Shorter juvenile telomere length is associated with higher survival to spawning in migratory Atlantic salmon

The risk of mortality associated with a long-distance migration will depend on an animal's physiological state, as well as the prevailing ecological conditions. Here we assess whether juvenile telomere length, which in endotherms has been shown to be a biomarker of physiological state and expec...

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Published in:Functional Ecology
Main Authors: McLennan, Darryl, Armstrong, John D., Stewart, David C., Mckelvey, Simon, Boner, Winnie, Monaghan, Pat, Metcalfe, Neil B.
Format: Article in Journal/Newspaper
Language:English
Published: Wiley 2017
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Online Access:https://eprints.gla.ac.uk/144554/
https://eprints.gla.ac.uk/144554/7/144554.pdf
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spelling ftuglasgow:oai:eprints.gla.ac.uk:144554 2023-05-15T15:31:54+02:00 Shorter juvenile telomere length is associated with higher survival to spawning in migratory Atlantic salmon McLennan, Darryl Armstrong, John D. Stewart, David C. Mckelvey, Simon Boner, Winnie Monaghan, Pat Metcalfe, Neil B. 2017-11 text https://eprints.gla.ac.uk/144554/ https://eprints.gla.ac.uk/144554/7/144554.pdf en eng Wiley https://eprints.gla.ac.uk/144554/7/144554.pdf McLennan, D. <http://eprints.gla.ac.uk/view/author/38610.html>, Armstrong, J. D., Stewart, D. C., Mckelvey, S., Boner, W. <http://eprints.gla.ac.uk/view/author/13193.html> , Monaghan, P. <http://eprints.gla.ac.uk/view/author/10154.html> and Metcalfe, N. B. <http://eprints.gla.ac.uk/view/author/10179.html> (2017) Shorter juvenile telomere length is associated with higher survival to spawning in migratory Atlantic salmon. Functional Ecology <https://eprints.gla.ac.uk/view/journal_volume/Functional_Ecology.html>, 31(11), pp. 2070-2079. (doi:10.1111/1365-2435.12939 <https://doi.org/10.1111/1365-2435.12939>) cc_by_4 CC-BY Articles PeerReviewed 2017 ftuglasgow https://doi.org/10.1111/1365-2435.12939 2022-09-22T22:13:39Z The risk of mortality associated with a long-distance migration will depend on an animal's physiological state, as well as the prevailing ecological conditions. Here we assess whether juvenile telomere length, which in endotherms has been shown to be a biomarker of physiological state and expected lifespan, predicts whether wild Atlantic salmon Salmo salar successfully complete their marine migration. Over 1800 juvenile fish were trapped, measured, PIT-tagged and a tissue biopsy taken when migrating as juveniles down-river towards the sea. Survivors of the marine phase of the life cycle were then re-trapped and re-sampled when returning to the river to spawn as sexually mature adults, 1.5-2.5 years later. Most individuals experienced a reduction in telomere length during the marine migratory phase of their life cycle. While the relative rate of telomere loss was greater in males than females, telomere loss was unrelated to growth at sea. Contrary to expectations, salmon that had the shortest telomeres at the time of the outward migration had the greatest probability of surviving through to the return migration. This effect, independent of body size, may indicate a trade-off between investment in readiness for marine life (which favours high glucocorticoid levels, known to increase telomere attrition in other vertebrate species) and investment in telomere maintenance. Survival was also significantly influenced by the seasonal timing of outward migration, with the fish migrating downstream earliest in the spring having the highest probability of return. This study reveals that telomere length is associated with survival, although in ways that contrast with patterns seen in endotherms. This illustrates that while telomeres may be universally important for chromosome protection, the potential for telomere dynamics to predict performance may vary across taxa. Article in Journal/Newspaper Atlantic salmon Salmo salar University of Glasgow: Enlighten - Publications Functional Ecology 31 11 2070 2079
institution Open Polar
collection University of Glasgow: Enlighten - Publications
op_collection_id ftuglasgow
language English
description The risk of mortality associated with a long-distance migration will depend on an animal's physiological state, as well as the prevailing ecological conditions. Here we assess whether juvenile telomere length, which in endotherms has been shown to be a biomarker of physiological state and expected lifespan, predicts whether wild Atlantic salmon Salmo salar successfully complete their marine migration. Over 1800 juvenile fish were trapped, measured, PIT-tagged and a tissue biopsy taken when migrating as juveniles down-river towards the sea. Survivors of the marine phase of the life cycle were then re-trapped and re-sampled when returning to the river to spawn as sexually mature adults, 1.5-2.5 years later. Most individuals experienced a reduction in telomere length during the marine migratory phase of their life cycle. While the relative rate of telomere loss was greater in males than females, telomere loss was unrelated to growth at sea. Contrary to expectations, salmon that had the shortest telomeres at the time of the outward migration had the greatest probability of surviving through to the return migration. This effect, independent of body size, may indicate a trade-off between investment in readiness for marine life (which favours high glucocorticoid levels, known to increase telomere attrition in other vertebrate species) and investment in telomere maintenance. Survival was also significantly influenced by the seasonal timing of outward migration, with the fish migrating downstream earliest in the spring having the highest probability of return. This study reveals that telomere length is associated with survival, although in ways that contrast with patterns seen in endotherms. This illustrates that while telomeres may be universally important for chromosome protection, the potential for telomere dynamics to predict performance may vary across taxa.
format Article in Journal/Newspaper
author McLennan, Darryl
Armstrong, John D.
Stewart, David C.
Mckelvey, Simon
Boner, Winnie
Monaghan, Pat
Metcalfe, Neil B.
spellingShingle McLennan, Darryl
Armstrong, John D.
Stewart, David C.
Mckelvey, Simon
Boner, Winnie
Monaghan, Pat
Metcalfe, Neil B.
Shorter juvenile telomere length is associated with higher survival to spawning in migratory Atlantic salmon
author_facet McLennan, Darryl
Armstrong, John D.
Stewart, David C.
Mckelvey, Simon
Boner, Winnie
Monaghan, Pat
Metcalfe, Neil B.
author_sort McLennan, Darryl
title Shorter juvenile telomere length is associated with higher survival to spawning in migratory Atlantic salmon
title_short Shorter juvenile telomere length is associated with higher survival to spawning in migratory Atlantic salmon
title_full Shorter juvenile telomere length is associated with higher survival to spawning in migratory Atlantic salmon
title_fullStr Shorter juvenile telomere length is associated with higher survival to spawning in migratory Atlantic salmon
title_full_unstemmed Shorter juvenile telomere length is associated with higher survival to spawning in migratory Atlantic salmon
title_sort shorter juvenile telomere length is associated with higher survival to spawning in migratory atlantic salmon
publisher Wiley
publishDate 2017
url https://eprints.gla.ac.uk/144554/
https://eprints.gla.ac.uk/144554/7/144554.pdf
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
op_relation https://eprints.gla.ac.uk/144554/7/144554.pdf
McLennan, D. <http://eprints.gla.ac.uk/view/author/38610.html>, Armstrong, J. D., Stewart, D. C., Mckelvey, S., Boner, W. <http://eprints.gla.ac.uk/view/author/13193.html> , Monaghan, P. <http://eprints.gla.ac.uk/view/author/10154.html> and Metcalfe, N. B. <http://eprints.gla.ac.uk/view/author/10179.html> (2017) Shorter juvenile telomere length is associated with higher survival to spawning in migratory Atlantic salmon. Functional Ecology <https://eprints.gla.ac.uk/view/journal_volume/Functional_Ecology.html>, 31(11), pp. 2070-2079. (doi:10.1111/1365-2435.12939 <https://doi.org/10.1111/1365-2435.12939>)
op_rights cc_by_4
op_rightsnorm CC-BY
op_doi https://doi.org/10.1111/1365-2435.12939
container_title Functional Ecology
container_volume 31
container_issue 11
container_start_page 2070
op_container_end_page 2079
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