Abstract
Studies on human telomeres have established that telomeres exert a significant influence on lifespan and health of organisms. However, recent research has indicated that the original idea that telomeres affect lifespan in a universal and central manner across all eukaryotic species is an oversimplification. Indeed, findings from a variety of animal species revealed that the role of telomere biology in aging is more subtle and intricate than previously recognized. Here, we show how telomere biology varies depending on the taxon. We also show how telomere biology corresponds to basic life history traits and affects the life table of a species and investments in growth, body size, reproduction, and lifespan; telomeres are hypothesized to shape evolutionary perspectives for species in an active but complex manner. Our evaluation is based on telomere biology data from many examples from throughout the animal kingdom that vary according to the degree of organismal complexity and life history strategies.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adeoye O, Olawumi J, Opeyemi A, Christiania O (2018) Review on the role of glutathione on oxidative stress and infertility. J Bras Reprod Assist 22:61–66. https://doi.org/10.5935/1518-0557.20180003
Aihie Sayer A, Cooper C (2002) Early diet and growth: impact on ageing. Proc Nutr Soc 61:79–85. https://doi.org/10.1079/pns2001138
Almazán A, Çevrim Ç, Musser JM et al (2022) Crustacean leg regeneration restores complex microanatomy and cell diversity. Sci Adv 8:1–15. https://doi.org/10.1126/sciadv.abn9823
Andreu-Sánchez S, Aubert G, Ripoll-cladellas A et al (2022) Genetic, parental and lifestyle factors influence telomere length. Commun Biol 5:1–14. https://doi.org/10.1038/s42003-022-03521-7
Andrew T, Aviv A, Falchi M et al (2006) Mapping genetic loci that determine leukocyte telomere length in a large sample of unselected female sibling pairs. Am J Hum Genet 78:480–486
Arendt JD (1997) Adaptive intrinsic growth rates: an integration across taxa. Q Rev Biol 72:149–177. https://doi.org/10.1086/419764
Aston KI, Hunt SC, Susser E et al (2012) Divergence of sperm and leukocyte age-dependent telomere dynamics: implications for male-driven evolution of telomere length in humans. MHR: Basic Sci Reprod Med 18:517–522. https://doi.org/10.1093/molehr/gas028
Aubert G, Lansdorp PM, Aubert G, Lansdorp PM (2008) Telomeres and aging. Phys Rev. https://doi.org/10.1152/physrev.00026.2007
Austad SN, Fischer KE (2016) Sex differences in lifespan. Cell Metab 23:1022–1033. https://doi.org/10.1016/j.cmet.2016.05.019
Baerlocher GM, Mak J, Röth A et al (2003) Telomere shortening in leukocyte subpopulations from baboons. J Leukoc Biol 73:289–296. https://doi.org/10.1189/jlb.0702361
Baerlocher GM, Vulto I, de Jong G, Lansdorp PM (2006) Flow cytometry and FISH to measure the average length of telomeres (flow FISH). Nat Protoc 1:2365–2376. https://doi.org/10.1038/nprot.2006.263
Barja G (1998) Mitochondrial free radical production and aging in mammals and birds. Ann NY Acad Sci 854:224–238
Barlian A, Riani YD (2020) Aging process in dermal fibroblast cell culture of Green Turtle (Chelonia mydas). BIO J Biol Sci Technol Manag 2:11. https://doi.org/10.5614/3bio.2020.2.2.2
Barrett ELB, Richardson DS (2011) Sex differences in telomeres and lifespan. Aging Cell 10:913–921. https://doi.org/10.1111/j.1474-9726.2011.00741.x
Barthelemy RM, Casanova J-P, Faure E (2008) Transcriptome analysis of ESTs from a Chaetognath reveals a deep-branching clade of Retrovirus-Like Retrotransposons. Open Virol J 2:44–60. https://doi.org/10.2174/1874357900802010044
Bassham S, Beam A, Shampay J (1998) Telomere variation in Xenopus laevis. Mol Cell Biol 18:269–275. https://doi.org/10.1128/mcb.18.1.269
Bateson M, Nettle D (2017) The telomere lengthening conundrum—it could be biology. Aging Cell 16:312–319. https://doi.org/10.1111/acel.12555
Bauch C, Becker PH, Verhulst S (2013) Telomere length reflects phenotypic quality and costs of reproduction in a long-lived seabird. Proc R Soc B Biol Sci 280:20122540. https://doi.org/10.1098/rspb.2012.2540
Beaulieu M, Reichert S, Maho Y, Le et al (2011) Oxidative status and telomere length in a long facing a costly reproductive event. Funct Ecol 25:577–585. https://doi.org/10.1111/j.l365-2435.2010.01825.x
Benetos A, Kark JD, Susser E et al (2013) Tracking and fixed ranking of leukocyte telomere length across the adult life course. Aging Cell 12:615–621. https://doi.org/10.1111/acel.12086
Bielby J, Mace GM, Bininda-Emonds ORP et al (2007) The fast-slow continuum in mammalian life history: an empirical reevaluation. Am Nat 169:748–757. https://doi.org/10.1086/516847
Bize P, Devevey G, Monaghan P et al (2008) Fecundity and survival in relation to resistance to oxidative stress in a free-living bird. Ecology 89:2584–2593. https://doi.org/10.1890/07-1135.1
Blackburn EH (1991) Structure and function of telomeres. Nature 350:569–573
Blackburn EH, Gall JG (1978) A tandemly repeated sequence at the termini of the extrachromosomal ribosomal RNA genes in Tetrahymena. J Mol Biol 120:33–53
Bombarová M, Vítková M, Špakulová M, Koubková B (2009) Telomere analysis of platyhelminths and acanthocephalans by FISH and Southern hybridization. Genome 52:897–903. https://doi.org/10.1139/G09-063
Burraco P, Comas M, Reguera S et al (2020) Telomere length mirrors age structure along a 2200-m altitudinal gradient in a Mediterranean lizard. Comp Biochem Physiol 247:110741. https://doi.org/10.1016/j.cbpa.2020.110741
Capkova Frydrychova R (2023) Telomerase as a possible key to bypass the cost of reproduction effect. Mol Ecol. https://doi.org/10.1111/mec.16870
Casagrande S, Hau M (2019) Telomere attrition: metabolic regulation and signalling function? Biol Lett. https://doi.org/10.1098/rsbl.2018.0885
Cawthon RM (2002) Telomere measurement by quantitative PCR. Nucleic Acids Res 30:e47
Chakravarti D, LaBella KA, DePinho RA (2021) Telomeres: history, health, and hallmarks of aging. Cell 184:306–322. https://doi.org/10.1016/j.cell.2020.12.028
Chatelain M, Drobniak SM, Szulkin M (2020) The association between stressors and telomeres in non-human vertebrates: a meta-analysis. Ecol Lett 23:381–398. https://doi.org/10.1111/ele.13426
Chen CF, Sung TL, Chen LY, Chen JH (2018) Telomere maintenance during anterior regeneration and aging in the freshwater annelid Aeolosoma viride. Sci Rep 8:1–13. https://doi.org/10.1038/s41598-018-36396-y
Chen L, Mei K, Tan L et al (2022) Variability in newborn telomere length is explained by inheritance and intrauterine environment. BMC Med 20:1–17
Chu B, Marwaha K, Sanvictores T, Ayers D (2022) Physiology, stress reaction. StatPearls. StatPearls Publishing, Treasure Island
Creighton HB, McClintock B (1931) The correlation of cytological and genetical crossing-over in Zea mays. Proc Natl Acad Sci 17:148–150. https://doi.org/10.1073/pnas.21.3.148
Criscuolo F, Dobson FS, Schull Q (2021) The influence of phylogeny and life history on telomere lengths and telomere rate of change among bird species: a meta-analysis. Ecol Evol 11:12908–12922. https://doi.org/10.1002/ece3.7931
Dalgård C, Benetos A, Verhulst S et al (2015) Leukocyte telomere length dynamics in women and men: menopause vs age effects. Int J Epidemiol 44:1688–1695. https://doi.org/10.1093/ije/dyv165
Daniali L, Benetos A, Susser E et al (2013) Telomeres shorten at equivalent rates in somatic tissues of adults. Nat Commun 4:1596–1597. https://doi.org/10.1038/ncomms2602
Dantzer B, Fletcher QE (2015) Telomeres shorten more slowly in slow-aging wild animals than in fast-aging ones. Exp Gerontol 71:38–47. https://doi.org/10.1016/j.exger.2015.08.012
De Magalhães JP, Costa J, Church GM (2007) An analysis of the relationship between metabolism, developmental schedules, and longevity using phylogenetic independent contrasts. J Gerontol Ser A Biol Sci Med Sci 62:149–160. https://doi.org/10.1093/gerona/62.2.149
Del Giudice M (2020) Rethinking the fast-slow continuum of individual differences. Evol Hum Behav 41:536–549. https://doi.org/10.1016/j.evolhumbehav.2020.05.004
Delany ME, Krupkin AB, Miller MM (2000) Organization of telomere sequences in birds: evidence for arrays of extreme length and for in vivo shortening. Cytogenet Genome Res 90:139–145
Dixon L, Kuster R, Rueppell O (2014) Reproduction, social behavior, and aging trajectories in honeybee workers. Age (Omaha) 36:89–101. https://doi.org/10.1007/s11357-013-9546-7
Dupoué A, Rutschmann A, Le Galliard JF et al (2017) Shorter telomeres precede population extinction in wild lizards. Sci Rep 7:1–8. https://doi.org/10.1038/s41598-017-17323-z
Eastwood JR, Hall ML, Teunissen N et al (2019) Early-life telomere length predicts lifespan and lifetime reproductive success in a wild bird. Mol Ecol 28:1127–1137. https://doi.org/10.1111/mec.15002
Ebert TA, Russell MP, Gamba G, Bodnar A (2008) Growth, survival, and longevity estimates for the rock-boring sea urchin Echinometra lucunter lucunter (Echinodermata, Echinoidea) in Bermuda. Bull Mar Sci 82:381–403
Eisenberg DTA (2014) Inconsistent inheritance of telomere length (T): is offspring TL more strongly correlated with maternal or paternal TL? Eur J Hum Genet. https://doi.org/10.1038/ejhg.2013.202
Eisenberg DTA, Hayes MG, Kuzawa CW (2012) Delayed paternal age of reproduction in humans is associated with longer telomeres across two generations of descendants. Proc Natl Acad Sci USA 109:10251–10256. https://doi.org/10.1073/pnas.1202092109
Eisenberg DTA, Tackney J, Cawthon RM et al (2017) Paternal and grandpaternal ages at conception and descendant telomere lengths in chimpanzees and humans. Am J Phys Anthropol. https://doi.org/10.1002/ajpa.23109
Elmore LW, Norris MW, Sircar S et al (2008) Upregulation of telomerase function during tissue regeneration. Exp Biol Med 233:958–967. https://doi.org/10.3181/0712-RM-345
Entringer S, Epel ES, Kumsta R et al (2011) Stress exposure in intrauterine life is associated with shorter telomere length in young adulthood. Proc Natl Acad Sci U S A 108:E513–E518. https://doi.org/10.1073/pnas.1107759108
Entringer S, de Punder K, Buss C, Wadhwa PD (2018) The fetal programming of telomere biology hypothesis: an update. Philos Trans R Soc B Biol Sci 373:20170151. https://doi.org/10.1098/rstb.2017.0151
Factor-Litvak P, Susser E, Kezios K et al (2016) Leukocyte telomere length in newborns: implications for the role of telomeres in Human Disease. Pediatrics. https://doi.org/10.1542/peds.2015-3927
Fairclough SR, Chen Z, Kramer E et al (2013) Premetazoan genome evolution and the regulation of cell differentiation in the choanoflagellate Salpingoeca rosetta. Genome Biol 14:1–15. https://doi.org/10.1186/gb-2013-14-2-r15
Fairlie J, Holland R, Pilkington JG et al (2016) Lifelong leukocyte telomere dynamics and survival in a free-living mammal. Aging Cell 15:140–148. https://doi.org/10.1111/acel.12417
Fajkus P, Adámik M, Nelson ADL et al (2023) Telomerase RNA in Hymenoptera (Insecta) switched to plant/ciliate-like biogenesis. Nucleic Acids Res 51:420–433. https://doi.org/10.1093/nar/gkac1202
Fitzpatrick LJ, Olsson M, Pauliny A et al (2021) Individual telomere dynamics and their links to life history in a viviparous lizard. Proc R Soc B Biol Sci. https://doi.org/10.1098/rspb.2021.0271
Fradiani PA, Ascenzioni F, Lavitrano M, Donini P (2004) Telomeres and telomerase activity in pig tissues. Biochimie 86:7–12. https://doi.org/10.1016/j.biochi.2003.11.009
Francis N, Gregg T, Owen R et al (2006) Lack of age-associated telomere shortening in long- and short-lived species of sea urchins. FEBS Lett 580:4713–4717. https://doi.org/10.1016/j.febslet.2006.07.049
Freitas-Simoes TM, Ros E, Sala-Vila A (2016) Nutrients, foods, dietary patterns and telomere length: update of epidemiological studies and randomized trials. Metabolism 65:406–415. https://doi.org/10.1016/j.metabol.2015.11.004
Frenck RW, Blackburn EH, Shannon KM (1998) The rate of telomere sequence loss in human leukocytes varies with age. PNAS 95:5607–5610
Friedrich U, Griese EU, Schwab M et al (2000) Telomere length in different tissues of elderly patients. Mech Ageing Dev 119:89–99. https://doi.org/10.1016/S0047-6374(00)00173-1
Fulnečková J, Ševčíková T, Fajkus J et al (2013) A broad phylogenetic survey unveils the diversity and evolution of telomeres in eukaryotes. Genome Biol Evol 5:468–483. https://doi.org/10.1093/gbe/evt019
Gao J, Munch SB (2015) Telomere length in Menidia menidia? PLoS ONE 10:e0125674. https://doi.org/10.1371/journal.pone.0125674
Gardner M, Bann D, Wiley L et al (2014) Gender and telomere length: systematic review and meta-analysis. Exp Gerontol 51:15–27. https://doi.org/10.1016/j.exger.2013.12.004
Geiger S, Le Vaillant M, Lebard T et al (2012) Catching-up but telomere loss: half-opening the black box of growth and ageing trade-off in wild king penguin chicks. Mol Ecol 21:1500–1510. https://doi.org/10.1111/j.1365-294X.2011.05331.x
Geserick C, Tejera A, González-Suárez E et al (2006) Expression of mTert in primary murine cells links the growth-promoting effects of telomerase to transforming growth factor-β signaling. Oncogene 25:4310–4319. https://doi.org/10.1038/sj.onc.1209465
Gladyshev EA, Arkhipova IR (2007) Telomere-associated endonuclease-deficient Penelope-like retroelements in diverse eukaryotes. Proc Natl Acad Sci USA 104:9352–9357. https://doi.org/10.1073/pnas.0702741104
Godwin RM, Frusher S, Montgomery SS, Ovenden J (2011) Telomere length analysis in crustacean species: Metapenaeus macleayi, Sagmariasus verreauxi, and Jasus edwardsii. ICES J Mar Sci 68:2053–2058. https://doi.org/10.1093/icesjms/fsr144
Gomes NMV, Shay JW, Wright WE (2010) Telomere biology in metazoa. Fed Eur Biochem Soc 584:3741–3751. https://doi.org/10.1016/j.febslet.2010.07.031
Gomes NMV, Ryder OA, Houck ML et al (2011) Comparative biology of mammalian telomeres: hypotheses on ancestral states and the roles of telomeres in longevity determination. Aging Cell 10:761–768. https://doi.org/10.1111/j.1474-9726.2011.00718.x
Gorbunova V, Seluanov A (2009) Coevolution of telomerase activity and body mass in mammals: from mice to beavers. Mech Ageing Dev 130:1–7. https://doi.org/10.1016/j.mad.2008.02.008.Coevolution
Greider CW, Blackburn EH (1985) Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 43:405–413. https://doi.org/10.1016/0092-8674(85)90170-9
Greider CW, Blackburn EH (1989) A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature 337:331–337. https://doi.org/10.1038/337331a0
Gruber H, Schaible R, Ridgway ID et al (2014) Telomere-independent ageing in the longest-lived non-colonial animal, Arctica islandica. Exp Gerontol 51:38–45. https://doi.org/10.1016/j.exger.2013.12.014
Haendeler J, Dröse S, Büchner N et al (2009) Mitochondrial telomerase reverse transcriptase binds to and protects mitochondrial DNA and function from damage. Arterioscler Thromb Vasc Biol 29:929–935. https://doi.org/10.1161/ATVBAHA.109.185546
Hallmann K, Griebeler EM (2018) An exploration of differences in the scaling of life history traits with body mass within reptiles and between amniotes. Ecol Evol 8:5480–5494. https://doi.org/10.1002/ece3.4069
Harley CB, Futcher AB, Greider CW (1990) Telomeres shorten during ageing of human fibroblasts. Nature 345:458–460. https://doi.org/10.1038/345458a0
Harshman LG, Zera AJ (2007) The cost of reproduction: the devil in the details. Trends Ecol Evol 22:80–86. https://doi.org/10.1016/j.tree.2006.10.008
Hartmann A, Heinze J (2003) Lay eggs, live longer: division of labor and life span in a clonal ant species. Evol (NY) 57:2424–2429. https://doi.org/10.1111/j.0014-3820.2003.tb00254.x
Haussmann MF, Winkler DW, O’Reilly KM et al (2003) Telomeres shorten more slowly in long-lived birds and mammals than in short-lived ones. Proc R Soc B Biol Sci 270:1387–1392. https://doi.org/10.1098/rspb.2003.2385
Haussmann MF, Winkler DW, Huntington CE et al (2007) Telomerase activity is maintained throughout the lifespan of long-lived birds. Exp Gerontol 42:610–618. https://doi.org/10.1016/j.exger.2007.03.004
Hayflick L (1965) The limited in vitro lifetime of human diploid cell strains. Exp Cell Res 37:614–636. https://doi.org/10.1016/0014-4827(65)90211-9
Hayflick L, Moorhead P (1961) The serial cultivation of human diploid cell strains. Exp Cell Res 25:585–621
Healy K, Guillerme T, Finlay S et al (2014) Ecology and mode-of-life explain lifespan variation in birds and mammals. Proc R Soc B Biol Sci. https://doi.org/10.1098/rspb.2014.0298
Heidinger BJ, Blount JD, Boner W et al (2011) Telomere length in early life predicts lifespan. PNAS 109:1–6. https://doi.org/10.1073/pnas.1113306109
Heidinger BJ, Blount JD, Boner W et al (2012) Telomere length in early life predicts life span. Obstet Gynecol Surv 67:283–284. https://doi.org/10.1097/OGX.0b013e3182546dd0
Herrmann M, Pusceddu I, Herrmann W (2018) Telomere biology and age-related diseases. Clin Chem Lab Med 56:1210–1222
Hiebert LS, Simpson C, Tiozzo S (2021) Coloniality, clonality, and modularity in animals: the elephant in the room. J Exp Zool Part B Mol Dev Evol 336:198–211. https://doi.org/10.1002/jez.b.22944
Hjelmborg JB, Dalgård C, Möller S et al (2015) The heritability of leucocyte telomere length dynamics. J Med Genet 52:297–302. https://doi.org/10.1136/jmedgenet-2014-102736
Hoelzl F, Smith S, Cornils JS et al (2016) Telomeres are elongated in older individuals in a hibernating rodent, the edible dormouse (Glis glis). Sci Rep 6:1–9. https://doi.org/10.1038/srep36856
Holmes DJ, Flückiger R, Austad SN (2001) Comparative biology of aging in birds: an update. Exp Gerontol 36:869–883. https://doi.org/10.1016/S0531-5565(00)00247-3
Howard RJ, Giacomelli M, Lozano-Fernandez J et al (2022) The ediacaran origin of Ecdysozoa: integrating fossil and phylogenomic data. J Geol Soc London. https://doi.org/10.1144/jgs2021-107
Ingles ED, Deakin JE (2016) Telomeres, species differences, and unusual telomeres in vertebrates: presenting challenges and opportunities to understanding telomere dynamics. AIMS Genet 03:001–024. https://doi.org/10.3934/genet.2016.1.1
Jayesh P, Vrinda S, Priyaja P et al (2016) Impaired telomerase activity hinders proliferation and in vitro transformation of Penaeus monodon lymphoid cells. Cytotechnology 68:1301–1314. https://doi.org/10.1007/s10616-015-9890-9
Jones DP (2008) Radical-free biology of oxidative stress. Am J Physiol Cell Physiol 295:C849–C868. https://doi.org/10.1152/ajpcell.00283.2008
Joseph NA, Chen C-F, Chen H-H, Chen L-Y (2022) Monitoring telomere maintenance during regeneration of Annelids. Methods Mol Biol 2450:467–478
Kalmbach KH, Antunes DMF, Cracxler RC et al (2013) Telomeres and human reproduction. Fertil Steril 99:1–7. https://doi.org/10.1016/j.fertnstert.2012.11.039.Telomeres
Kimura M, Cherkas LF, Kato BS et al (2008) Offspring ’s leukocyte telomere length, Paternal Ag, and Telomere Elongation in sperm. PLoS Genet 4:1–9. https://doi.org/10.1371/journal.pgen.0040037
Klapper W, Kühne K, Singh KK et al (1998) Longevity of lobsters is linked to ubiquitous telomerase expression. FEBS Lett 439:143–146
Kohlmeier P, Negroni MA, Kever M et al (2017) Intrinsic worker mortality depends on behavioral caste and the queens’ presence in a social insect. Sci Nat 104:34. https://doi.org/10.1007/s00114-017-1452-x
Korandová M, Frydrychová R (2016) Activity of telomerase and telomeric length in Apis mellifera. Chromosoma 125:405–411. https://doi.org/10.1007/s00412-015-0547-4
Korandová M, Krůček T, Vrbová K, Frydrychová RC (2014) Distribution of TTAGG-specific telomerase activity in insects. Chromosom Res 22:495–503
Korandová M, Krůček T, Szakosová K et al (2018) Chronic low-dose pro-oxidant treatment stimulates transcriptional activity of telomeric retroelements and increases telomere length in Drosophila. J Insect Physiol 104:1–8. https://doi.org/10.1016/j.jinsphys.2017.11.002
Koroleva AG, Evtushenko EV, Timoshkin OA et al (2013) Telomeric DNA length and phylogenetic relationship of Baikal and siberian planarians (Turbellaria, Tricladida). Cell tissue biol 7:369–374. https://doi.org/10.1134/S1990519X13040081
Koroleva AG, Evtushenko EV, Vershinin AV et al (2020) Age Dynamics of Telomere length in endemic Baikal Planarians. Mol Biol 54:553–562. https://doi.org/10.1134/S002689332004007X
Kotrschal A, Ilmonen P, Penn DJ (2007) Stress impacts telomere dynamics. Biol Lett 3:128–130. https://doi.org/10.1098/rsbl.2006.0594
Koubová J, Čapková Frydrychová R (2021) Telomerase-positive somatic tissues of honeybee queens (Apis mellifera) display no DNA replication. Cytogenet Genome Res Oct 14:1–6
Koubová J, Jehlík T, Kodrik D et al (2019) Telomerase activity is upregulated in the fat bodies of pre-diapause bumblebee queens (Bombus terrestris). Insect Biochem Mol Biol 115:103241
Koubová J, Pangrácová M, Jankásek M et al (2021) Long-lived termite kings and queens activate telomerase in somatic organs. Proc R Soc B 288:20210511
Koziol C, Borojevic R, Stefen R, Muller WEG (1998) Sponges (Porifera) model systems to study the shift from immortal to senescent somatic cells: the telomerase activity in somatic cells. Mech Ageing Dev 100:107–120
Kresovich JK, Parks CG, Sandler DP, Taylor JA (2018) Reproductive history and blood cell telomere length. Aging 10:2383–2393. https://doi.org/10.18632/aging.101558
Kuszewska K, Miler K, Rojek W, Woyciechowski M (2017) Honeybee workers with higher reproductive potential live longer lives. Exp Gerontol 98:8–12. https://doi.org/10.1016/j.exger.2017.08.022
Lai AG, Pouchkina-Stantcheva N, Di Donfrancesco A et al (2017) The protein subunit of telomerase displays patterns of dynamic evolution and conservation across different metazoan taxa. BMC Evol Biol 17:1–21. https://doi.org/10.1186/s12862-017-0949-4
Laird DJ, Weissman IL (2004) Telomerase maintained in self-renewing tissues during serial regeneration of the urochordate Botryllus schlosseri. Dev Biol 273:185–194. https://doi.org/10.1016/j.ydbio.2004.05.029
Lang GH, Wang Y, Nomura N, Matsumura M (2004) Detection of telomerase activity in tissues and primary cultured lymphoid cells of Penaeus japonicus. Mar Biotechnol 6:347–354. https://doi.org/10.1007/s10126-003-0038-0
Lansdorp PM (2022) Sex differences in telomere length, lifespan, and embryonic dyskerin levels. Aging Cell 21:1–5. https://doi.org/10.1111/acel.13614
Lapp HE, Bartlett AA, Hunter RG (2019) Stress and glucocorticoid receptor regulation of mitochondrial gene expression. J Mol Endocrinol 62:R121–R128. https://doi.org/10.1530/JME-18-0152
Laumer CE, Fernández R, Lemer S et al (2019) Revisiting metazoan phylogeny with genomic sampling of all phyla. Proc R Soc B Biol Sci. https://doi.org/10.1098/rspb.2019.0831
Law E, Girgis A, Sylvie L et al (2016) Telomeres and stress: promising avenues for research in psycho-oncology. Asia-Pacific J Oncol Nurs 3:137–147. https://doi.org/10.4103/2347-5625.182931
Lejnine S, Makarov VL, Langmore JP (1995) Conserved nucleoprotein structure at the ends of vertebrate and invertebrate chromosomes. Proc Natl Acad Sci USA 92:2393–2397. https://doi.org/10.1073/pnas.92.6.2393
Liker A, Székely T (2005) Mortality costs of sexual selection and parental care in natural populations of birds. Evol (NY) 59:890–897. https://doi.org/10.1111/j.0014-3820.2005.tb01762.x
Lin J, Epel E (2022) Stress and telomere shortening: insights from cellular mechanisms. Ageing Res Rev. https://doi.org/10.1016/j.arr.2021.101507
Liu L, Trimarchi JR, Smith PJS, Keefe DL (2002) Mitochondrial dysfunction leads to telomere attrition and genomic instability. Aging Cell 1:40–46. https://doi.org/10.1046/j.1474-9728.2002.00004.x
Lou Z, Wei J, Riethman H et al (2009) Telomere length regulates ISG15 xpression in human cells. Aging 1:608–621
Lucas ER, Keller L (2018) Elevated expression of ageing and immunity genes in queens of the black garden ant. Exp Gerontol 108:92–98. https://doi.org/10.1016/j.exger.2018.03.020
Lyčka M, Peska V, Demko M et al (2021) WALTER: an easy way to online evaluate telomere lengths from terminal restriction fragment analysis. BMC Bioinform 22:1–14. https://doi.org/10.1186/s12859-021-04064-0
Majer AD, Fasanello VJ, Tindle K et al (2019) Is there an oxidative cost of acute stress? Characterization, implication of glucocorticoids and modulation by prior stress experience. Proc R Soc B Biol Sci. https://doi.org/10.1098/rspb.2019.1698
Majoe M, Libbrecht R, Foitzik S, Nehring V (2021) Queen loss increases worker survival in leaf-cutting ants under paraquat-induced oxidative stress. Philos Trans R Soc B Biol Sci 376:20190735. https://doi.org/10.1098/rstb.2019.0735
Marais GAB, Gaillard JM, Vieira C et al (2018) Sex gap in aging and longevity: can sex chromosomes play a role? Biol Sex Differ 9:1–14. https://doi.org/10.1186/s13293-018-0181-y
Mason JM, Reddy HM, Capkova Frydrychova R (2011) Telomere maintenance in organisms without telomerase. In: Seligman H (ed) DNA Replication-Current Advances. InTech, London, pp 323–346
Mason JM, Randall TA, Frydrychova RC (2016) Telomerase lost? Chromosoma 125:65–73. https://doi.org/10.1007/s00412-015-0528-7
Maximova N, Koroleva A, Sitnikova T et al (2017) Age dynamics of telomere length of Baikal gastropods is sex-specific and multidirectional. Folia Biol 65:187–197. https://doi.org/10.3409/fb65_4.187
McLennan D, Armstrong JD, Stewart DC et al (2017) Shorter juvenile telomere length is associated with higher survival to spawning in migratory Atlantic salmon. Funct Ecol 31:2070–2079. https://doi.org/10.1111/1365-2435.12939
Meyne J, Ratliff R, l, Moyzis RK (1989) Conservation of the human telomere sequence (TTAGGG)n among vertebrates. Proc Natl Acad Sci USA 86:7049–7053
Montpetit AJ, Alhareeri AA, Montpetit M et al (2014) Telomere length: a review of methods for measurement. Nurs Res 63:289–299. https://doi.org/10.1097/NNR.0000000000000037
Moyzis RK, Buckingham JM, Cram LS et al (1988) A highly conserved repetitive DNA sequence, (TTAGGG)n, present at the telomeres of human chromosomes. Proc Natl Acad Sci USA 85:6622–6626
Mukherjee S, Firpo EJ, Wang Y, Roberts JM (2011) Separation of telomerase functions by reverse genetics. Proc Natl Acad Sci USA 108:1363–1371. https://doi.org/10.1073/pnas.1112414108
Muller HJ (1938) The remaking of chromosomes. Collect Nat 13:181–198
Müller WEG, Müller IM (2003) The hypothetical ancestral animal the Urmetazoa: telomerase activity in sponges (Porifera). J Serbian Chem Soc 68:257–268. https://doi.org/10.2298/jsc0305257w
Muraki K, Nyhan K, Han L, John P (2012) Mechanisms of telomere loss and their consequences for chromosome instability. Front Oncol 2:1–13. https://doi.org/10.3389/fonc.2012.00135
Negroni MA, Foitzik S, Feldmeyer B (2019) Long-lived Temnothorax ant queens switch from investment in immunity to antioxidant production with age. Sci Rep 9:1–10. https://doi.org/10.1038/s41598-019-43796-1
Neumann AA, Watson CM, Noble JR et al (2013) Alternative lengthening of telomeres in normal mammalian somatic cells. Genes Dev 18:18–23. https://doi.org/10.1101/gad.205062.112.Freely
Njajou OT, Cawthon RM, Damcott CM et al (2007) Telomere length is paternally inherited and is associated with parental lifespan. Proc Natl Acad Sci 104:12135–12139
Noguera JC, Velando A (2019) Bird embryos perceive vibratory cues of predation risk from clutch mates. Nat Ecol Evol 3:1225–1232. https://doi.org/10.1038/s41559-019-0929-8
Nordfjall K, Larefalk A, Lindgren P et al (2005) Telomere length and heredity: indications of paternal inheritance. PNAS 102:16374–16378. https://doi.org/10.1073/pnas.0501724102
Ojimi MC, Isomura N, Hidaka M (2009) Telomerase activity is not related to life history stage in the jellyfish Cassiopea sp. Comp Biochem Physiol - A Mol Integr Physiol 152:240–244. https://doi.org/10.1016/j.cbpa.2008.10.008
Okuda K, Bardeguez A, Gardner JP et al (2002) Telomere length in the Newborn. Pediatr Res 52:377–381. https://doi.org/10.1203/01.pdr.0000022341.72856.72
Olovnikov AM (1973) A theory of marginotomy. J Theor Biol 41:181–190. https://doi.org/10.1016/0022-5193(73)90198-7
Olsson M, Pauliny A, Wapstra E, Blomqvist D (2010) Proximate determinants of telomere length in sand lizards (Lacerta agilis). Biol Lett 6:651–653. https://doi.org/10.1098/rsbl.2010.0126
Olsson M, Wapstra E, Friesen C (2018) Ectothermic telomeres: it’s time they came in from the cold. Philos Trans R Soc B Biol Sci 373:20160449. https://doi.org/10.1098/rstb.2016.0449
Owen R, Sarkis S, Bodnar A (2007) Developmental pattern of telomerase expression in the sand scallop, Euvola ziczac. Invertebr Biol 126:40–45. https://doi.org/10.1111/j.1744-7410.2007.00074.x
Paitz RT, Haussmann MF, Bowden RM et al (2004) Long telomeres may minimize the effect of aging in the painted turtle. Integr Comp Biol 44:617
Panasiak L, Dobosz S, Ocalewicz K (2020) Telomere dynamics in the diploid and triploid rainbow trout (Oncorhynchus mykiss) assessed by q-fish analysis. Genes (Basel) 11:1–12. https://doi.org/10.3390/genes11070786
Panasiak L, Szubert K, Polonis M, Ocalewicz K (2022) Telomere length variation does not correspond with the growth disturbances in the rainbow trout (Oncorhynchus mykiss). J Appl Genet 63:133–139. https://doi.org/10.1007/s13353-021-00669-6
Parry GD (1981) The meanings of r- and K-Selection. Oecologia 48:260–264
Pascual-Torner M, Carrero D, Perez-Silva JG et al (2022) Comparative genomics of mortal and immortal cnidarians unveils novel keys behind rejuvenation. Proc Natl Acad Sci USA 119:1–8. https://doi.org/10.1073/pnas.2118763119
Passos F, Saretzki G, Ahmed S et al (2007) Mitochondrial dysfunction accounts for the stochastic heterogeneity in telomere-dependent senescence. Plos Biol 5:1138–1151. https://doi.org/10.1371/journal.pbio.0050110
Pepke M, Le, Eisenberg DTA (2022) On the comparative biology of mammalian telomeres: telomere length co-evolves with body mass, lifespan and cancer risk. Mol Ecol 31:6286–6296. https://doi.org/10.1111/mec.15870
Pepper GV, Bateson M, Nettle D (2018) Telomeres as integrative markers of exposure to stress and adversity: a systematic review and meta-analysis. R Soc Open Sci. https://doi.org/10.1098/rsos.180744
Picard M, McEwen BS, Epel ES, Sandi C (2018) An energetic view of stress: focus on mitochondria. Front Neuroendocrinol 49:72–85. https://doi.org/10.1016/j.yfrne.2018.01.001
Plot V, Criscuolo F, Zahn S, Georges JY (2012) Telomeres, age and reproduction in a long-lived reptile. PLoS ONE 7:1–6. https://doi.org/10.1371/journal.pone.0040855
Poon SS, Lansdorp PM (2001) Quantitative fluorescence in situ hybridization (Q-FISH). Curr Protoc Cell Biol Chap 18:1–21. https://doi.org/10.1002/0471143030.cb1804s12
Prušáková D, Peska V, Pekár S et al (2021) Telomeric DNA sequences in beetle taxa vary with species richness. Sci Rep 11:13319. https://doi.org/10.1038/s41598-021-92705-y
Reddien PW (2018) The cellular and molecular basis for planarian regeneration Peter. Cell 175:327–345. https://doi.org/10.1053/j.gastro.2016.08.014.CagY
Rehkopf DH, Needham BL, Lin J et al (2016) Leukocyte telomere length in relation to 17 biomarkers of Cardiovascular Disease Risk: a cross-sectional study of US adults. PLoS Med. https://doi.org/10.1371/journal.pmed.1002188
Remot F, Ronget V, Froy H et al (2020) No sex differences in adult telomere length across vertebrates: a meta-analysis: sex differences in adult telomere length. R Soc Open Sci 7:200548. https://doi.org/10.1098/rsos.200548
Reznick D (1985) Costs of reproduction: an evaluation of the empirical evidence. Oikos 44:257–267
Robertson HM (2009) Simple telomeres in a simple animal: absence of subtelomeric repeat regions in the placozoan Trichoplax adhaerens. Genetics 181:323–325. https://doi.org/10.1534/genetics.108.096289
Rocca MS, Foresta C, Ferlin A (2019) Telomere length: lights and shadows on their role in human reproduction. Biol Reprod 100:305–317. https://doi.org/10.1093/biolre/ioy208
Rodrigue KL, May BP, Famula TR, Delany ME (2005) Meiotic instability of chicken ultra-long telomeres and mapping of a 2.8 megabase array to the W-sex chromosome. Chromosom Res 13:581–591. https://doi.org/10.1007/s10577-005-0984-7
Rollings N, Uhrig EJ, Krohmer RW et al (2017) Age-related sex differences in body condition and telomere dynamics of red-sided garter snakes. Proc R Soc B Biol Sci. https://doi.org/10.1098/rspb.2016.2146
Romano GH, Harari Y, Yehuda T et al (2013) Environmental stresses disrupt telomere length homeostasis. PLoS Genet 9:e1003721. https://doi.org/10.1371/journal.pgen.1003721
Sahara K, Marec F, Traut W (1999) TTAGG telomeric repeats in chromosomes of some insects and other arthropods. Chromosome Res 7:449–460
Sakai M, Okumura SI, Onuma K et al (2007) Identification of a telomere sequence type in three sponge species (Porifera) by fluorescence in situ hybridization analysis. Fish Sci 73:77–80. https://doi.org/10.1111/j.1444-2906.2007.01304.x
Sánchez-Montes G, Martínez-Solano Í, Díaz-Paniagua C et al (2020) Telomere attrition with age in a wild amphibian population. Biol Lett 16:20200168. https://doi.org/10.1098/rsbl.2020.0168
Sanders JL, Newman AB (2013) Telomere length in epidemiology: a biomarker of aging, age-related disease, both, or neither? Epidemiol Rev 35:112–131. https://doi.org/10.1093/epirev/mxs008
Saretzki G (2009) Telomerase, mitochondria and oxidative stress. Exp Gerontol 44:485–492. https://doi.org/10.1016/j.exger.2009.05.004
Sauer DJ, Heidinger BJ, Kittilson JD et al (2021) No evidence of physiological declines with age in an extremely long-lived fish. Sci Rep 11:9065. https://doi.org/10.1038/s41598-021-88626-5
Schneider SA, Schrader C, Wagner AE et al (2011) Stress resistance and longevity are not directly linked to levels of enzymatic antioxidants in the ponerine ant Harpegnathos saltator. PLoS ONE 6:e14601. https://doi.org/10.1371/journal.pone.0014601
Schultz DT, Haddock SHD, Bredeson JV et al (2023) Ancient gene linkages support ctenophores as sister to other animals. Nature 618:110–117. https://doi.org/10.1038/s41586-023-05936-6
Schumpert C, Nelson J, Kim E et al (2015) Telomerase activity and telomere length in Daphnia. PLoS ONE 10:1–15. https://doi.org/10.1371/journal.pone.0127196
Schutte NS, Malouff JM (2016) The relationship between perceived stress and telomere length: a meta-analysis. Stress Heal 32:313–319. https://doi.org/10.1002/smi.2607
Scott NM, Haussmann MF, Elsey RM et al (2006) Telomere length shortens with body length in Alligator mississippiensis. Southeast Nat 5:685–692. https://doi.org/10.1656/1528-7092(2006)5[685:TLSWBL]2.0.CO;2
Ségal-Bendirdjian E, Geli V, Cayuela ML (2019) Non-canonical roles of telomerase: unraveling the imbroglio. Front Cell Dev Biol 7:1–12. https://doi.org/10.3389/fcell.2019.00332
Seluanov A, Chen Z, Hine C et al (2007) Telomerase activity coevolves with body mass, not lifespan. Aging Cell 6:45–52. https://doi.org/10.1111/j.1474-9726.2006.00262.x.Telomerase
Sharaf R, Frampton GM, Albacker LA (2022) Mutations in the TERC template sequence can be incorporated into the telomeres of human tumors. PLoS ONE 17:1–7. https://doi.org/10.1371/journal.pone.0272707
Shokhirev MN, Johnson AA (2014) Effects of extrinsic mortality on the evolution of aging: a stochastic modeling approach. PLoS ONE. https://doi.org/10.1371/journal.pone.0086602
Sholes SL, Karimian K, Gershman A et al (2022) Chromosome-specific telomere lengths and the minimal functional telomere revealed by nanopore sequencing. Genome Res 32:616–628. https://doi.org/10.1101/gr.275868.121
Silva B, Arora R, Azzalin CM (2022) The alternative lengthening of telomeres mechanism jeopardizes telomere integrity if not properly restricted. Proc Natl Acad Sci USA 119:3–5. https://doi.org/10.1073/pnas.2208669119
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. Physiol Biochem Zool 89:441–447. https://doi.org/10.1086/687378
Sinclair CS, Richmond RH, Ostrander GK (2007) Characterization of the telomere regions of scleractinian coral, Acropora surculosa. Genetica 129:227–233. https://doi.org/10.1007/s10709-006-0001-x
Singchat W, Kraichak E, Tawichasri P et al (2019) Dynamics of telomere length in captive siamese cobra (Naja kaouthia) related to age and sex. Ecol Evol 9:6366–6377. https://doi.org/10.1002/ece3.5208
Sköld HN, Asplund ME, Wood CA, Bishop JDD (2011) Telomerase deficiency in a colonial ascidian after prolonged asexual propagation. J Exp Zool Part B Mol Dev Evol 316B:276–283. https://doi.org/10.1002/jez.b.21399
Slagboom PE, Droog S, Boomsma D (1994) Genetic determination of Telomere size in humans: a twin study of three age groups. Am J Hum Genet 55:876–882
Speakman JR (2005) Body size, energy metabolism and lifespan. J Exp Biol 208:1717–1730. https://doi.org/10.1242/jeb.01556
Spurgin LG, Bebbington K, Fairfield EA et al (2018) Spatio-temporal variation in lifelong telomere dynamics in a long-term ecological study. J Anim Ecol 87:187–198. https://doi.org/10.1111/1365-2656.12741
Tan TCJ, Rahman R, Jaber-Hijazi F et al (2012) Telomere maintenance and telomerase activity are differentially regulated in asexual and sexual worms. Proc Natl Acad Sci USA 109:4209–4214. https://doi.org/10.1073/pnas.1118885109
Tham CY, Poon LF, Yan TD et al (2023) High-throughput telomere length measurement at nucleotide resolution using the PacBio high fidelity sequencing platform. Nat Commun. https://doi.org/10.1038/s41467-023-35823-7
Tian X, Doerig K, Park R et al (2018) Evolution of telomere maintenance and tumour suppressor mechanisms across mammals. Philos Trans R Soc B Biol Sci. https://doi.org/10.1098/rstb.2016.0443
Traut W, Szczepanowski M, Vítková M et al (2007a) The telomere repeat motif of basal metazoa. Chromosome Res 15:371–382. https://doi.org/10.1007/s10577-007-1132-3
Tricola GM, Simons MJP, Atema E et al (2018) The rate of telomere loss is related to maximum lifespan in birds. Philos Trans R Soc B Biol Sci 373:20160445. https://doi.org/10.1098/rstb.2016.0445
Turner S, Wong HP, Rai J, Hartshorne GM (2010) Telomere lengths in human oocytes, cleavage stage embryos and blastocysts. Mol Hum Reprod 16:685–694. https://doi.org/10.1093/molehr/gaq048
Ujvari B, Biro PA, Charters JE et al (2017) Curvilinear telomere length dynamics in a squamate reptile. Funct Ecol 31:753–759. https://doi.org/10.1111/1365-2435.12764
Vaiserman AM (2014) Early-life nutritional programming of longevity. J Dev Orig Health Dis 5:325–338. https://doi.org/10.1017/S2040174414000294
van Lieshout SHJ, Bretman A, Newman C et al (2019) Individual variation in early-life telomere length and survival in a wild mammal. Mol Ecol 28:4152–4165. https://doi.org/10.1111/mec.15212
Varney RM, Pomory CM, Janosik AM (2017) Telomere elongation and telomerase expression in regenerating arms of the starfish Luidia clathrata (Asteroidea: Echinodermata). Mar Biol 164:1–6. https://doi.org/10.1007/s00227-017-3230-x
Verhulst S, Dalgård C, Labat C et al (2016) A short leucocyte telomere length is associated with development of insulin resistance. Diabetologia 59:1258–1265. https://doi.org/10.1007/s00125-016-3915-6
Vítková M, Král J, Traut W et al (2005) The evolutionary origin of insect telomeric repeats, (TTAGG)n. Chromosome Res 13:145–156. https://doi.org/10.1007/s10577-005-7721-0
Vogt G (2012) Ageing and longevity in the Decapoda (Crustacea): a review. Zool Anz 251:1–25. https://doi.org/10.1016/j.jcz.2011.05.003
von Zglinicki T (2002) Oxidative stress shortens telomeres. Trends Biochem Sci 27:339–344
Wanamaker AD, Heinemeier J, Scourse JD et al (2008) Very long lived mollusks confirm 17th century AD tephra based radiocarbon reservoir ages for north icelandic shelf waters. Radiocarbon 50:399–412. https://doi.org/10.1017/S0033822200053510
Wang Q, Zhan Y, Pedersen NL et al (2018) Telomere length and all-cause mortality: a Meta-analysis. Ageing Res Rev 48:11–20. https://doi.org/10.1016/j.arr.2018.09.002
Watson JD (1972) Origin of Concatemeric T7DNA. Nat New Biol 239:197–201
Whittemore K, Vera E, Martínez-Nevado E et al (2019) Telomere shortening rate predicts species life span. Proc Natl Acad Sci USA 116:15122–15127. https://doi.org/10.1073/pnas.1902452116
Wicky C, Villeneuve a M, Lauper N et al (1996) Telomeric repeats (TTAGGC)n are sufficient for chromosome capping function in Caenorhabditis elegans. Proc Natl Acad Sci U S A 93:8983–8988
Wilbourn RV, Moatt JP, Froy H et al (2018) The relationship between telomere length and mortality risk in non-model vertebrate systems: a meta-analysis. Philos Trans R Soc B Biol Sci 373:20160447. https://doi.org/10.1098/rstb.2016.0447
Wright WE, Piatyszek MA, Rainey WE et al (1996) Telomerase activity inHuman germline and embryonic tissues and cells. Dev Genet 18:173–179
Wright D, Gibbons W, Lanzendorf S (2000) Characterization of telomerase activity in the human oocyte and preimplantation embryo. Fertil Steril 74:S67. https://doi.org/10.1016/s0015-0282(00)00902-x
Xirocostas ZA, Everingham SE, Moles AT (2020) The sex with the reduced sex chromosome dies earlier: a comparison across the tree of life. Biol Lett. https://doi.org/10.1098/rsbl.2019.0867
Xu M, Wu XB, Yan P, Zhu HT (2009) Telomere length shortens with age in chinese alligators (Alligator sinensis). J Appl Anim Res 36:109–112. https://doi.org/10.1080/09712119.2009.9707042
Yano K, Stevens JD, Compagno LJV (2004) A review of the systematics of the sleeper shark genus Somniosus with redescriptions of Somniosus (Somniosus) antarcticus and Somniosus (Rhinoscymnus) longus (Squaliformes: Somniosidae). Ichthyol Res 51:360–373. https://doi.org/10.1007/s10228-004-0244-4
Ye J, Renault VM, Jamet K, Gilson E (2014) Transcriptional outcome of telomere signalling. Nat Rev Genet 15:491–503. https://doi.org/10.1038/nrg3743
Yoshida Y, Koutsovoulos G, Laetsch DR et al (2017) Comparative genomics of the tardigrades Hypsibius dujardini and Ramazzottius varieornatus. PLoS Biol 7:e2002266
Zarulli V, Barthold Jones JA, Oksuzyan A et al (2018) Women live longer than men even during severe famines and epidemics. Proc Natl Acad Sci U S A 115:E832–E840. https://doi.org/10.1073/pnas.1701535115
Závodník M, Fajkus P, Franek M et al (2023) Telomerase RNA gene paralogs in plants—the usual pathway to unusual telomeres. New Phytol. https://doi.org/10.1111/nph.19110
Zhdanova NS, Karamisheva TV, Minina J et al (2005) Unusual distribution pattern of telomeric repeats in the shrews Sorex araneus and Sorex granarius. Chromosom Res 13:617–625. https://doi.org/10.1007/s10577-005-0988-3
Zheng Q, Huang J, Wang G et al (2019) Mitochondria, telomeres and telomerase subunits. Front Cell Dev Biol 7:1–10. https://doi.org/10.3389/fcell.2019.00274
Zhou Y, Wang Y, Xiong X et al (2022) Profiles of telomeric repeats in Insecta reveal diverse forms of telomeric motifs in Hymenopterans. Life Sci Alliance 5:1–15. https://doi.org/10.26508/lsa.202101163
Zhu H, Belcher M, van der Harst P (2011) Healthy aging and disease: role for telomere biology? Clin Sci (Lond) 120:427–440. https://doi.org/10.1042/CS20100385
Zielke S, Bodnar A (2010) Telomeres and telomerase activity in scleractinian corals and Symbiodinium spp. Biol Bull 218:113–121. https://doi.org/10.1086/BBLv218n2p113
Zielke S, Bodnar A, Zielke S, Bodnar A (2010) Telomeres and telomerase activity in Scleractinian Corals and Symbiodinium spp. Biol Bull 218:113–121
Acknowledgements
The authors thank to Joshua Wright for critical reading of the manuscript and Jan Zrzavý for advice on the consensus phylogenetic tree of Metazoa. This study was supported by grant from Ministry of Education of the Czech Republic (LUAUS23128), grant from Strategy AV21, Diversity of Life and Health of Ecosystems, and by the projects RVO 60077344 of the Institute of Entomology, BC, České Budějovice.
Author information
Authors and Affiliations
Contributions
RCF designed the main conceptual idea and wrote the manuscript with support of BK and VP, MB and MS assisted with data collecting. All authors discussed the results and contributed to the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflicts of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Frydrychová, R.Č., Konopová, B., Peska, V. et al. Telomeres and telomerase: active but complex players in life-history decisions. Biogerontology 25, 205–226 (2024). https://doi.org/10.1007/s10522-023-10060-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10522-023-10060-z