Telomere Elongation During Early Development is Independent of Environmental Temperatures in Atlantic Salmon

Overview

Journal J Exp Biol

Specialty Biology

Date 2018 Apr 12

PMID 29636409

Citations 14

Authors

Darryl McLennan

John D Armstrong

David C Stewart

Simon McKelvey

Winnie Boner

Pat Monaghan

Neil B Metcalfe

Affiliations

Soon will be listed here.

Abstract

There is increasing evidence from endothermic vertebrates that telomeres, which cap the ends of chromosomes and play an important role in chromosome protection, decline in length during postnatal life and are a useful indicator of physiological state and expected lifespan. However, much less is currently known about telomere dynamics in ectothermic vertebrates, which are likely to differ from that of endotherms, at least in part due to the sensitivity of ectotherm physiology to environmental temperature. We report here on an experiment in which Atlantic salmon () were reared through the embryonic and larval stages of development, and under differing temperatures, in order to examine the effects of environmental temperature during early life on telomere dynamics, oxidative DNA damage and cellular proliferation. Telomere length significantly increased between the embryonic and larval stages of development. Contrary to our expectations, variation in telomere length at the end of the larval stage was unrelated to either cell proliferation rate or the relative level of oxidative DNA damage, and did not vary between the temperature treatments. This study suggests that salmon are able to restore the length of their telomeres during early development, which may possibly help to buffer potentially harmful environmental effects experienced in early life.

Citing Articles

Sex and early-life conditions shape telomere dynamics in an ectotherm.

Hansson A, Wapstra E, While G, Olsson M J Exp Biol. 2024; 227(3).

PMID: 38230426 PMC: 10912812. DOI: 10.1242/jeb.246512.

Thermal Preconditioning Alters the Stability of Hump-Snout Whitefish () and Its Hybrid Form, Showing Potential for Aquaculture.

Sapozhnikova Y, Koroleva A, Yakhnenko V, Volkova A, Avezova T, Glyzina O Biology (Basel). 2023; 12(10).

PMID: 37887058 PMC: 10603914. DOI: 10.3390/biology12101348.

Does pre-spawning catch and release angling affect offspring telomere dynamics in Atlantic salmon?.

Duncan E, Papatheodoulou M, Metcalfe N, McLennan D Conserv Physiol. 2023; 11(1):coad018.

PMID: 37113976 PMC: 10129346. DOI: 10.1093/conphys/coad018.

Longitudinal telomere dynamics within natural lifespans of a wild bird.

Pepke M, Kvalnes T, Wright J, Araya-Ajoy Y, Ranke P, Boner W Sci Rep. 2023; 13(1):4272.

PMID: 36922555 PMC: 10017829. DOI: 10.1038/s41598-023-31435-9.

Lizards from warm and declining populations are born with extremely short telomeres.

Dupoue A, Blaimont P, Angelier F, Ribout C, Rozen-Rechels D, Richard M Proc Natl Acad Sci U S A. 2022; 119(33):e2201371119.

PMID: 35939680 PMC: 9388115. DOI: 10.1073/pnas.2201371119.

References

Boonekamp J, Mulder G, Salomons H, Dijkstra C, Verhulst S . Nestling telomere shortening, but not telomere length, reflects developmental stress and predicts survival in wild birds. Proc Biol Sci. 2014; 281(1785):20133287. PMC: 4024283. DOI: 10.1098/rspb.2013.3287. View

Gomez-Mestre I, Kulkarni S, Buchholz D . Mechanisms and consequences of developmental acceleration in tadpoles responding to pond drying. PLoS One. 2013; 8(12):e84266. PMC: 3865288. DOI: 10.1371/journal.pone.0084266. View

Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J . qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 2007; 8(2):R19. PMC: 1852402. DOI: 10.1186/gb-2007-8-2-r19. View

Auer S, Arendt J, Chandramouli R, Reznick D . Juvenile compensatory growth has negative consequences for reproduction in Trinidadian guppies (Poecilia reticulata). Ecol Lett. 2010; 13(8):998-1007. DOI: 10.1111/j.1461-0248.2010.01491.x. View

Johnston I, Manthri S, Alderson R, Smart A, Campbell P, Nickell D . Freshwater environment affects growth rate and muscle fibre recruitment in seawater stages of Atlantic salmon (Salmo salar L.). J Exp Biol. 2003; 206(Pt 8):1337-51. DOI: 10.1242/jeb.00262. View

Haussmann M, Winkler D, OReilly K, Huntington C, Nisbet I, Vleck C . Telomeres shorten more slowly in long-lived birds and mammals than in short-lived ones. Proc Biol Sci. 2003; 270(1522):1387-92. PMC: 1691385. DOI: 10.1098/rspb.2003.2385. View

Ohlsson T, Smith H, Raberg L, Hasselquist D . Pheasant sexual ornaments reflect nutritional conditions during early growth. Proc Biol Sci. 2002; 269(1486):21-7. PMC: 1690866. DOI: 10.1098/rspb.2001.1848. View

Arendt J . Ecological correlates of body size in relation to cell size and cell number: patterns in flies, fish, fruits and foliage. Biol Rev Camb Philos Soc. 2007; 82(2):241-56. DOI: 10.1111/j.1469-185X.2007.00013.x. View

Liu L, Bailey S, Okuka M, Munoz P, Li C, Zhou L . Telomere lengthening early in development. Nat Cell Biol. 2007; 9(12):1436-41. DOI: 10.1038/ncb1664. View

10.

Nettle D, Monaghan P, Gillespie R, Brilot B, Bedford T, Bateson M . An experimental demonstration that early-life competitive disadvantage accelerates telomere loss. Proc Biol Sci. 2014; 282(1798):20141610. PMC: 4262165. DOI: 10.1098/rspb.2014.1610. View

11.

Dupoue A, Rutschmann A, Le Galliard J, Clobert J, Angelier F, Marciau C . Shorter telomeres precede population extinction in wild lizards. Sci Rep. 2017; 7(1):16976. PMC: 5717062. DOI: 10.1038/s41598-017-17323-z. View

12.

Salmon P, Nilsson J, Watson H, Bensch S, Isaksson C . Selective disappearance of great tits with short telomeres in urban areas. Proc Biol Sci. 2017; 284(1862). PMC: 5597837. DOI: 10.1098/rspb.2017.1349. View

13.

Henriques C, Ferreira M . Consequences of telomere shortening during lifespan. Curr Opin Cell Biol. 2012; 24(6):804-8. DOI: 10.1016/j.ceb.2012.09.007. View

14.

Yip B, Mok H, Peterson D, Wan M, Taniguchi Y, Ge W . Sex-dependent telomere shortening, telomerase activity and oxidative damage in marine medaka Oryzias melastigma during aging. Mar Pollut Bull. 2017; 124(2):701-709. DOI: 10.1016/j.marpolbul.2017.01.021. View

15.

Ortego L, Hawkins W, Walker W, Krol R, Benson W . Detection of proliferating cell nuclear antigen in tissues of three small fish species. Biotech Histochem. 1994; 69(6):317-23. DOI: 10.3109/10520299409106312. View

16.

Boonekamp J, Bauch C, Mulder E, Verhulst S . Does oxidative stress shorten telomeres?. Biol Lett. 2017; 13(5). PMC: 5454244. DOI: 10.1098/rsbl.2017.0164. View

17.

Olsson M, Wapstra E, Friesen C . Ectothermic telomeres: it's time they came in from the cold. Philos Trans R Soc Lond B Biol Sci. 2018; 373(1741). PMC: 5784069. DOI: 10.1098/rstb.2016.0449. View

18.

Cram D, Monaghan P, Gillespie R, Clutton-Brock T . Effects of early-life competition and maternal nutrition on telomere lengths in wild meerkats. Proc Biol Sci. 2017; 284(1861). PMC: 5577495. DOI: 10.1098/rspb.2017.1383. View

19.

Monaghan P . Telomeres and life histories: the long and the short of it. Ann N Y Acad Sci. 2010; 1206:130-42. DOI: 10.1111/j.1749-6632.2010.05705.x. View

20.

Ridout K, Levandowski M, Ridout S, Gantz L, Goonan K, Palermo D . Early life adversity and telomere length: a meta-analysis. Mol Psychiatry. 2017; 23(4):858-871. PMC: 5608639. DOI: 10.1038/mp.2017.26. View