Decline in telomere length with increasing age across nonhuman vertebrates: A meta-analysis.

Publisher: Blackwell Scientific Publications Country of Publication: England NLM ID: 9214478 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1365-294X (Electronic) Linking ISSN: 09621083 NLM ISO Abbreviation: Mol Ecol Subsets: MEDLINE

Original Publication: Oxford, UK : Blackwell Scientific Publications, c1992-

Aging*/genetics ; Vertebrates*/genetics; Adult ; Humans ; Animals ; Telomere/genetics ; Telomere Shortening/genetics

The prediction that telomere length (TL) shortens with increasing age is a major element in considering the role of telomeres as a key player in evolution. While telomere attrition is found in humans both in vitro and in vivo, the increasing number of studies reporting diverse age-specific patterns of TL challenges the hypothesis of a universal decline of TL with increasing age. Here, we performed a meta-analysis to estimate the relationship between TL and age across 175 estimates encompassing 98 species of vertebrates. We found that, on average, TL does decline with increasing age during adulthood. However, this decline was weak and variable across vertebrate classes, and we also found evidence for a publication bias that might weaken our current evidence of decreasing TL with increasing age. We found no evidence for a faster decline in TL with increasing age when considering the juvenile stage (from birth to age at first reproduction) compared to the adult stage. Heterogeneity in TL ageing rates was explained by the method used to measure telomeres: detectable TL declines with increasing age were found only among studies using TRF with in-gel hybridisation and qFISH methods, but not in studies using qPCR and Southern blot-based TRF methods. While we confirmed that TL declines with increasing age in most adult vertebrates, our results identify an influence of telomere measurement methodology, which highlights the need to examine more thoroughly the effect of the method of measurement on TL estimates.
(© 2021 John Wiley & Sons Ltd.)

*Angelier, F., Weimerskirch, H., Barbraud, C., & Chastel, O. (2019). Is telomere length a molecular marker of individual quality? Insights from a long-lived bird. Functional Ecology, 33(6), 1076-1087. https://doi.org/10.1111/1365-2435.13307.
*Argyle, D., Ellsmore, V., Gault, E., Munro, A., & Nasir, L. (2003). Equine telomeres and telomerase in cellular immortalisation and ageing. Mechanisms of Ageing and Development, 124(6), 759-764. https://doi.org/10.1016/S0047-6374(03)00104-0.
*Asghar, M., Bensch, S., Tarka, M., Hansson, B., & Hasselquist, D. (2015). Maternal and genetic factors determine early life telomere length. Proceedings of the Royal Society B: Biological Sciences, 282(1799), 20142263. https://doi.org/10.1098/rspb.2014.2263.
Aubert, G., Baerlocher, G. M., Vulto, I., Poon, S. S., & Lansdorp, P. M. (2012). Collapse of telomere homeostasis in hematopoietic cells caused by heterozygous mutations in telomerase genes. PLoS Genetics, 8(5), e1002696. https://doi.org/10.1371/journal.pgen.1002696.
Aubert, G., & Lansdorp, P. M. (2008). Telomeres and aging. Physiological Reviews, 88(2), 557-579. https://doi.org/10.1152/physrev.00026.2007.
Aviv, A., Hunt, S. C., Lin, J., Cao, X., Kimura, M., & Blackburn, E. (2011). Impartial comparative analysis of measurement of leukocyte telomere length/DNA content by Southern blots and qPCR. Nucleic Acids Research, 39(20), e134. https://doi.org/10.1093/nar/gkr634.
*Aydinonat, D., Penn, D. J., Smith, S., Moodley, Y., Hoelzl, F., Knauer, F., & Schwarzenberger, F. (2014). Social isolation shortens telomeres in African grey parrots (Psittacus erithacus erithacus). PLoS One, 9(4), e93839. https://doi.org/10.1371/journal.pone.0093839.
Barrett, E. L. B., & Richardson, D. S. (2011). Sex differences in telomeres and lifespan. Aging Cell, 10(6), 913-921. https://doi.org/10.1111/j.1474-9726.2011.00741.x.
Bartoń, K. (2019). MuMIn: Multi-model inference (version 1.43.15). https://CRAN.R-project.org/package=MuMIn.
Bates, D., Maechler, M., Bolker, B., Walker, S., Christensen, R. H. B., Singmann, H., Dai, B., Scheipl, F., Grothendieck, G., Green, P., & Fox, J. (2020). lme4: Linear mixed-effects models using “Eigen” and S4 (version 1.1-23). https://CRAN.R-project.org/package=lme4.
*Bauch, C., Boonekamp, J. J., Korsten, P., Mulder, E., & Verhulst, S. (2019). Epigenetic inheritance of telomere length in wild birds. PLOS Genetics, 15(2), e1007827. https://doi.org/10.1371/journal.pgen.1007827.
*Bauch, C., Gatt, M. C., Granadeiro, J. P., Verhulst, S., & Catry, P. (2020). Sex-specific telomere length and dynamics in relation to age and reproductive success in Cory’s shearwaters. Molecular Ecology, 29(7), 1344-1357. https://doi.org/10.1111/mec.15399.
*Bauer, C. M., Graham, J. L., Abolins-Abols, M., Heidinger, B. J., Ketterson, E. D., & Greives, T. J. (2018). Chronological and biological age predict seasonal reproductive timing: An investigation of clutch initiation and telomeres in birds of known age. The American Naturalist, 191(6), 777-782. https://doi.org/10.1086/697224.
*Beaulieu, M., Benoit, L., Abaga, S., Kappeler, P. M., & Charpentier, M. J. E. (2017). Mind the cell: Seasonal variation in telomere length mirrors changes in leucocyte profile. Molecular Ecology, 26(20), 5603-5613. https://doi.org/10.1111/mec.14329.
*Bebbington, K., Spurgin, L. G., Fairfield, E. A., Dugdale, H. L., Komdeur, J., Burke, T., & Richardson, D. S. (2016). Telomere length reveals cumulative individual and transgenerational inbreeding effects in a passerine bird. Molecular Ecology, 25(12), 2949-2960. https://doi.org/10.1111/mec.13670.
Beirne, C., Delahay, R., Hares, M., & Young, A. (2014). Age-related declines and disease-associated variation in immune cell telomere length in a wild mammal. PLoS One, 9(9), e108964. https://doi.org/10.1371/journal.pone.0108964.
*Bichet, C., Bouwhuis, S., Bauch, C., Verhulst, S., Becker, P. H., & Vedder, O. (2020). Telomere length is repeatable, shortens with age and reproductive success, and predicts remaining lifespan in a long-lived seabird. Molecular Ecology, 29(2), 429-441. https://doi.org/10.1111/mec.15331.
*Bize, P., Criscuolo, F., Metcalfe, N. B., Nasir, L., & Monaghan, P. (2009). Telomere dynamics rather than age predict life expectancy in the wild. Proceedings of the Royal Society B: Biological Sciences, 276(1662), 1679-1683. https://doi.org/10.1098/rspb.2008.1817.
Blackburn, E. H. (1991). Structure and function of telomeres. Nature, 350(6319), 569-573. https://doi.org/10.1038/350569a0.
Boonekamp, J. J., Mulder, G. A., Salomons, H. M., Dijkstra, C., & Verhulst, S. (2014). Nestling telomere shortening, but not telomere length, reflects developmental stress and predicts survival in wild birds. Proceedings of the Royal Society B: Biological Sciences, 281(1785), 20133287. https://doi.org/10.1098/rspb.2013.3287.
*Bronikowski, A. M. (2008). The evolution of aging phenotypes in snakes: A review and synthesis with new data. AGE, 30(2-3), 169-176. https://doi.org/10.1007/s11357-008-9060-5.
*Buddhachat, K., Kriangwanich, W., Kumoun, I., Brown, J. L., Chailangkarn, S., Somgird, C., Thitaram, C., Prasitwattanaseree, S., & Nganvongpanit, K. (2017). Telomeric attrition with increasing age in short- (Chihuahua dog) and long- (Asian elephant) life span animals. Kafkas Universitesi Veteriner Fakultesi Dergisi, 23(4), 643-649. https://doi.org/10.9775/kvfd.2017.17504.
Burnham, K. P., & Anderson, D. R. (2002). Model selection and multimodel inference: A practical information-theoretic approach (2nd ed.). Springer-Verlag.
Cawthon, R. M. (2002). Telomere measurement by quantitative PCR. Nucleic Acids Research, 30(10), e47. https://doi.org/10.1093/nar/30.10.e47.
Chatelain, M., Drobniak, S. M., & Szulkin, M. (2020). The association between stressors and telomeres in non-human vertebrates: A meta-analysis. Ecology Letters, 23(2), 381-398. https://doi.org/10.1111/ele.13426.
*Cherdsukjai, P., Buddhachat, K., Brown, J., Kaewkool, M., Poommouang, A., Kaewmong, P., Kittiwattanawong, K., & Nganvongpanit, K. (2020). Age relationships with telomere length, body weight and body length in wild dugong (Dugong dugon). PeerJ, 8, e10319. https://doi.org/10.7717/peerj.10319.
Cheynel, L., Lemaître, J.-F., Gaillard, J.-M., Rey, B., Bourgoin, G., Ferté, H., Jégo, M., Débias, F., Pellerin, M., Jacob, L., & Gilot-Fromont, E. (2017). Immunosenescence patterns differ between populations but not between sexes in a long-lived mammal. Scientific Reports, 7(1), 13700. https://doi.org/10.1038/s41598-017-13686-5.
Cohen (1977). Statistical power analysis for the behavioral sciences (Rev.ed.). Elsevier. https://doi.org/10.1016/C2013-0-10517-X.
*Coviello-McLaughlin, G. M., & Prowse, K. R. (1997). Telomere length regulation during postnatal development and ageing in Mus spretus. Nucleic Acids Research, 25(15), 3051-3058. https://doi.org/10.1093/nar/25.15.3051.
*Criscuolo, F., Pillay, N., Zahn, S., & Schradin, C. (2020). Seasonal variation in telomere dynamics in African striped mice. Oecologia, 194(4), 609-620. https://doi.org/10.1007/s00442-020-04801-x.
Dantzer, B., & Fletcher, Q. E. (2015). Telomeres shorten more slowly in slow-aging wild animals than in fast-aging ones. Experimental Gerontology, 71, 38-47. https://doi.org/10.1016/j.exger.2015.08.012.
Demanelis, K., Jasmine, F., Chen, L. S., Chernoff, M., Tong, L., Delgado, D., Zhang, C., Shinkle, J., Sabarinathan, M., Lin, H., Ramirez, E., Oliva, M., Kim-Hellmuth, S., Stranger, B. E., Lai, T.-P., Aviv, A., Ardlie, K. G., Aguet, F., Ahsan, H., … Pierce, B. L. (2020). Determinants of telomere length across human tissues. Science, 369(6509), eaaz6876. https://doi.org/10.1126/science.aaz6876.
*Denham, J., & Denham, M. M. (2018). Leukocyte telomere length in the Thoroughbred racehorse. Animal Genetics, 49(5), 452-456. https://doi.org/10.1111/age.12681.
*Denham, J., Stevenson, K., & Denham, M. M. (2019). Age-associated telomere shortening in Thoroughbred horses. Experimental Gerontology, 127, 110718. https://doi.org/10.1016/j.exger.2019.110718.
Eastwood, J. R., Mulder, E., Verhulst, S., & Peters, A. (2018). Increasing the accuracy and precision of relative telomere length estimates by RT qPCR. Molecular Ecology Resources, 18(1), 68-78. https://doi.org/10.1111/1755-0998.12711.
Egger, M., Davey Smith, G., Schneider, M., & Minder, C. (1997). Bias in meta-analysis detected by a simple, graphical test. BMJ, 315(7109), 629-634. https://doi.org/10.1136/bmj.315.7109.629.
Eisenberg, D. T. A., Kuzawa, C. W., & Hayes, M. G. (2015). Improving qPCR telomere length assays: Controlling for well position effects increases statistical power. American Journal of Human Biology, 27(4), 570-575. https://doi.org/10.1002/ajhb.22690.
*Eisenberg, D. T. A., Tackney, J., Cawthon, R. M., Cloutier, C. T., & Hawkes, K. (2017). Paternal and grandpaternal ages at conception and descendant telomere lengths in chimpanzees and humans. American Journal of Physical Anthropology, 162(2), 201-207. https://doi.org/10.1002/ajpa.23109.
Elbers, C. C., Garcia, M. E., Kimura, M., Cummings, S. R., Nalls, M. A., Newman, A. B., Park, V., Sanders, J. L., Tranah, G. J., Tishkoff, S. A., Harris, T. B., & Aviv, A. (2014). Comparison between Southern blots and qPCR analysis of leukocyte telomere length in the Health ABC Study. The Journals of Gerontology: Series A, 69(5), 527-531. https://doi.org/10.1093/gerona/glt121.
Fairlie, J., Holland, R., Pilkington, J. G., Pemberton, J. M., Harrington, L., & Nussey, D. H. (2016). Lifelong leukocyte telomere dynamics and survival in a free-living mammal. Aging Cell, 15(1), 140-148. https://doi.org/10.1111/acel.12417.
*Fick, L. J., Fick, G. H., Li, Z., Cao, E., Bao, B. O., Heffelfinger, D., Parker, H. G., Ostrander, E. A., & Riabowol, K. (2012). Telomere length correlates with life span of dog breeds. Cell Reports, 2(6), 1530-1536. https://doi.org/10.1016/j.celrep.2012.11.021.
*Fitzpatrick, L. J., Olsson, M., Pauliny, A., While, G. M., & Wapstra, E. (2021). Individual telomere dynamics and their links to life history in a viviparous lizard. Proceedings of the Royal Society B: Biological Sciences, 288(1951), 20210271. https://doi.org/10.1098/rspb.2021.0271.
*Foley, N. M., Hughes, G. M., Huang, Z., Clarke, M., Jebb, D., Whelan, C. V., Petit, E. J., Touzalin, F., Farcy, O., Jones, G., Ransome, R. D., Kacprzyk, J., O’Connell, M. J., Kerth, G., Rebelo, H., Rodrigues, L., Puechmaille, S. J., & Teeling, E. C. (2018). Growing old, yet staying young: The role of telomeres in bats’ exceptional longevity. Science Advances, 4(2), eaao0926. https://doi.org/10.1126/sciadv.aao0926.
*Foote, C. G. (2008). Avian telomere dynamics. University of Glasgow.
Foote, C. G., Vleck, D., & Vleck, C. M. (2013). Extent and variability of interstitial telomeric sequences and their effects on estimates of telomere length. Molecular Ecology Resources, 13(3), 417-428. https://doi.org/10.1111/1755-0998.12079.
Frenck, R. W., Blackburn, E. H., & Shannon, K. M. (1998). The rate of telomere sequence loss in human leukocytes varies with age. Proceedings of the National Academy of Sciences of the United States of America, 95(10), 5607-5610. https://doi.org/10.1073/pnas.95.10.5607.
Froy, H., Phillips, R. A., Wood, A. G., Nussey, D. H., & Lewis, S. (2013). Age-related variation in reproductive traits in the wandering albatross: Evidence for terminal improvement following senescence. Ecology Letters, 16(5), 642-649. https://doi.org/10.1111/ele.12092.
Gaillard, J.-M., Yoccoz, N. G., Lebreton, J.-D., Bonenfant, C., Devillard, S., Loison, A., Pontier, D., & Allaine, D. (2005). Generation time: A reliable metric to measure life-history variation among mammalian populations. The American Naturalist, 166(1), 119-123, discussion 124-128. https://doi.org/10.1086/430330.
Gardner, M., Bann, D., Wiley, L., Cooper, R., Hardy, R., Nitsch, D., Martin-Ruiz, C., Shiels, P., Sayer, A. A., Barbieri, M., Bekaert, S., Bischoff, C., Brooks-Wilson, A., Chen, W., Cooper, C., Christensen, K., De Meyer, T., Deary, I., Der, G., … Ben-Shlomo, Y. (2014). Gender and telomere length: Systematic review and meta-analysis. Experimental Gerontology, 51, 15-27. https://doi.org/10.1016/j.exger.2013.12.004.
Gomes, N. M. V., Ryder, O. A., Houck, M. L., Charter, S. J., Walker, W., Forsyth, N. R., Austad, S. N., Venditti, C., Pagel, M., Shay, J. W., & Wright, W. E. (2011). Comparative biology of mammalian telomeres: Hypotheses on ancestral states and the roles of telomeres in longevity determination. Aging Cell, 10(5), 761-768. https://doi.org/10.1111/j.1474-9726.2011.00718.x.
Gomes, N. M. V., Shay, J. W., & Wright, W. E. (2010). Telomere biology in Metazoa. FEBS Letters, 584(17), 3741-3751. https://doi.org/10.1016/j.febslet.2010.07.031.
*Graham, J. L., Bauer, C. M., Heidinger, B. J., Ketterson, E. D., & Greives, T. J. (2019). Early-breeding females experience greater telomere loss. Molecular Ecology, 28(1), 114-126. https://doi.org/10.1111/mec.14952.
*Hall, M. E., Nasir, L., Daunt, F., Gault, E. A., Croxall, J. P., Wanless, S., & Monaghan, P. (2004). Telomere loss in relation to age and early environment in long-lived birds. Proceedings of the Royal Society of London. Series B: Biological Sciences, 271(1548), 1571-1576. https://doi.org/10.1098/rspb.2004.2768.
*Hares, M. C., Vitikainen, E. I. K., Marshall, H. H., Thompson, F. J., Blount, J. D., & Cant, M. A. (2018). Telomere dynamics in wild banded mongooses: Evaluating longitudinal and quasi-longitudinal markers of senescence. Experimental Gerontology, 107, 67-73. https://doi.org/10.1016/j.exger.2017.09.021.
Harley, C. B., Futcher, A. B., & Greider, C. W. (1990). Telomeres shorten during ageing of human fibroblasts. Nature, 345(6274), 458-460. https://doi.org/10.1038/345458a0.
*Hatakeyama, H., Nakamura, K.-I., 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. Mechanisms of Ageing and Development, 129(9), 550-557. https://doi.org/10.1016/j.mad.2008.05.006.
*Hatase, H., Sudo, R., Watanabe, K. K., Kasugai, T., Saito, T., Okamoto, H., Uchida, I., & Tsukamoto, K. (2008). Shorter telomere length with age in the loggerhead turtle: A new hope for live sea turtle age estimation. Genes & Genetic Systems, 83(5), 423-426. https://doi.org/10.1266/ggs.83.423.
*Haussmann, M. F., & Mauck, R. A. (2008). New strategies for telomere-based age estimation. Molecular Ecology Resources, 8(2), 264-274. https://doi.org/10.1111/j.1471-8286.2007.01973.x.
*Haussmann, M., & Vleck, C. (2002). Telomere length provides a new technique for aging animals. Oecologia, 130(3), 325-328. https://doi.org/10.1007/s00442-001-0827-y.
*Haussmann, M., Vleck, C., & Nisbet, I. (2003). Calibrating the telomere clock in common terns, Sterna hirundo. Experimental Gerontology, 38(7), 787-789. https://doi.org/10.1016/S0531-5565(03)00109-8.
Haussmann, M. F., Winkler, D. W., Huntington, C. E., Nisbet, I. C. T., & Vleck, C. M. (2007). Telomerase activity is maintained throughout the lifespan of long-lived birds. Experimental Gerontology, 42(7), 610-618. https://doi.org/10.1016/j.exger.2007.03.004.
*Haussmann, M. F., Winkler, D. W., O’Reilly, K. M., Huntington, C. E., Nisbet, I. C. T., & Vleck, C. M. (2003). Telomeres shorten more slowly in long-lived birds and mammals than in short-lived ones. Proceedings of the Royal Society B: Biological Sciences, 270(1522), 1387-1392. https://doi.org/10.1098/rspb.2003.2385.
*Heidinger, B. J., Blount, J. D., Boner, W., Griffiths, K., Metcalfe, N. B., & Monaghan, P. (2012). Telomere length in early life predicts lifespan. Proceedings of the National Academy of Sciences of the United States of America, 109(5), 1743-1748. https://doi.org/10.1073/pnas.1113306109.
*Heidinger, B. J., Kucera, A. C., Kittilson, J. D., & Westneat, D. F. (2021). Longer telomeres during early life predict higher lifetime reproductive success in females but not males. Proceedings of the Royal Society B: Biological Sciences, 288(1951), 20210560. https://doi.org/10.1098/rspb.2021.0560.
Herrmann, M., Pusceddu, I., März, W., & Herrmann, W. (2018). Telomere biology and age-related diseases. Clinical Chemistry and Laboratory Medicine (CCLM), 56(8), 1210-1222. https://doi.org/10.1515/cclm-2017-0870.
*Hoelzl, F., Cornils, J. S., Smith, S., Moodley, Y., & Ruf, T. (2016). Telomere dynamics in free-living edible dormice (Glis glis): The impact of hibernation and food supply. Journal of Experimental Biology, 219(16), 2469-2474. https://doi.org/10.1242/jeb.140871.
*Hoelzl, F., Smith, S., Cornils, J. S., Aydinonat, D., Bieber, C., & Ruf, T. (2016). Telomeres are elongated in older individuals in a hibernating rodent, the edible dormouse (Glis glis). Scientific Reports, 6(1), 36856. https://doi.org/10.1038/srep36856.
*Horn, T., Gemmell, N. J., Robertson, B. C., & Bridges, C. R. (2008). Telomere length change in European sea bass (Dicentrarchus labrax). Australian Journal of Zoology, 56(3), 207-210. https://doi.org/10.1071/ZO08046.
*Horn, T., Robertson, B. C., Will, M., Eason, D. K., Elliott, G. P., & Gemmell, N. J. (2011). Inheritance of telomere length in a bird. PLoS One, 6(2), e17199. https://doi.org/10.1371/journal.pone.0017199.
*Ineson, K. M., O’Shea, T. J., Kilpatrick, C. W., Parise, K. L., & Foster, J. T. (2020). Ambiguities in using telomere length for age determination in two North American bat species. Journal of Mammalogy, 101(4), 958-969. https://doi.org/10.1093/jmammal/gyaa064.
*Izzo, C. (2010). Patterns of telomere length change with age in aquatic vertebrates and the phylogenetic distribution of the pattern among jawed vertebrates. University of Adelaide.
*Juola, F. A., Haussmann, M. F., Dearborn, D. C., & Vleck, C. M. (2006). Telomere shortening in a long-lived marine Birds: Cross-sectional analysis and test of an aging tool. The Auk, 123(3), 775. https://doi.org/10.1642/0004-8038(2006)123[775:TSIALM]2.0.CO;2.
*Karell, P., Bensch, S., Ahola, K., & Asghar, M. (2017). Pale and dark morphs of tawny owls show different patterns of telomere dynamics in relation to disease status. Proceedings of the Royal Society B: Biological Sciences, 284(1859), 20171127. https://doi.org/10.1098/rspb.2017.1127.
*Katepalli, M. P., Adams, A. A., Lear, T. L., & Horohov, D. W. (2008). The effect of age and telomere length on immune function in the horse. Developmental and Comparative Immunology, 32(12), 1409-1415. https://doi.org/10.1016/j.dci.2008.06.007.
Kawanishi S., & Oikawa S. (2004). Mechanism of Telomere Shortening by Oxidative Stress. Annals of the New York Academy of Sciences, 1019, (1), 278. -284. http://dx.doi.org/10.1196/annals.1297.047.
*Khoriauli, L., Romano, A., Caprioli, M., Santagostino, M., Nergadze, S. G., Costanzo, A., Rubolini, D., Giulotto, E., Saino, N., & Parolini, M. (2017). Assortative mating for telomere length and antioxidant capacity in barn swallows (Hirundo rustica). Behavioral Ecology and Sociobiology, 71(8), 124. https://doi.org/10.1007/s00265-017-2352-y.
*Kim, Y. J., Subramani, V. K., & Sohn, S. H. (2011). Age prediction in the chickens using telomere quantity by quantitative fluorescence in situ hybridization technique. Asian-Australian Journal of Animal Sciences, 24(5), 603-609. https://doi.org/10.5713/ajas.2011.10187.
*Kirby, R., Alldredge, M. W., & Pauli, J. N. (2017). Environmental, not individual, factors drive markers of biological aging in black bears. Evolutionary Ecology, 31(4), 571-584. https://doi.org/10.1007/s10682-017-9885-4.
*Kirby, R., Johnson, H. E., Alldredge, M. W., & Pauli, J. N. (2019). The cascading effects of human food on hibernation and cellular aging in free-ranging black bears. Scientific Reports, 9(1), 2197. https://doi.org/10.1038/s41598-019-38937-5.
Kumar, S., Stecher, G., Suleski, M., & Hedges, S. B. (2017). TimeTree: A resource for timelines, timetrees, and divergence times. Molecular Biology and Evolution, 34(7), 1812-1819. https://doi.org/10.1093/molbev/msx116.
Lai, T.-P., Wright, W. E., & Shay, J. W. (2018). Comparison of telomere length measurement methods. Philosophical Transactions of the Royal Society B: Biological Sciences, 373(1741), 20160451. https://doi.org/10.1098/rstb.2016.0451.
Lansdorp, P. M., Verwoerd, N. P., van de Rijke, F. M., Dragowska, V., Little, M. T., Dirks, R. W., Raap, A. K., Tanke, H. J. (1996). Heterogeneity in telomere length of human chromosomes. Human Molecular Genetics, 5(5), 685-691. https://doi.org/10.1093/hmg/5.5.685.
Lapham, K., Kvale, M. N., Lin, J., Connell, S., Croen, L. A., Dispensa, B. P., Fang, L., Hesselson, S., Hoffmann, T. J., Iribarren, C., Jorgenson, E., Kushi, L. H., Ludwig, D., Matsuguchi, T., McGuire, W. B., Miles, S., Quesenberry, C. P., Rowell, S., Sadler, M., … Blackburn, E. H. (2015). Automated assay of telomere length measurement and informatics for 100,000 subjects in the Genetic Epidemiology Research on Adult Health and Aging (GERA) Cohort. Genetics, 200(4), 1061-1072. https://doi.org/10.1534/genetics.115.178624.
*Le Vaillant, M., Viblanc, V. A., Saraux, C., Le Bohec, C., Le Maho, Y., Kato, A., Criscuolo, F., & Ropert-Coudert, Y. (2015). Telomere length reflects individual quality in free-living adult king penguins. Polar Biology, 38(12), 2059-2067. https://doi.org/10.1007/s00300-015-1766-0.
*Lee, W.-W., Nam, K.-H., Terao, K., & Yoshikawa, Y. (2002). Age-related telomere length dynamics in peripheral blood mononuclear cells of healthy cynomolgus monkeys measured by Flow FISH. Immunology, 105(4), 458-465. https://doi.org/10.1046/j.1365-2567.2002.01386.x.
Levy, M. Z., Allsopp, R. C., Futcher, A. B., Greider, C. W., & Harley, C. B. (1992). Telomere end-replication problem and cell aging. Journal of Molecular Biology, 225(4), 951-960. https://doi.org/10.1016/0022-2836(92)90096-3.
*Lewin, N., Treidel, L. A., Holekamp, K. E., Place, N. J., & Haussmann, M. F. (2015). Socioecological variables predict telomere length in wild spotted hyenas. Biology Letters, 11(2), 20140991. https://doi.org/10.1098/rsbl.2014.0991.
Li, C. (2012). Deer antler regeneration: A stem cell-based epimorphic process. Birth Defects Research Part C: Embryo Today: Reviews, 96(1), 51-62. https://doi.org/10.1002/bdrc.21000.
Liberati, A., Altman, D. G., Tetzlaff, J., Mulrow, C., Gøtzsche, P. C., Ioannidis, J. P. A., Clarke, M., Devereaux, P. J., Kleijnen, J., & Moher, D. (2009). The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: Explanation and elaboration. PLoS Medicine, 6(7), e1000100. https://doi.org/10.1371/journal.pmed.1000100.
*Lieshout, S. H. J., Sparks, A. M., Bretman, A., Newman, C., Buesching, C. D., Burke, T., Macdonald, D. W., & Dugdale, H. L. (2021). Estimation of environmental, genetic and parental age at conception effects on telomere length in a wild mammal. Journal of Evolutionary Biology, 34(2), 296-308. https://doi.org/10.1111/jeb.13728.
Lin, J., Cheon, J., Brown, R., Coccia, M., Puterman, E., Aschbacher, K., Sinclair, E., Epel, E., & Blackburn, E. H. (2016). Systematic and cell type-specific telomere length changes in subsets of lymphocytes. Journal of Immunology Research, 2016, 1-9. http://dx.doi.org/10.1155/2016/5371050.
Lin, J., Smith, D. L., Esteves, K., & Drury, S. (2019). Telomere length measurement by qPCR - Summary of critical factors and recommendations for assay design. Psychoneuroendocrinology, 99, 271-278. https://doi.org/10.1016/j.psyneuen.2018.10.005.
*López-Arrabé, J., Monaghan, P., Cantarero, A., Boner, W., Pérez-Rodríguez, L., & Moreno, J. (2018). Sex-specific associations between telomere dynamics and oxidative status in adult and nestling pied flycatchers. Physiological and Biochemical Zoology, 91(3), 868-877. https://doi.org/10.1086/697294.
López-Otín, C., Blasco, M. A., Partridge, L., Serrano, M., & Kroemer, G. (2013). The hallmarks of aging. Cell, 153(6), 1194-1217. https://doi.org/10.1016/j.cell.2013.05.039.
Mabille, G., Boutard, O., Shaffer, S. A., Costa, D. P., & Weimerskirch, H. (2004). Growth and energy expenditure of Wandering Albatross Diomedea exulans chicks. Ibis, 146(1), 85-94. https://doi.org/10.1111/j.1474-919X.2004.00222.x.
*McKevitt, T. P., Nasir, L., Wallis, C. V., & Argyle, D. J. (2003). A cohort study of telomere and telomerase biology in cats. American Journal of Veterinary Research, 64(12), 1496-1499. https://doi.org/10.2460/ajvr.2003.64.1496.
*Mclennan, D., Armstrong, J. D., Stewart, D. C., Mckelvey, S., Boner, W., Monaghan, P., & Metcalfe, N. B. (2016). Interactions between parental traits, environmental harshness and growth rate in determining telomere length in wild juvenile salmon. Molecular Ecology, 25(21), 5425-5438. https://doi.org/10.1111/mec.13857.
*McLennan, D., Armstrong, J. D., Stewart, D. C., McKelvey, S., Boner, W., Monaghan, P., & Metcalfe, N. B. (2018). Links between parental life histories of wild salmon and the telomere lengths of their offspring. Molecular Ecology, 27(3), 804-814. https://doi.org/10.1111/mec.14467.
Meyne, J., Baker, R. J., Hobart, H. H., Hsu, T. C., Ryder, O. A., Ward, O. G., Wiley, J. E., Wurster-Hill, D. H., Yates, T. L., & Moyzis, R. K. (1990). Distribution of non-telomeric sites of the (TTAGGG)n telomeric sequence in vertebrate chromosomes. Chromosoma, 99(1), 3-10. https://doi.org/10.1007/BF01737283.
*Mizutani, Y., Tomita, N., Kazama, K., Takahashi, H., Hasegawa, O., & Niizuma, Y. (2009). Relationship between telomere length and age in Black-tailed Gull. Japanese Journal of Ornithology, 58(2), 192-195. https://doi.org/10.3838/jjo.58.192.
*Mizutani, Y., Tomita, N., Niizuma, Y., & Yoda, K. (2013). Environmental perturbations influence telomere dynamics in long-lived birds in their natural habitat. Biology Letters, 9(5), 20130511. https://doi.org/10.1098/rsbl.2013.0511.
Monaghan, P., Eisenberg, D. T. A., Harrington, L., & Nussey, D. (2018). Understanding diversity in telomere dynamics. Philosophical Transactions of the Royal Society B: Biological Sciences, 373(1741), 20160435. https://doi.org/10.1098/rstb.2016.0435.
Monaghan, P., & Ozanne, S. E. (2018). Somatic growth and telomere dynamics in vertebrates: Relationships, mechanisms and consequences. Philosophical Transactions of the Royal Society B: Biological Sciences, 373(1741), 20160446. https://doi.org/10.1098/rstb.2016.0446.
Nakagawa, S., & Cuthill, I. C. (2007). Effect size, confidence interval and statistical significance: A practical guide for biologists. Biological Reviews of the Cambridge Philosophical Society, 82(4), 591-605. https://doi.org/10.1111/j.1469-185X.2007.00027.x.
Nakagawa, S., Lagisz, M., O’Dea, R. E., Rutkowska, J., Yang, Y., Noble, D. W. A., & Senior, A. M. (2019). The Orchard Plot: Cultivating a forest plot for use in ecology, evolution and beyond [Preprint]. EcoEvoRxiv, https://doi.org/10.32942/osf.io/epqa7.
Nakagawa, S., & Santos, E. S. A. (2012). Methodological issues and advances in biological meta-analysis. Evolutionary Ecology, 26(5), 1253-1274. https://doi.org/10.1007/s10682-012-9555-5.
Nussey, D. H., Baird, D., Barrett, E., Boner, W., Fairlie, J., Gemmell, N., Hartmann, N., Horn, T., Haussmann, M., Olsson, M., Turbill, C., Verhulst, S., Zahn, S., & Monaghan, P. (2014). Measuring telomere length and telomere dynamics in evolutionary biology and ecology. Methods in Ecology and Evolution, 5(4), 299-310. https://doi.org/10.1111/2041-210X.12161.
Nussey, D. H., Coulson, T., Festa-Bianchet, M., & Gaillard, J.-M. (2008). Measuring senescence in wild animal populations: Towards a longitudinal approach. Functional Ecology, 22(3), 393-406. https://doi.org/10.1111/j.1365-2435.2008.01408.x.
*Olsen, M. T., Robbins, J., Bérubé, M., Rew, M. B., & Palsbøll, P. J. (2014). Utility of telomere length measurements for age determination of humpback whales. NAMMCO Scientific Publications, 10. https://doi.org/10.7557/3.3194.
Olsson, M., Geraghty, N. J., Wapstra, E., & Wilson, M. (2020). Telomere length varies substantially between blood cell types in a reptile. Royal Society Open Science, 7(6), 192136. https://doi.org/10.1098/rsos.192136.
*Olsson, M., Pauliny, A., Wapstra, E., Uller, T., Schwartz, T., Miller, E., & Blomqvist, D. (2011). Sexual differences in telomere selection in the wild. Molecular Ecology, 20(10), 2085-2099. https://doi.org/10.1111/j.1365-294X.2011.05085.x.
Olsson, M., Wapstra, E., & Friesen, C. (2018). Ectothermic telomeres: It’s time they came in from the cold. Philosophical Transactions of the Royal Society B: Biological Sciences, 373(1741), 20160449. https://doi.org/10.1098/rstb.2016.0449.
*Pauliny, A., Wagner, R., Augustin, J., Szep, T., & Blomqvist, D. (2006). Age-independent telomere length predicts fitness in two bird species. Molecular Ecology, 15(6), 1681-1687. https://doi.org/10.1111/j.1365-294X.2006.02862.x.
Peters, J. L., Sutton, A. J., Jones, D. R., Abrams, K. R., & Rushton, L. (2007). Performance of the trim and fill method in the presence of publication bias and between-study heterogeneity. Statistics in Medicine, 26(25), 4544-4562. https://doi.org/10.1002/sim.2889.
R Core Team. (2020). R: A language and environment for statistical computing (version 4.0.2). R Foundation for Statistical Computing. https://www.R-project.org/.
*Rattiste, K., Klandorf, H., Urvik, J., Sepp, T., Asghar, M., Hasselquist, D., Cooey, C., & Hõrak, P. (2015). Skin pentosidine and telomere length do not covary with age in a long-lived seabird. Biogerontology, 16(4), 435-441. https://doi.org/10.1007/s10522-015-9564-1.
*Reichert, S., Criscuolo, F., Verinaud, E., Zahn, S., & Massemin, S. (2013). Telomere length correlations among somatic tissues in adult zebra finches. PLoS One, 8(12), e81496. https://doi.org/10.1371/journal.pone.0081496.
*Reichert, S., Froy, H., Boner, W., Burg, T. M., Daunt, F., Gillespie, R., Griffiths, K., Lewis, S., Phillips, R. A., Nussey, D. H., & Monaghan, P. (2017). Telomere length measurement by qPCR in birds is affected by storage method of blood samples. Oecologia, 184(2), 341-350. https://doi.org/10.1007/s00442-017-3887-3.
*Reichert, S., Rojas, E. R., Zahn, S., Robin, J.-P., Criscuolo, F., & Massemin, S. (2015). Maternal telomere length inheritance in the king penguin. Heredity, 114(1), 10-16. https://doi.org/10.1038/hdy.2014.60.
Reichert, S., & Stier, A. (2017). Does oxidative stress shorten telomeres in vivo? A review. Biology Letters, 13(12), 20170463. https://doi.org/10.1098/rsbl.2017.0463.
Remot, F., Ronget, V., Froy, H., Rey, B., Gaillard, J.-M., Nussey, D. H., & Lemaître, J.-F. (2020). No sex differences in adult telomere length across vertebrates: A meta-analysis. Royal Society Open Science, 7(11), 200548. https://doi.org/10.1098/rsos.200548.
*Rollings, N., Uhrig, E. J., Krohmer, R. W., Waye, H. L., Mason, R. T., Olsson, M., Whittington, C. M., & Friesen, C. R. (2017). Age-related sex differences in body condition and telomere dynamics of red-sided garter snakes. Proceedings of the Royal Society B: Biological Sciences, 284(1852), 20162146. https://doi.org/10.1098/rspb.2016.2146.
Salmón, P., Nilsson, J. F., Nord, A., Bensch, S., & Isaksson, C. (2016). Urban environment shortens telomere length in nestling great tits, Parus major. Biology Letters, 12(6), 20160155. https://doi.org/10.1098/rsbl.2016.0155.
*Salmón, P., Nilsson, J. F., Watson, H., Bensch, S., & Isaksson, C. (2017). Selective disappearance of great tits with short telomeres in urban areas. Proceedings of the Royal Society B: Biological Sciences, 284(1862), 20171349. https://doi.org/10.1098/rspb.2017.1349.
*Sauer, D. J., Heidinger, B. J., Kittilson, J. D., Lackmann, A. R., & Clark, M. E. (2021). No evidence of physiological declines with age in an extremely long-lived fish. Scientific Reports, 11(1), 9065. https://doi.org/10.1038/s41598-021-88626-5.
*Seeker, L. A., Ilska, J. J., Psifidi, A., Wilbourn, R. V., Underwood, S. L., Fairlie, J., Holland, R., Froy, H., Salvo-Chirnside, E., Bagnall, A., Whitelaw, B., Coffey, M. P., Nussey, D. H., & Banos, G. (2018). Bovine telomere dynamics and the association between telomere length and productive lifespan. Scientific Reports, 8(1), 12748. https://doi.org/10.1038/s41598-018-31185-z.
*Seibt, K. D., Häussler, S., Vecchio, D., DeCarlo, E., Ceciliani, F., & Sauerwein, H. (2019). Comparison of telomere lengths in leukocytes and in nasal and vaginal epithelial cells from Water Buffaloes (Bubalus bubalis) of different ages. Research in Veterinary Science, 124, 328-333. https://doi.org/10.1016/j.rvsc.2019.04.013.
*Sheldon, E., Eastwood, J., Teunissen, N., Roast, M., Fan, M., Hall, M., Aranzamendi, N. H., Kingma, S., Verhulst, S., & Peters, A. (2021). Telomere dynamics in the first year of life, but not later in life, predict lifespan in a wild bird. Authorea Preprints. https://doi.org/10.22541/au.162168440.03821228/v1.
Sherratt, D. J., West, S. C., Chan, S. R. W. L., & Blackburn, E. H. (2004). Telomeres and telomerase. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 359(1441), 109-122. https://doi.org/10.1098/rstb.2003.1370.
Sidorov, I. A., Gee, D., & Dimitrov, D. S. (2004). A kinetic model of telomere shortening in infants and adults. Journal of Theoretical Biology, 226(2), 169-175. https://doi.org/10.1016/j.jtbi.2003.08.009.
*Simide, R., Angelier, F., Gaillard, S., & Stier, A. (2016). Age and heat stress as determinants of telomere length in a long-lived fish, the Siberian sturgeon. Physiological and Biochemical Zoology, 89(5), 441-447. https://doi.org/10.1086/687378.
*Singchat, W., Kraichak, E., Tawichasri, P., Tawan, T., Suntronpong, A., Sillapaprayoon, S., Phatcharakullawarawat, R., Muangmai, N., Suntrarachun, S., Baicharoen, S., Punyapornwithaya, V., Peyachoknagul, S., Chanhome, L., & Srikulnath, K. (2019). Dynamics of telomere length in captive Siamese cobra (Naja kaouthia) related to age and sex. Ecology and Evolution, 9(11), 6366-6377. https://doi.org/10.1002/ece3.5208.
*Stier, A., Hsu, B.-Y., Marciau, C., Doligez, B., Gustafsson, L., Bize, P., & Ruuskanen, S. (2020). Born to be young? Prenatal thyroid hormones increase early-life telomere length in wild collared flycatchers. Biology Letters, 16(11), 20200364. https://doi.org/10.1098/rsbl.2020.0364.
Stier, A., Metcalfe, N. B., & Monaghan, P. (2020). Pace and stability of embryonic development affect telomere dynamics: An experimental study in a precocial bird model. Proceedings of the Royal Society B: Biological Sciences, 287, 20201378. https://doi.org/10.1098/rspb.2020.1378.
Sudyka, J. (2019). Does reproduction shorten telomeres? Towards integrating individual quality with life-history strategies in telomere biology. BioEssays, 41(11), 1900095. https://doi.org/10.1002/bies.201900095.
*Sudyka, J., Arct, A., Drobniak, S., Dubiec, A., Gustafsson, L., & Cichon, M. (2014). Experimentally increased reproductive effort alters telomere length in the blue tit (Cyanistes caeruleus). Journal of Evolutionary Biology, 27(10), 2258-2264. https://doi.org/10.1111/jeb.12479.
*Sudyka, J., Podmokła, E., Drobniak, S. M., Dubiec, A., Arct, A., Gustafsson, L., & Cichoń, M. (2019). Sex-specific effects of parasites on telomere dynamics in a short-lived passerine-the blue tit. Die Naturwissenschaften, 106(1-2), 6. https://doi.org/10.1007/s00114-019-1601-5.
*Taff, C. C., & Freeman-Gallant, C. R. (2017). Sexual signals reflect telomere dynamics in a wild bird. Ecology and Evolution, 7(10), 3436-3442. https://doi.org/10.1002/ece3.2948.
*Tricola, G. M., Simons, M. J. P., Atema, E., Boughton, R. K., Brown, J. L., Dearborn, D. C., Divoky, G., Eimes, J. A., Huntington, C. E., Kitaysky, A. S., Juola, F. A., Lank, D. B., Litwa, H. P., Mulder, E. G. A., Nisbet, I. C. T., Okanoya, K., Safran, R. J., Schoech, S. J., Schreiber, E. A., … Haussmann, M. F. (2018). The rate of telomere loss is related to maximum lifespan in birds. Philosophical Transactions of the Royal Society B: Biological Sciences, 373(1741), 20160445. https://doi.org/10.1098/rstb.2016.0445.
*Tsui, C. (2005). Evaluation of telomere length as an age-marker in marine teleosts (University of Hong Kong). University of Hong Kong. http://hub.hku.hk/handle/10722/29403.
*Ujvari, B., Biro, P. A., Charters, J. E., Brown, G., Heasman, K., Beckmann, C., & Madsen, T. (2017). Curvilinear telomere length dynamics in a squamate reptile. Functional Ecology, 31(3), 753-759. https://doi.org/10.1111/1365-2435.12764.
*Ujvari, B., & Madsen, T. (2009). Short telomeres in hatchling snakes: Erythrocyte telomere dynamics and longevity in tropical pythons. PLoS One, 4(10), e7493. https://doi.org/10.1371/journal.pone.0007493.
Vágási, C. I., Vincze, O., Pătraș, L., Osváth, G., Pénzes, J., Haussmann, M. F., Barta, Z., & Pap, P. L. (2019). Longevity and life history coevolve with oxidative stress in birds. Functional Ecology, 33(1), 152-161. https://doi.org/10.1111/1365-2435.13228.
Vedder, O., Verhulst, S., Bauch, C., & Bouwhuis, S. (2017). Telomere attrition and growth: A life-history framework and case study in common terns. Journal of Evolutionary Biology, 30(7), 1409-1419. https://doi.org/10.1111/jeb.13119.
*Vernasco, B. J., Dakin, R., Majer, A. D., Haussmann, M. F., Ryder, T. B., & Moore, I. T. (2021). Longitudinal dynamics and behavioural correlates of telomeres in male wire-tailed manakins. Functional Ecology, 35(2), 450-462. https://doi.org/10.1111/1365-2435.13715.
Viechtbauer, W. (2010). Conducting Meta-analyses in R with the metafor package. Journal of Statistical Software, 36(1), 1-48. https://doi.org/10.18637/jss.v036.i03.
von Zglinicki, T., Bürkle, A., & Kirkwood, T. B. L. (2001). Stress, DNA damage and ageing-An integrative approach. Experimental Gerontology, 36(7), 1049-1062. https://doi.org/10.1016/S0531-5565(01)00111-5.
Wang, Q., Zhan, Y., Pedersen, N. L., Fang, F., & Hägg, S. (2018). Telomere length and all-cause mortality: A meta-analysis. Ageing Research Reviews, 48, 11-20. https://doi.org/10.1016/j.arr.2018.09.002.
*Watson, R. L., Bird, E. J., Underwood, S., Wilbourn, R. V., Fairlie, J., Watt, K., Salvo-Chirnside, E., Pilkington, J. G., Pemberton, J. M., McNeilly, T. N., Froy, H., & Nussey, D. H. (2017). Sex differences in leucocyte telomere length in a free-living mammal. Molecular Ecology, 26(12), 3230-3240. https://doi.org/10.1111/mec.13992.
*Whittemore, K., Vera, E., Martínez-Nevado, E., Sanpera, C., & Blasco, M. A. (2019). Telomere shortening rate predicts species life span. Proceedings of the National Academy of Sciences of the United States of America, 116(30), 15122-15127. https://doi.org/10.1073/pnas.1902452116.
*Wilbourn, R. V., Froy, H., McManus, M.-C., Cheynel, L., Gaillard, J.-M., Gilot-Fromont, E., Regis, C., Rey, B., Pellerin, M., Lemaître, J.-F., & Nussey, D. H. (2017). Age-dependent associations between telomere length and environmental conditions in roe deer. Biology Letters, 13(9), 20170434. https://doi.org/10.1098/rsbl.2017.0434.
Wilbourn, R. V., Moatt, J. P., Froy, H., Walling, C. A., Nussey, D. H., & Boonekamp, J. J. (2018). The relationship between telomere length and mortality risk in non-model vertebrate systems: A meta-analysis. Philosophical Transactions of the Royal Society B: Biological Sciences, 373(1741), 20160447. https://doi.org/10.1098/rstb.2016.0447.
*Wnuk, M., Lewinska, A., Gurgul, A., Zabek, T., Potocki, L., Oklejewicz, B., Bugno-Poniewierska, M., Wegrzyn, M., & Slota, E. (2014). Changes in DNA methylation patterns and repetitive sequences in blood lymphocytes of aged horses. AGE, 36(1), 31-48. https://doi.org/10.1007/s11357-013-9541-z.
*Wood, E. M., Capilla-Lasheras, P., Cram, D. L., Walker, L. A., York, J. E., Lange, A., Hamilton, P. B., Tyler, C. R., & Young, A. J. (2021). Social dominance and rainfall predict telomere dynamics in a cooperative arid-zone bird. Molecular Ecology, 1-14. https://doi.org/10.1111/mec.15868.
Zeichner, S. L., Palumbo, P., Feng, Y. R., Xiao, X., Gee, D., Sleasman, J., Goodenow, M., Biggar, R., & Dimitrov, D. (1999). Rapid telomere shortening in children. Blood, 93(9), 2824-2830. https://doi.org/10.1182/blood.V93.9.2824.

P51 RR000165 United States RR NCRR NIH HHS; P51 RR013986 United States RR NCRR NIH HHS

Keywords: ageing; life-history traits; qPCR; systematic review; telomere attrition; telomere restriction fragment

Date Created: 20210826 Date Completed: 20230130 Latest Revision: 20230301

20231215

10.1111/mec.16145

34437736