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Proc Biol Sci. 2003 July 7; 270(1522): 1387–1392.
PMCID: PMC1691385

Telomeres shorten more slowly in long-lived birds and mammals than in short-lived ones.


We know very little about physiological constraints on the evolution of life-history traits in general, and, in particular, about physiological and molecular adjustments that accompany the evolution of variation in lifespan. Identifying mechanisms that underlie adaptive variation in lifespan should provide insight into the evolution of trade-offs between lifespan and other life-history traits. Telomeres, the DNA caps at the ends of linear chromosomes, usually shorten as animals age, but whether telomere rate of change is associated with lifespan is unknown. We measured telomere length in erythrocytes from five bird species with markedly different lifespans. Species with shorter lifespans lost more telomeric repeats with age than species with longer lifespans. A similar correlation is seen in mammals. Furthermore, telomeres did not shorten with age in Leach's storm-petrels, an extremely long-lived bird, but actually lengthened. This novel finding suggests that regulation of telomere length is associated not only with cellular replicative lifespan, but also with organismal lifespan, and that very long-lived organisms have escaped entirely any telomeric constraint on cellular replicative lifespan.

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Selected References

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  • Austad SN. An experimental paradigm for the study of slowly aging organisms. Exp Gerontol. 2001 Apr;36(4-6):599–605. [PubMed]
  • Barja G, Herrero A. Oxidative damage to mitochondrial DNA is inversely related to maximum life span in the heart and brain of mammals. FASEB J. 2000 Feb;14(2):312–318. [PubMed]
  • Barja G, Cadenas S, Rojas C, Pérez-Campo R, López-Torres M. Low mitochondrial free radical production per unit O2 consumption can explain the simultaneous presence of high longevity and high aerobic metabolic rate in birds. Free Radic Res. 1994 Oct;21(5):317–327. [PubMed]
  • Counter CM, Avilion AA, LeFeuvre CE, Stewart NG, Greider CW, Harley CB, Bacchetti S. Telomere shortening associated with chromosome instability is arrested in immortal cells which express telomerase activity. EMBO J. 1992 May;11(5):1921–1929. [PubMed]
  • Coviello-McLaughlin GM, Prowse KR. Telomere length regulation during postnatal development and ageing in Mus spretus. Nucleic Acids Res. 1997 Aug 1;25(15):3051–3058. [PMC free article] [PubMed]
  • Feng YR, Norwood D, Shibata R, Gee D, Xiao X, Martin M, Zeichner SL, Dimitrov DS. Telomere dynamics in HIV-1 infected and uninfected chimpanzees measured by an improved method based on high-resolution two-dimensional calibration of DNA sizes. J Med Primatol. 1998 Oct;27(5):258–265. [PubMed]
  • Feng YR, Biggar RJ, Gee D, Norwood D, Zeichner SL, Dimitrov DS. Long-term telomere dynamics: modest increase of cell turnover in HIV-infected individuals followed for up to 14 years. Pathobiology. 1999;67(1):34–38. [PubMed]
  • Forsyth Nicholas R, Wright Woodring E, Shay Jerry W. Telomerase and differentiation in multicellular organisms: turn it off, turn it on, and turn it off again. Differentiation. 2002 Jan;69(4-5):188–197. [PubMed]
  • Frenck RW, Jr, Blackburn EH, Shannon KM. The rate of telomere sequence loss in human leukocytes varies with age. Proc Natl Acad Sci U S A. 1998 May 12;95(10):5607–5610. [PubMed]
  • Friedrich U, Griese E, Schwab M, Fritz P, Thon K, Klotz U. Telomere length in different tissues of elderly patients. Mech Ageing Dev. 2000 Nov 15;119(3):89–99. [PubMed]
  • Goldstein S. Replicative senescence: the human fibroblast comes of age. Science. 1990 Sep 7;249(4973):1129–1133. [PubMed]
  • Greider CW, Blackburn EH. Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell. 1985 Dec;43(2 Pt 1):405–413. [PubMed]
  • Harley CB, Kim NW, Prowse KR, Weinrich SL, Hirsch KS, West MD, Bacchetti S, Hirte HW, Counter CM, Greider CW, et al. Telomerase, cell immortality, and cancer. Cold Spring Harb Symp Quant Biol. 1994;59:307–315. [PubMed]
  • HARMAN D. Aging: a theory based on free radical and radiation chemistry. J Gerontol. 1956 Jul;11(3):298–300. [PubMed]
  • Hastie ND, Dempster M, Dunlop MG, Thompson AM, Green DK, Allshire RC. Telomere reduction in human colorectal carcinoma and with ageing. Nature. 1990 Aug 30;346(6287):866–868. [PubMed]
  • Hemann MT, Strong MA, Hao LY, Greider CW. The shortest telomere, not average telomere length, is critical for cell viability and chromosome stability. Cell. 2001 Oct 5;107(1):67–77. [PubMed]
  • Henson Jeremy D, Neumann Axel A, Yeager Thomas R, Reddel Roger R. Alternative lengthening of telomeres in mammalian cells. Oncogene. 2002 Jan 21;21(4):598–610. [PubMed]
  • Ku HH, Sohal RS. Comparison of mitochondrial pro-oxidant generation and anti-oxidant defenses between rat and pigeon: possible basis of variation in longevity and metabolic potential. Mech Ageing Dev. 1993 Nov;72(1):67–76. [PubMed]
  • Lee Won-Woo, Nam Ki-Hoan, Terao Keiji, Yoshikawa Yasuhiro. Age-related telomere length dynamics in peripheral blood mononuclear cells of healthy cynomolgus monkeys measured by Flow FISH. Immunology. 2002 Apr;105(4):458–465. [PubMed]
  • McClintock B. The Stability of Broken Ends of Chromosomes in Zea Mays. Genetics. 1941 Mar;26(2):234–282. [PubMed]
  • Miyashita Norikazu, Shiga Kazuho, Yonai Miharu, Kaneyama Kanako, Kobayashi Shuji, Kojima Toshiyuki, Goto Yuji, Kishi Masao, Aso Hisashi, Suzuki Toshiyuki, et al. Remarkable differences in telomere lengths among cloned cattle derived from different cell types. Biol Reprod. 2002 Jun;66(6):1649–1655. [PubMed]
  • Nasir L, Devlin P, Mckevitt T, Rutteman G, Argyle DJ. Telomere lengths and telomerase activity in dog tissues: a potential model system to study human telomere and telomerase biology. Neoplasia. 2001 Jul-Aug;3(4):351–359. [PMC free article] [PubMed]
  • Ogburn CE, Carlberg K, Ottinger MA, Holmes DJ, Martin GM, Austad SN. Exceptional cellular resistance to oxidative damage in long-lived birds requires active gene expression. J Gerontol A Biol Sci Med Sci. 2001 Nov;56(11):B468–B474. [PubMed]
  • Prowse KR, Greider CW. Developmental and tissue-specific regulation of mouse telomerase and telomere length. Proc Natl Acad Sci U S A. 1995 May 23;92(11):4818–4822. [PubMed]
  • Röhme D. Evidence for a relationship between longevity of mammalian species and life spans of normal fibroblasts in vitro and erythrocytes in vivo. Proc Natl Acad Sci U S A. 1981 Aug;78(8):5009–5013. [PubMed]
  • Shibata R, Feng YR, Gee D, Norwood D, Xiao X, Zeichner SL, Martin MA, Dimitrov DS. Telomere dynamics in monkeys: increased cell turnover in macaques infected with chimeric simian-human immunodeficiency viruses. J Med Primatol. 1999 Feb;28(1):1–10. [PubMed]
  • Shiels PG, Kind AJ, Campbell KH, Waddington D, Wilmut I, Colman A, Schnieke AE. Analysis of telomere lengths in cloned sheep. Nature. 1999 May 27;399(6734):316–317. [PubMed]
  • Sohal RS, Svensson I, Brunk UT. Hydrogen peroxide production by liver mitochondria in different species. Mech Ageing Dev. 1990 Apr 30;53(3):209–215. [PubMed]
  • Vaziri H, Schächter F, Uchida I, Wei L, Zhu X, Effros R, Cohen D, Harley CB. Loss of telomeric DNA during aging of normal and trisomy 21 human lymphocytes. Am J Hum Genet. 1993 Apr;52(4):661–667. [PubMed]
  • Vaziri H, Dragowska W, Allsopp RC, Thomas TE, Harley CB, Lansdorp PM. Evidence for a mitotic clock in human hematopoietic stem cells: loss of telomeric DNA with age. Proc Natl Acad Sci U S A. 1994 Oct 11;91(21):9857–9860. [PubMed]
  • von Zglinicki T, Pilger R, Sitte N. Accumulation of single-strand breaks is the major cause of telomere shortening in human fibroblasts. Free Radic Biol Med. 2000 Jan 1;28(1):64–74. [PubMed]
  • Watson JD. Origin of concatemeric T7 DNA. Nat New Biol. 1972 Oct 18;239(94):197–201. [PubMed]
  • West MD, Pereira-Smith OM, Smith JR. Replicative senescence of human skin fibroblasts correlates with a loss of regulation and overexpression of collagenase activity. Exp Cell Res. 1989 Sep;184(1):138–147. [PubMed]
  • Yazawa M, Okuda M, Setoguchi A, Iwabuchi S, Nishimura R, Sasaki N, Masuda K, Ohno K, Tsujimoto H. Telomere length and telomerase activity in canine mammary gland tumors. Am J Vet Res. 2001 Oct;62(10):1539–1543. [PubMed]

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