Co-inheritance of sea age at maturity and iteroparity in the Atlantic salmon vgll3 genomic region

Co-inheritance in life-history traits may result in unpredictable evolutionary trajectories if not accounted for in life-history models. Iteroparity (the reproductive strategy of reproducing more than once) in Atlantic salmon (Salmo salar) is a fitness trait with substantial variation within and amo...

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Published in:Journal of Evolutionary Biology
Main Authors: Aykanat, Tutku, Ozerov, Mikhail, Vähä, Juha-Pekka, Orell, Panu, Niemelä, Eero, Erkinaro, Jaakko, Primmer, Craig R.
Other Authors: Evolution, Conservation, and Genomics, Genetics, Organismal and Evolutionary Biology Research Programme, Helsinki Institute of Sustainability Science (HELSUS), Institute of Biotechnology
Format: Article in Journal/Newspaper
Language:English
Published: Wiley 2021
Subjects:
Online Access:http://hdl.handle.net/10138/324094
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author Aykanat, Tutku
Ozerov, Mikhail
Vähä, Juha-Pekka
Orell, Panu
Niemelä, Eero
Erkinaro, Jaakko
Primmer, Craig R.
author2 Evolution, Conservation, and Genomics
Genetics
Organismal and Evolutionary Biology Research Programme
Helsinki Institute of Sustainability Science (HELSUS)
Institute of Biotechnology
author_facet Aykanat, Tutku
Ozerov, Mikhail
Vähä, Juha-Pekka
Orell, Panu
Niemelä, Eero
Erkinaro, Jaakko
Primmer, Craig R.
author_sort Aykanat, Tutku
collection HELDA – University of Helsinki Open Repository
container_issue 4
container_start_page 343
container_title Journal of Evolutionary Biology
container_volume 32
description Co-inheritance in life-history traits may result in unpredictable evolutionary trajectories if not accounted for in life-history models. Iteroparity (the reproductive strategy of reproducing more than once) in Atlantic salmon (Salmo salar) is a fitness trait with substantial variation within and among populations. In the Teno River in northern Europe, iteroparous individuals constitute an important component of many populations and have experienced a sharp increase in abundance in the last 20 years, partly overlapping with a general decrease in age structure. The physiological basis of iteroparity bears similarities to that of age at first maturity, another life-history trait with substantial fitness effects in salmon. Sea age at maturity in Atlantic salmon is controlled by a major locus around the vgll3 gene, and we used this opportunity demonstrate that these two traits are co-inherited around this genome region. The odds ratio of survival until second reproduction was up to 2.4 (1.8-3.5 90% CI) times higher for fish with the early-maturing vgll3 genotype (EE) compared to fish with the late-maturing genotype (LL). The L allele was dominant in individuals remaining only one year at sea before maturation, but the dominance was reversed, with the E allele being dominant in individuals maturing after two or more years at sea. Post hoc analysis indicated that iteroparous fish with the EE genotype had accelerated growth prior to first reproduction compared to first-time spawners, across all age groups, whereas this effect was not detected in fish with the LL genotype. These results broaden the functional link around the vgll3 genome region and help us understand constraints in the evolution of life-history variation in salmon. Our results further highlight the need to account for genetic correlations between fitness traits when predicting demographic changes in changing environments. Peer reviewed
format Article in Journal/Newspaper
genre Atlantic salmon
North Atlantic
Salmo salar
genre_facet Atlantic salmon
North Atlantic
Salmo salar
geographic Teno
geographic_facet Teno
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language English
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op_container_end_page 355
op_relation 10.1111/jeb.13418
Maj ja Tor Nesslingin Saatio, Grant/Award Number: 201600445; Suomen Akatemia, Grant/Award Number: 284941, 286334, 302873, 307593 and 318939
Aykanat , T , Ozerov , M , Vähä , J-P , Orell , P , Niemelä , E , Erkinaro , J & Primmer , C R 2019 , ' Co-inheritance of sea age at maturity and iteroparity in the Atlantic salmon vgll3 genomic region ' , Journal of Evolutionary Biology , vol. 32 , no. 4 , pp. 343-355 . https://doi.org/10.1111/jeb.13418
ORCID: /0000-0002-3687-8435/work/57308654
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spelling ftunivhelsihelda:oai:helda.helsinki.fi:10138/324094 2025-01-16T21:02:16+00:00 Co-inheritance of sea age at maturity and iteroparity in the Atlantic salmon vgll3 genomic region Aykanat, Tutku Ozerov, Mikhail Vähä, Juha-Pekka Orell, Panu Niemelä, Eero Erkinaro, Jaakko Primmer, Craig R. Evolution, Conservation, and Genomics Genetics Organismal and Evolutionary Biology Research Programme Helsinki Institute of Sustainability Science (HELSUS) Institute of Biotechnology 2021-01-07T07:57:02Z 13 application/pdf http://hdl.handle.net/10138/324094 eng eng Wiley 10.1111/jeb.13418 Maj ja Tor Nesslingin Saatio, Grant/Award Number: 201600445; Suomen Akatemia, Grant/Award Number: 284941, 286334, 302873, 307593 and 318939 Aykanat , T , Ozerov , M , Vähä , J-P , Orell , P , Niemelä , E , Erkinaro , J & Primmer , C R 2019 , ' Co-inheritance of sea age at maturity and iteroparity in the Atlantic salmon vgll3 genomic region ' , Journal of Evolutionary Biology , vol. 32 , no. 4 , pp. 343-355 . https://doi.org/10.1111/jeb.13418 ORCID: /0000-0002-3687-8435/work/57308654 2284ddd7-6b29-47b1-b8ca-5954ebd30afd http://hdl.handle.net/10138/324094 000464516900005 openAccess info:eu-repo/semantics/openAccess Atlantic salmon co-inheritance iteroparity life-history evolution sea age at first maturity LIFE-HISTORY GENETIC CORRELATIONS WILD POPULATION QUANTITATIVE GENETICS MIRAMICHI RIVER NORTH-ATLANTIC CLIMATE-CHANGE CLUTCH SIZE SELECTION PLEIOTROPY 1181 Ecology evolutionary biology Article acceptedVersion 2021 ftunivhelsihelda 2023-12-14T00:02:52Z Co-inheritance in life-history traits may result in unpredictable evolutionary trajectories if not accounted for in life-history models. Iteroparity (the reproductive strategy of reproducing more than once) in Atlantic salmon (Salmo salar) is a fitness trait with substantial variation within and among populations. In the Teno River in northern Europe, iteroparous individuals constitute an important component of many populations and have experienced a sharp increase in abundance in the last 20 years, partly overlapping with a general decrease in age structure. The physiological basis of iteroparity bears similarities to that of age at first maturity, another life-history trait with substantial fitness effects in salmon. Sea age at maturity in Atlantic salmon is controlled by a major locus around the vgll3 gene, and we used this opportunity demonstrate that these two traits are co-inherited around this genome region. The odds ratio of survival until second reproduction was up to 2.4 (1.8-3.5 90% CI) times higher for fish with the early-maturing vgll3 genotype (EE) compared to fish with the late-maturing genotype (LL). The L allele was dominant in individuals remaining only one year at sea before maturation, but the dominance was reversed, with the E allele being dominant in individuals maturing after two or more years at sea. Post hoc analysis indicated that iteroparous fish with the EE genotype had accelerated growth prior to first reproduction compared to first-time spawners, across all age groups, whereas this effect was not detected in fish with the LL genotype. These results broaden the functional link around the vgll3 genome region and help us understand constraints in the evolution of life-history variation in salmon. Our results further highlight the need to account for genetic correlations between fitness traits when predicting demographic changes in changing environments. Peer reviewed Article in Journal/Newspaper Atlantic salmon North Atlantic Salmo salar HELDA – University of Helsinki Open Repository Teno ENVELOPE(25.690,25.690,68.925,68.925) Journal of Evolutionary Biology 32 4 343 355
spellingShingle Atlantic salmon
co-inheritance
iteroparity
life-history evolution
sea age at first maturity
LIFE-HISTORY
GENETIC CORRELATIONS
WILD POPULATION
QUANTITATIVE GENETICS
MIRAMICHI RIVER
NORTH-ATLANTIC
CLIMATE-CHANGE
CLUTCH SIZE
SELECTION
PLEIOTROPY
1181 Ecology
evolutionary biology
Aykanat, Tutku
Ozerov, Mikhail
Vähä, Juha-Pekka
Orell, Panu
Niemelä, Eero
Erkinaro, Jaakko
Primmer, Craig R.
Co-inheritance of sea age at maturity and iteroparity in the Atlantic salmon vgll3 genomic region
title Co-inheritance of sea age at maturity and iteroparity in the Atlantic salmon vgll3 genomic region
title_full Co-inheritance of sea age at maturity and iteroparity in the Atlantic salmon vgll3 genomic region
title_fullStr Co-inheritance of sea age at maturity and iteroparity in the Atlantic salmon vgll3 genomic region
title_full_unstemmed Co-inheritance of sea age at maturity and iteroparity in the Atlantic salmon vgll3 genomic region
title_short Co-inheritance of sea age at maturity and iteroparity in the Atlantic salmon vgll3 genomic region
title_sort co-inheritance of sea age at maturity and iteroparity in the atlantic salmon vgll3 genomic region
topic Atlantic salmon
co-inheritance
iteroparity
life-history evolution
sea age at first maturity
LIFE-HISTORY
GENETIC CORRELATIONS
WILD POPULATION
QUANTITATIVE GENETICS
MIRAMICHI RIVER
NORTH-ATLANTIC
CLIMATE-CHANGE
CLUTCH SIZE
SELECTION
PLEIOTROPY
1181 Ecology
evolutionary biology
topic_facet Atlantic salmon
co-inheritance
iteroparity
life-history evolution
sea age at first maturity
LIFE-HISTORY
GENETIC CORRELATIONS
WILD POPULATION
QUANTITATIVE GENETICS
MIRAMICHI RIVER
NORTH-ATLANTIC
CLIMATE-CHANGE
CLUTCH SIZE
SELECTION
PLEIOTROPY
1181 Ecology
evolutionary biology
url http://hdl.handle.net/10138/324094