsky, R. (2022) Is aging an inevitable characteristic of organic life or an evolutionary adaptation? Biochemistry (Moscow), 87, 1413-1445, https://doi.org/10.1134/S0006297922120021.

    Article  CAS  PubMed  Google Scholar 

  82. Bronikowski, A., and Vleck, D. (2010) Metabolism, body size and life span: a case study in evolutionarily divergent populations of the garter snake (Thamnophis elegans), Integr. Comp. Biol., 50, 880-887, https://doi.org/10.1093/icb/icq132.

    Article  PubMed  Google Scholar 

  83. Dammann, P., Šaffa, G., and Šumbera, R. (2022) Longevity of a solitary mole-rat species and its implications for the assumed link between sociality and longevity in African mole-rats (Bathyergidae), Biol. Lett., 18, 20220243, https://doi.org/10.1098/rsbl.2022.0243.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Burgin, C. J., Colella, J. P., Kahn, P. L., and Upham, N. S. (2018) How many species of mammals are there? J. Mammal., 99, 1-14, https://doi.org/10.1093/jmammal/gyx147.

    Article  Google Scholar 

  85. Giaimo, S., and Traulsen, A. (2022) The selection force weakens with age because ageing evolves and not vice versa, Nat. Commun., 13, 686, https://doi.org/10.1038/s41467-022-28254-3.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  86. Prum, R. O., Berv, J. S., Dornburg, A., Field, D. J., Townsend, J. P., Lemmon, E. M., and Lemmon, A. R. (2015) A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing, Nature, 526, 569-573, https://doi.org/10.1038/nature15697.

    Article  ADS  CAS  PubMed  Google Scholar 

  87. Rotger, A., Tenan, S., Igual, J. M., Bonner, S., and Tavecchia, G. (2023) Life span, growth, senescence and island syndrome: Accounting for imperfect detection and continuous growth, J. Anim. Ecol., 9, 183-194, https://doi.org/10.1111/1365-2656.13842.

    Article  Google Scholar 

  88. Van Schaik, C. P., Song, Z., Schuppli, C., Drobniak, S. M., Heldstab, S. A., Griesser, M. (2023) Extended parental provisioning and variation in vertebrate brain sizes, PLoS Biol., 21, e3002016, https://doi.org/10.1371/journal.pbio.3002016.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Sacher, G. A. (1968) Molecular versus systemic theories on the genesis of ageing, Exp. Gerontol., 3, 265-271, https://doi.org/10.1016/0531-5565(68)90011-9.

    Article  CAS  PubMed  Google Scholar 

  90. Knope, M. L., Bush, A. M., Frishkoff, L. O., Heim, N. A., and Payne, J. L. (2020) Ecologically diverse clades dominate the oceans via extinction resistance, Science, 367, 1035-1038, https://doi.org/10.1126/science.aax6398.

    Article  ADS  CAS  PubMed  Google Scholar 

  91. Lewis, K. N., Wason, E., Edrey, Y. H., Kristan, D. M., Nevo, E., and Buffenstein, R. (2015) Regulation of Nrf2 signaling and longevity in naturally long-lived rodents, Proc. Natl. Acad. Sci. USA, 112, 3722-3727, https://doi.org/10.1073/pnas.1417566112.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  92. Shilovsky, G. A., Shram, S. I., Morgunova, G. V., and Khokhlov, A. N. (2017) Protein poly(ADP-ribosyl)ation system: Changes in development and aging as well as due to restriction of cell proliferation, Biochemistry (Moscow), 82, 1391-1401, https://doi.org/10.1134/S0006297917110177.

    Article  CAS  PubMed  Google Scholar 

  93. Shilovsky, G. A. (2022) Lability of the Nrf2/Keap/ARE cell defense system in different models of cell aging and age-related pathologies, Biochemistry (Moscow), 87, 70-85, https://doi.org/10.1134/S0006297922010060.

    Article  CAS  PubMed  Google Scholar 

  94. Jové, M., Mota-Martorell, N., Fernàndez-Bernal, A., Portero-Otin, M., Barja, G., and Pamplona, R. (2023) Phenotypic molecular features of long-lived animal species, Free Radic. Biol. Med., 208, 728-747, https://doi.org/10.1016/j.freeradbiomed.2023.09.023.

    Article  CAS  PubMed  Google Scholar 

  95. Rafikova, E., Nemirovich-Danchenko, N., Ogmen, A., Parfenenkova, A., Velikanova, A., Tikhonov, S., Peshkin, L., Rafikov, K., Spiridonova, O., Belova, Y., Glinin, T., Egorova, A., and Batin, M. (2023) Open Genes – a new comprehensive database of human genes associated with aging and longevity, Nucleic Acids Res., 52, gkad712, https://doi.org/10.1093/nar/gkad712.

    Article  Google Scholar 

  96. Vyssokikh, M. Y., Holtze, S., Averina, O. A., Lyamzaev, K. G., Panteleeva, A. A., Marey, M. V., Zinovkin, R. A., Severin, F. F., Skulachev, M. V., Fasel, N., Hildebrandt, T. B., and Skulachev, V. P. (2020) Mild depolarization of the inner mitochondrial membrane is a crucial component of an antiaging program, Proc. Natl. Acad. Sci. USA, 117, 64916501, https://doi.org/10.1073/pnas.1916414117.

    Article  CAS  Google Scholar 

  97. Odeh, A., Eddini, H., Shawasha, L., Chaban, A., Avivi, A., Shams, I., and Manov, I. (2023) Senescent secretome of blind mole rat Spalax inhibits malignant behavior of human breast cancer cells triggering bystander senescence and targeting inflammatory response, Int. J. Mol. Sci., 24, 5132, https://doi.org/10.3390/ijms24065132.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Yakovleva, E. U., Naimark, E. B., and Markov, A. V. (2016) Adaptation of Drosophila melanogaster to unfavorable growth medium affects lifespan and age-related fecundity, Biochemistry (Moscow), 81, 1445-1460, https://doi.org/10.1134/S0006297916120063.

    Article  CAS  PubMed  Google Scholar 

  99. Jacobs, P. J., Hart, D. W., Merchant, H. N., Voigt, C., and Bennett, N. C. (2023) The evolution and ecology of oxidative and antioxidant status: a comparative approach in African mole-rats, Antioxidants (Basel), 12, 1486, https://doi.org/10.3390/antiox12081486.

    Article  CAS  PubMed  Google Scholar 

  100. Tyshkovskiy, A., Ma, S., Shindyapina, A. V., Tikhonov, S., Lee, S. G., Bozaykut, P., Castro, J. P., Seluanov, A., Schork, N. J., Gorbunova, V., Dmitriev, S. E., Miller, R. A., and Gladyshev, V. N. (2023) Distinct longevity mechanisms across and within species and their association with aging, Cell, 186, 2929-2949.e20, https://doi.org/10.1016/j.cell.2023.05.002.

    Article  CAS  PubMed  Google Scholar 

  101. Grosfeld, E. V., Bidiuk, V. A., Mitkevich, O. V., Ghazy, E. S. M. O., Kushnirov, V. V., and Alexandrov, A. I. (2021) A systematic survey of characteristic features of yeast cell death triggered by external factors, J. Fungi (Basel), 7, 886, https://doi.org/10.3390/jof7110886.

    Article  CAS  PubMed  Google Scholar 

  102. Khan, I., Yousif, A., Chesnokov, M., Hong, L., and Chefetz, I. (2021) A decade of cell death studies: breathing new life into necroptosis, Pharmacol. Ther., 220, 107717, https://doi.org/10.1016/j.pharmthera.2020.107717.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors are grateful to S. V. Ogurtsov (Department of Vertebrate Zoology), A. V. Seliverstov, and O. S. Luchkina for their valuable advice while writing the article.

Funding

This work was supported by ongoing institutional funding. No additional grants to carry out or direct this particular research were obtained.

Author information

Authors and Affiliations

  1. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, 119991, Moscow, Russia

    Gregory A. Shilovsky

  2. Faculty of Biology, Lomonosov Moscow State University, 119234, Moscow, Russia

    Gregory A. Shilovsky, Tatyana S. Putyatina & Alexander V. Markov

  3. Institute for Information Transmission Problems (Kharkevich Institute), Russian Academy of Sciences, 127051, Moscow, Russia

    Gregory A. Shilovsky

Authors
  1. Gregory A. Shilovsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tatyana S. Putyatina
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alexander V. Markov
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

G.A.S. developed the concept of the work, T.S.P., A.V.M., and G.A.S. wrote and edited the manuscript and prepared tables and figure.

Corresponding author

Correspondence to Gregory A. Shilovsky.

Ethics declarations

This work does not contain any studies involving human and animal subjects. The authors of this work declare that they have no conflicts of interest.

Additional information

Publisher’s Note. Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shilovsky, G.A., Putyatina, T.S. & Markov, A.V. Evolution of Longevity in Tetrapods: Safety Is More Important than Metabolism Level. Biochemistry Moscow 89, 322–340 (2024). https://doi.org/10.1134/S0006297924020111

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297924020111

Keywords

Search

Navigation