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...

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Published in:Proceedings of the Royal Society B: Biological Sciences
Main Authors: Prokkola, Jenni M., Åsheim, Eirik R., Morozov, Sergey, Bangura, Paul, Erkinaro, Jaakko, Ruokolainen, Annukka, Primmer, Craig R., Aykanat, Tutku
Other Authors: 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
Language:English
Published: ROYAL BELGIAN SOC EAR, NOSE, THROAT, HEAD & NECK SURGERY 2022
Subjects:
Online Access:http://hdl.handle.net/10138/340587
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spelling 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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