Genetic coupling of life-history and aerobic performance in Atlantic salmon
A better understanding of the genetic and phenotypic architecture underlying life-history variation is a longstanding aim in biology. Theories suggest energy metabolism determines life-history variation by modulating resource acquisition and allocation trade-offs, but the genetic underpinnings of th...
Published in: | Proceedings of the Royal Society B: Biological Sciences |
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Language: | English |
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ROYAL BELGIAN SOC EAR, NOSE, THROAT, HEAD & NECK SURGERY
2022
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Online Access: | http://hdl.handle.net/10138/340587 |
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ftunivhelsihelda:oai:helda.helsinki.fi:10138/340587 2024-01-07T09:42:14+01:00 Genetic coupling of life-history and aerobic performance in Atlantic salmon Prokkola, Jenni M. Åsheim, Eirik R. Morozov, Sergey Bangura, Paul Erkinaro, Jaakko Ruokolainen, Annukka Primmer, Craig R. Aykanat, Tutku Organismal and Evolutionary Biology Research Programme Ecological Genetics Research Unit Evolution, Conservation, and Genomics Institute of Biotechnology Biosciences Helsinki Institute of Sustainability Science (HELSUS) 2022-02-17T14:23:02Z 10 application/pdf http://hdl.handle.net/10138/340587 eng eng ROYAL BELGIAN SOC EAR, NOSE, THROAT, HEAD & NECK SURGERY 10.1098/rspb.2021.2500 The study was funded by Academy of Finland (T. Aykanat: 325964, 1328860, C. R. Primmer: 314254 and 314255, 327255), the European Research Council under the European Union's Horizon 2020 research and innovation programme (grant no. 742312), and the University of Helsinki. Prokkola , J M , Åsheim , E R , Morozov , S , Bangura , P , Erkinaro , J , Ruokolainen , A , Primmer , C R & Aykanat , T 2022 , ' Genetic coupling of life-history and aerobic performance in Atlantic salmon ' , Proceedings of the Royal Society B. Biological Sciences , vol. 289 , no. 1967 , 20212500 . https://doi.org/10.1098/rspb.2021.2500 ORCID: /0000-0002-8171-9732/work/108466730 ORCID: /0000-0002-3687-8435/work/108466857 ORCID: /0000-0003-2987-4417/work/108467090 e03abf07-cc09-4756-b10e-8a1498daed13 http://hdl.handle.net/10138/340587 000746806400017 cc_by openAccess info:eu-repo/semantics/openAccess age-at-maturity energetics metabolic rate life-history evolution STANDARD METABOLIC-RATE INDIVIDUAL VARIATION FOOD-DEPRIVATION MODEL SELECTION BODY-SIZE SEA-AGE GROWTH POPULATION EVOLUTION MATURITY 1181 Ecology evolutionary biology Article publishedVersion 2022 ftunivhelsihelda 2023-12-14T00:04:34Z A better understanding of the genetic and phenotypic architecture underlying life-history variation is a longstanding aim in biology. Theories suggest energy metabolism determines life-history variation by modulating resource acquisition and allocation trade-offs, but the genetic underpinnings of the relationship and its dependence on ecological conditions have rarely been demonstrated. The strong genetic determination of age-at-maturity by two unlinked genomic regions (vgll3 and six6) makes Atlantic salmon (Salmo salar) an ideal model to address these questions. Using more than 250 juveniles in common garden conditions, we quantified the covariation between metabolic phenotypes-standard and maximum metabolic rates (SMR and MMR), and aerobic scope (AS)-and the life-history genomic regions, and tested if food availability modulates the relationships. We found that the early maturation genotype in vgll3 was associated with higher MMR and consequently AS. Additionally, MMR exhibited physiological epistasis; it was decreased when late maturation genotypes co-occurred in both genomic regions. Contrary to our expectation, the life-history genotypes had no effects on SMR. Furthermore, food availability had no effect on the genetic covariation, suggesting a lack of genotype-by-environment interactions. Our results provide insights on the key organismal processes that link energy use at the juvenile stage to age-at-maturity, indicating potential mechanisms by which metabolism and life-history can coevolve. Peer reviewed Article in Journal/Newspaper Atlantic salmon Salmo salar HELDA – University of Helsinki Open Repository Proceedings of the Royal Society B: Biological Sciences 289 1967 |
institution |
Open Polar |
collection |
HELDA – University of Helsinki Open Repository |
op_collection_id |
ftunivhelsihelda |
language |
English |
topic |
age-at-maturity energetics metabolic rate life-history evolution STANDARD METABOLIC-RATE INDIVIDUAL VARIATION FOOD-DEPRIVATION MODEL SELECTION BODY-SIZE SEA-AGE GROWTH POPULATION EVOLUTION MATURITY 1181 Ecology evolutionary biology |
spellingShingle |
age-at-maturity energetics metabolic rate life-history evolution STANDARD METABOLIC-RATE INDIVIDUAL VARIATION FOOD-DEPRIVATION MODEL SELECTION BODY-SIZE SEA-AGE GROWTH POPULATION EVOLUTION MATURITY 1181 Ecology evolutionary biology Prokkola, Jenni M. Åsheim, Eirik R. Morozov, Sergey Bangura, Paul Erkinaro, Jaakko Ruokolainen, Annukka Primmer, Craig R. Aykanat, Tutku Genetic coupling of life-history and aerobic performance in Atlantic salmon |
topic_facet |
age-at-maturity energetics metabolic rate life-history evolution STANDARD METABOLIC-RATE INDIVIDUAL VARIATION FOOD-DEPRIVATION MODEL SELECTION BODY-SIZE SEA-AGE GROWTH POPULATION EVOLUTION MATURITY 1181 Ecology evolutionary biology |
description |
A better understanding of the genetic and phenotypic architecture underlying life-history variation is a longstanding aim in biology. Theories suggest energy metabolism determines life-history variation by modulating resource acquisition and allocation trade-offs, but the genetic underpinnings of the relationship and its dependence on ecological conditions have rarely been demonstrated. The strong genetic determination of age-at-maturity by two unlinked genomic regions (vgll3 and six6) makes Atlantic salmon (Salmo salar) an ideal model to address these questions. Using more than 250 juveniles in common garden conditions, we quantified the covariation between metabolic phenotypes-standard and maximum metabolic rates (SMR and MMR), and aerobic scope (AS)-and the life-history genomic regions, and tested if food availability modulates the relationships. We found that the early maturation genotype in vgll3 was associated with higher MMR and consequently AS. Additionally, MMR exhibited physiological epistasis; it was decreased when late maturation genotypes co-occurred in both genomic regions. Contrary to our expectation, the life-history genotypes had no effects on SMR. Furthermore, food availability had no effect on the genetic covariation, suggesting a lack of genotype-by-environment interactions. Our results provide insights on the key organismal processes that link energy use at the juvenile stage to age-at-maturity, indicating potential mechanisms by which metabolism and life-history can coevolve. Peer reviewed |
author2 |
Organismal and Evolutionary Biology Research Programme Ecological Genetics Research Unit Evolution, Conservation, and Genomics Institute of Biotechnology Biosciences Helsinki Institute of Sustainability Science (HELSUS) |
format |
Article in Journal/Newspaper |
author |
Prokkola, Jenni M. Åsheim, Eirik R. Morozov, Sergey Bangura, Paul Erkinaro, Jaakko Ruokolainen, Annukka Primmer, Craig R. Aykanat, Tutku |
author_facet |
Prokkola, Jenni M. Åsheim, Eirik R. Morozov, Sergey Bangura, Paul Erkinaro, Jaakko Ruokolainen, Annukka Primmer, Craig R. Aykanat, Tutku |
author_sort |
Prokkola, Jenni M. |
title |
Genetic coupling of life-history and aerobic performance in Atlantic salmon |
title_short |
Genetic coupling of life-history and aerobic performance in Atlantic salmon |
title_full |
Genetic coupling of life-history and aerobic performance in Atlantic salmon |
title_fullStr |
Genetic coupling of life-history and aerobic performance in Atlantic salmon |
title_full_unstemmed |
Genetic coupling of life-history and aerobic performance in Atlantic salmon |
title_sort |
genetic coupling of life-history and aerobic performance in atlantic salmon |
publisher |
ROYAL BELGIAN SOC EAR, NOSE, THROAT, HEAD & NECK SURGERY |
publishDate |
2022 |
url |
http://hdl.handle.net/10138/340587 |
genre |
Atlantic salmon Salmo salar |
genre_facet |
Atlantic salmon Salmo salar |
op_relation |
10.1098/rspb.2021.2500 The study was funded by Academy of Finland (T. Aykanat: 325964, 1328860, C. R. Primmer: 314254 and 314255, 327255), the European Research Council under the European Union's Horizon 2020 research and innovation programme (grant no. 742312), and the University of Helsinki. Prokkola , J M , Åsheim , E R , Morozov , S , Bangura , P , Erkinaro , J , Ruokolainen , A , Primmer , C R & Aykanat , T 2022 , ' Genetic coupling of life-history and aerobic performance in Atlantic salmon ' , Proceedings of the Royal Society B. Biological Sciences , vol. 289 , no. 1967 , 20212500 . https://doi.org/10.1098/rspb.2021.2500 ORCID: /0000-0002-8171-9732/work/108466730 ORCID: /0000-0002-3687-8435/work/108466857 ORCID: /0000-0003-2987-4417/work/108467090 e03abf07-cc09-4756-b10e-8a1498daed13 http://hdl.handle.net/10138/340587 000746806400017 |
op_rights |
cc_by openAccess info:eu-repo/semantics/openAccess |
container_title |
Proceedings of the Royal Society B: Biological Sciences |
container_volume |
289 |
container_issue |
1967 |
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1787423163275018240 |