Abstract
Telomeres are highly conserved nucleoprotein structures which protect genome integrity. The length of telomeres is influenced by both genetic and environmental factors, but relatively little is known about how different hereditary and environmental factors interact in determining telomere length. We manipulated growth rates and timing of maturation by exposing full-sib nine-spined sticklebacks (Pungitius pungitius) to two different temperature treatments and quantified the effects of temperature treatments, sex, timing of maturation, growth rate and family (genetic influences) on telomere length. We did not find the overall effect of temperature treatment on the relative telomere length. However, we found that variation in telomere length was related to timing of maturation in a sex- and temperature-dependent manner. Telomere length was negatively related to age at maturation in elevated temperature and early maturing males and females differed in telomere length. Variation in growth rate did not explain any variation in telomere length. The broad sense heritability (h 2) of telomere length was estimated at h 2 = 0.31 − 0.47, suggesting predominance of environmental over genetic determinants of telomere length variability. This study provides the first evidence that age at maturation together with factors associated with it are influencing telomere length in an ectotherm. Future studies are encouraged to identify the extent to which these results can be replicated in other ectotherms.
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References
Adams CE, Huntingford FA (1997) Growth, maturation and reproductive investment in Arctic charr. J Fish Biol 51:750–759. doi:10.1111/j.1095-8649.1997.tb01996.x
Angelier F, Vleck CM, Holberton RL, Marra PP (2013) Telomere length, non-breeding habitat and return rate in male American redstarts. Funct Ecol 27:342–350. doi:10.1111/1365-2435.12041
Angilletta MJ (2009) Thermal adaptation: a theoretical and empirical synthesis. OUP, Oxford
Asghar M, Bensch S, Tarka M et al (2015) Maternal and genetic factors determine early life telomere length. Proc R Soc B Biol Sci 282:20142263. doi:10.1098/rspb.2014.2263
Atema E, Mulder E, Dugdale HL et al (2015) Heritability of telomere length in the zebra finch. J Ornithol 156:1113–1123. doi:10.1007/s10336-015-1212-7
Aviv A (2006) Telomeres and human somatic fitness. J Gerontol A Biol Sci Med Sci 61:871–873
Baird DM (2008) Mechanisms of telomeric instability. Cytogenet Genome Res 122:308–314. doi:10.1159/000167817
Bakaysa SL, Mucci LA, Slagboom PE, Boomsma DI, McClearn GE, Johansson B, Pedersen NL (2007) Telomere length predicts survival independent of genetic influences. Aging Cell 6:769–774. doi:10.1111/j.1474-9726.2007.00340.x
Barrett ELB, Richardson DS (2011) Sex differences in telomeres and lifespan. Aging Cell 10:913–921. doi:10.1111/j.1474-9726.2011.00741.x
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. doi:10.1098/rspb.2012.2540
Bayne S, Jones ME, Li H, Pinto AR, Simpson ER, Liu JP (2008) Estrogen deficiency leads to telomerase inhibition, telomere shortening and reduced cell proliferation in the adrenal gland of mice. Cell Res 18:1141–1150. doi:10.1038/cr.2008.291
Becker PJJ, Reichert S, Zahn S, Hegelbach J, Massemin S, Keller LF, Postma E, Criscuolo F (2015) Mother-offspring and nest-mate resemblance but no heritability in early-life telomere length in white-throated dippers. Proc R Soc B 282:20142924. doi:10.1098/rspb.2014.2924
Behl C, Skutella T, Lezoualc’h F, Post A, Widmann M, Newton CJ, Holsboer F (1997) Neuroprotection against oxidative stress by estrogens: structure-activity relationship. Mol Pharmacol 51:535–541. doi:10.1124/mol.51.4.535
Bertrand S, Alonso-Alvarez C, Devevey G, Faivre B, Prost J, Sorci G (2005) Carotenoids modulate the trade-off between egg production and resistance to oxidative stress in zebra finches. Oecologia 147:576–584. doi:10.1007/s00442-005-0317-8
Bischoff C, Graakjaer J, Petersen HC, HjelmborgJv Vaupel JW, Bohr V, Koelvraa S, Christensen K (2005) The heritability of telomere length among the elderly and oldest-old. Twin Res Hum Genet 8:433–439. doi:10.1375/twin.8.5.433
Blackburn EH (2000) Telomere states and cell fates. Nature 408:53–56. doi:10.1038/35040500
Blasco MA (2005) Telomeres and human disease: ageing, cancer and beyond. Nat Rev Genet 6:611–622. doi:10.1038/nrg1656
Broer L, Codd V, Nyholt DR, Deelen J, Mangino M, Willemsen G, Albrecht E, Amin N, Beekman M, de Geus EJ, Henders A, Nelson CP, Steves CJ, Wright MJ, de Craen AJ, Isaacs A, Matthews M, Moayyeri A, Montgomery GW, Oostra BA, Vink JM, Spector TD, Slagboom PE, Martin NG, Samani NJ, van Duijn CM, Boomsma DI (2013) Meta-analysis of telomere length in 19,713 subjects reveals high heritability, stronger maternal inheritance and a paternal age effect. Eur J Hum Genet 21:1163–1168. doi:10.1038/ejhg.2012.303
Campisi J (2005) Senescent cells, tumor suppression, and organismal aging: good citizens, bad neighbors. Cell 120:513–522. doi:10.1016/j.cell.2005.02.003
Cawthon RM (2002) Telomere measurement by quantitative PCR. Nucleic Acids Res 30:e47
Daniali L, Benetos A, Susser E, Kark JD, Labat C, Kimura M, Desai K, Granick M, Aviv A (2013) Telomeres shorten at equivalent rates in somatic tissues of adults. Nat Commun 4:1597. doi:10.1038/ncomms2602
Development Core Team R (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0
DormannCF Elith J, Bacher S, Buchmann C, Carl G, Carré G, Marquéz JRG, Gruber B, Lafourcade B, Leitão PJ, Münkemüller T, McClean C, Osborne PE, Reineking B, Schröder B, Skidmore AK, Zurell D, Lautenbach S (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36:27–46. doi:10.1111/j.1600-0587.2012.07348.x
Emaus A, Espetvedt S, Veierød MB, Ballard-Barbash R, Furberg AS, Ellison PT, Jasienska G, Hjartåker A, Thune I (2008) 17-beta-estradiol in relation to age at menarche and adult obesity in premenopausal women. Hum Reprod Oxf Engl 23:919–927. doi:10.1093/humrep/dem432
Epel ES, Blackburn EH, Lin J, Dhabhar FS, Adler NE, Morrow JD, Cawthon RM (2004) Accelerated telomere shortening in response to life stress. Proc Natl Acad Sci USA 101:17312–17315. doi:10.1073/pnas.0407162101
Foote CG, Daunt F, González-Solís J, Nasir L, Phillips RA, Monaghan P (2010) Individual state and survival prospects: age, sex, and telomere length in a long-lived seabird. Behav Ecol arq 178. doi:10.1093/beheco/arq178
Foote CG, Vleck D, Vleck CM (2013) Extent and variability of interstitial telomeric sequences and their effects on estimates of telomere length. Mol Ecol Resour 13:417–428. doi:10.1111/1755-0998.12079
Ganz J, Brand M (2016) Adult neurogenesis in fish. Cold Spring Harb Perspect Biol a019018. doi:10.1101/cshperspect.a019018
Gao J, Munch SB (2015) Does reproductive investment decrease telomere length in Menidiamenidia? PLoS One 10:e0125674. doi:10.1371/journal.pone.0125674
Geiger S, Le Vaillant M, Lebard T, Reichert S, Stier A, LE Maho Y, Criscuolo F (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. doi:10.1111/j.1365-294X.2011.05331.x
Gopalakrishnan S, Cheung NK, Yip BW, Au DW (2013) Medaka fish exhibits longevity gender gap, a natural drop in estrogen and telomere shortening during aging: a unique model for studying sex-dependent longevity. Front Zool 10:78. doi:10.1186/1742-9994-10-78
Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R Package. J Stat Softw 33:1–22
Hamel S, Côté SD, Gaillard JM, Festa-Bianchet M (2009) Individual variation in reproductive costs of reproduction: high-quality females always do better. J Anim Ecol 78:143–151. doi:10.1111/j.1365-2656.2008.01459.x
Hastings NB, Tanapat P, Gould E (2001) Neurogenesis in the adult mammalian brain. Clin Neurosci Res 1:175–182. doi:10.1016/S1566-2772(01)00003-2
Hatakeyama H, Nakamura K-I, Izumiyama-Shimomura N, Ishii A, Tsuchida S, Takubo K, Ishikawa N (2008) The teleost Oryziaslatipes shows telomere shortening with age despite considerable telomerase activity throughout life. Mech Ageing Dev 129:550–557. doi:10.1016/j.mad.2008.05.006
Hatakeyama H, Yamazaki H, Nakamura K-I, Izumiyama-Shimomura N, Aida J, Suzuki H, Tsuchida S, Matsuura M, Takubo K, Ishikawa N (2016) Telomere attrition and restoration in the normal teleost Oryziaslatipes are linked to growth rate and telomerase activity at each life stage. Aging 8:62–75
Hayward A, Gillooly JF (2011) The cost of sex: quantifying energetic investment in gamete production by males and females. PLoS One 6:e16557. doi:10.1371/journal.pone.0016557
Heidinger BJ, Blount JD, Boner W, Griffiths K, Metcalfe NB, Monaghan P (2012) Telomere length in early life predicts lifespan. Proc Natl Acad Sci USA 109:1743–1748. doi:10.1073/pnas.1113306109
Herczeg G, Gonda A, Merilä J (2010) Rensch’s rule inverted—female-driven gigantism in nine-spined stickleback Pungitius pungitius. J Anim Ecol 79:581–588. doi:10.1111/j.1365-2656.2010.01665.x
Herczeg G, Gonda A, Balázs G, Noreikiene K, Merilä J (2015) Experimental evidence for sex-specific plasticity in adult brain. Front Zool. doi:10.1186/s12983-015-0130-0
Horn T, Robertson BC, Will M, Eason DK, Elliott GP, Gemmell NJ (2011) Inheritance of telomere length in a bird. PLoS One 6:e17199. doi:10.1371/journal.pone.0017199
Houle D (1992) Comparing evolvability and variability of quantitative traits. Genetics 130:195–204
Kappei D, Londoño-Vallejo JA (2008) Telomere length inheritance and aging. Mech Ageing Dev 129:17–26. doi:10.1016/j.mad.2007.10.009
Kirkwood TBL (1977) Evolution of ageing. Nature 270:301–304. doi:10.1038/270301a0
Kirkwood TBL, Rose MR (1991) Evolution of senescence: late survival sacrificed for reproduction. Philos Trans R Soc B Biol Sci 332:15–24. doi:10.1098/rstb.1991.0028
Klapper W, Heidorn K, Kühne K, Parwaresch R, Krupp G (1998) Telomerase activity in “immortal” fish. FEBS Lett 434:409–412. doi:10.1016/S0014-5793(98)01020-5
Kuparinen A, Cano JM, Loehr J, Herczeg G, Gonda A, Merilä J (2011) Fish age at maturation is influenced by temperature independently of growth. Oecologia 167:435–443. doi:10.1007/s00442-011-1989-x
Kyo S, Takakura M, Kanaya T, Zhuo W, Fujimoto K, Nishio Y, Orimo A, Inoue M (1999) Estrogen activates telomerase. Cancer Res 59:5917–5921
Lee W-S, Monaghan P, Metcalfe NB (2013) Experimental demonstration of the growth rate-lifespan trade-off. Proc R Soc B 280:20122370. doi:10.1098/rspb.2012.2370
Lund TC, Glass TJ, Tolar J, Blazar BR (2009) Expression of telomerase and telomere length are unaffected by either age or limb regeneration in Daniorerio. PLoS One. doi:10.1371/journal.pone.0007688
Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Press, Sunderland, MA
Merilä J, Sheldon BC (1999) Genetic architecture of fitness and nonfitness traits: empirical patterns and development of ideas. Heredity 83:103–109. doi:10.1046/j.1365-2540.1999.00585.x
Mizutani Y, Tomita N, Niizuma Y, Yoda K (2013) Environmental perturbations influence telomere dynamics in long-lived birds in their natural habitat. Biol Lett 9:20130511. doi:10.1098/rsbl.2013.0511
Monaghan P (2010) Telomeres and life histories: the long and the short of it. Ann N Y Acad Sci 1206:130–142. doi:10.1111/j.1749-6632.2010.05705.x
Monaghan P, Haussmann MF (2006) Do telomere dynamics link lifestyle and lifespan? Trends Ecol Evol 21:47–53. doi:10.1016/j.tree.2005.11.007
Nussey DH, 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 Ecol Evol 5:299–310. doi:10.1111/2041-210X.12161
Ocalewicz K, Woznicki P, Furgala-Selezniow G, Jankun M (2011) Chromosomal location of Ag/CMA3-NORs, 5S rDNA and telomeric repeats in two stickleback species. Ital J Zool 78:12–19. doi:10.1080/11250003.2010.532160
Olsson M, Pauliny A, Wapstra E, Uller T, Schwartz T, Blomqvist D (2011) Sex differences in sand lizard telomere inheritance: paternal epigenetic effects increases telomere heritability and offspring survival. PLoS One 6:e17473. doi:10.1371/journal.pone.0017473
Park PJ, Chase I, Bell MA (2012) Phenotypic plasticity of the threespine stickleback Gasterosteus aculeatus telencephalon in response to experience in captivity. Curr Zool 58:189–210. doi:10.1093/czoolo/58.1.189
Peterson DR, Mok HOL, Au DWT (2015) Modulation of telomerase activity in fish muscle by biological and environmental factors. Comp Biochem Physiol Part C Toxicol Pharmacol 178:51–59. doi:10.1016/j.cbpc.2015.09.004
Plot V, Criscuolo F, Zahn S, Georges J-Y (2012) Telomeres, age and reproduction in a long-lived reptile. PLoS One 7:e40855. doi:10.1371/journal.pone.0040855
Price T, Schluter D (1991) On the low heritability of life-history traits. Evolution 45:853–861. doi:10.2307/2409693
Ramakers C, Ruijter JM, Deprez RHL, Moorman AFM (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339:62–66
Razmara A, Duckles SP, Krause DN, Procaccio V (2007) Estrogen suppresses brain mitochondrial oxidative stress in female and male rats. Brain Res 1176:71–81. doi:10.1016/j.brainres.2007.08.036
Reichert S, Rojas ER, Zahn S, Robin JP, Criscuolo F, Massemin S (2015) Maternal telomere length inheritance in the king penguin. Heredity 114:10–16. doi:10.1038/hdy.2014.60
Rice WR (1984) Sex chromosomes and the evolution of sexual dimorphism. Evolution 38:735–742. doi:10.2307/2408385
Roff DA (1993) Evolution of life histories: theory and analysis. Springer, New York
Rohlf FJ (2002) tpsDIG, digitize landmarks and outlines. Department of Ecology and Evolution State University of New York, Stony Brook
Rollings N, Miller E, Olsson M (2014) Telomeric attrition with age and temperature in Eastern mosquitofish (Gambusiaholbrooki). Naturwissenschaften 101:241–244. doi:10.1007/s00114-014-1142-x
Schultner J, Kitaysky AS, Gabrielsen GW, Hatch SA, Bech C (2013) Differential reproductive responses to stress reveal the role of life-history strategies within a species. Proc R Soc B Biol Sci 280:20132090. doi:10.1098/rspb.2013.2090
Sekoguchi S, Nakajima T, Moriguchi M, Jo M, Nishikawa T, Katagishi T, Kimura H, Minami M, Itoh Y, Kagawa K, Tani Y, Okanoue T (2007) Role of cell-cycle turnover and oxidative stress in telomere shortening and cellular senescence in patients with chronic hepatitis C. J Gastroenterol Hepatol 22:182–190. doi:10.1111/j.1440-1746.2006.04454.x
Shikano T, Merilä J (2011) Body size and the number of vertebrae in the nine-spined stickleback (Pungitius pungitius). Biol J Linn Soc 104:378–385. doi:10.1111/j.1095-8312.2011.01731.x
Shimada Y, Shikano T, Kuparinen A, Gonda A, Leinonen T, Merilä J (2011) Quantitative genetics of body size and timing of maturation in two nine-spined stickleback (Pungitius pungitius) populations. PLoS One 6:e28859. doi:10.1371/journal.pone.0028859
Slatkin M (1984) Ecological causes of sexual dimorphism. Evolution 38:622–630. doi:10.2307/2408711
Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3—new capabilities and interfaces. Nucleic Acids Res 40:e115. doi:10.1093/nar/gks596
Uusi-Heikkilä S, Kuparinen A, Wolter C, Meinelt T, Arlinghaus R (2011) Paternal body size affects reproductive success in laboratory-held zebrafish (Daniorerio). Environ Biol Fishes 93:461–474. doi:10.1007/s10641-011-9937-5
Vihko R, Apter D (1984) Endocrine characteristics of adolescent menstrual cycles: impact of early menarche. J Steroid Biochem 20:231–236. doi:10.1016/0022-4731(84)90209-7
Voillemot M, Hine K, Zahn S, Criscuolo F, Gustafsson L, Doligez B, Bize P (2012) Effects of brood size manipulation and common origin on phenotype and telomere length in nestling collared flycatchers. BMC Ecol 12:17. doi:10.1186/1472-6785-12-17
von Bertalanffy L (1938) A quantitative theory of organic growth (inquiries on growth laws. II). Hum Biol 10:181–213
von Zglinicki T (2002) Oxidative stress shortens telomeres. Trends Biochem Sci 27:339–344. doi:10.1016/S0968-0004(02)02110-2
Wang Y, Salmon AB, Harshman LG (2001) A cost of reproduction: oxidative stress susceptibility is associated with increased egg production in Drosophila melanogaster. Exp Gerontol 36:1349–1359. doi:10.1016/S0531-5565(01)00095-X
Acknowledgement
We would like to thank all people who helped with sampling and rearing fish, especially José M.Cano and John Loehr, Gábor Herczeg and Abigel Gonda. Sara Rezaei is thanked for her help with DNA extractions. Paolo Momigliano for linguistic corrections to an earlier version of this manuscript and Zitong Li for useful comments. This study was supported by the Academy of Finland (Grants 129662, 134728 and 218343 to JM; Grants 265671 and 303685 to AK), Natural Sciences and Engineering Research Council of Canada (Discovery Grant to AK), Finnish Cultural foundation (KN) and Nordenskiöld samfundet (KN).
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KN and JM conceived the idea, KN and AK designed the experiment, collected the data and performed statistical analyses, KN and JM wrote the manuscript, AK provided editorial advice.
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Communicated by Joel Trexler.
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Noreikiene, K., Kuparinen, A. & Merilä, J. Age at maturation has sex- and temperature-specific effects on telomere length in a fish. Oecologia 184, 767–777 (2017). https://doi.org/10.1007/s00442-017-3913-5
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DOI: https://doi.org/10.1007/s00442-017-3913-5