Variable parallelism in the genomic basis of age at maturity across spatial scales in Atlantic Salmon

Abstract Complex traits often exhibit complex underlying genetic architectures resulting from a combination of evolution from standing variation, hard and soft sweeps, and alleles of varying effect size. Increasingly, studies implicate both large‐effect loci and polygenic patterns underpinning adapt...

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Published in:Ecology and Evolution
Main Authors: Tony Kess, Sarah J. Lehnert, Paul Bentzen, Steven Duffy, Amber Messmer, J. Brian Dempson, Jason Newport, Christopher Whidden, Martha J. Robertson, Gerald Chaput, Cindy Breau, Julien April, Carole‐Anne Gillis, Matthew Kent, Cameron M. Nugent, Ian R. Bradbury
Format: Article in Journal/Newspaper
Language:English
Published: Wiley 2024
Subjects:
Online Access:https://doi.org/10.1002/ece3.11068
https://doaj.org/article/50d593be9e0a45f99fc2b759a20bb5a4
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spelling ftdoajarticles:oai:doaj.org/article:50d593be9e0a45f99fc2b759a20bb5a4 2024-09-09T19:30:10+00:00 Variable parallelism in the genomic basis of age at maturity across spatial scales in Atlantic Salmon Tony Kess Sarah J. Lehnert Paul Bentzen Steven Duffy Amber Messmer J. Brian Dempson Jason Newport Christopher Whidden Martha J. Robertson Gerald Chaput Cindy Breau Julien April Carole‐Anne Gillis Matthew Kent Cameron M. Nugent Ian R. Bradbury 2024-04-01T00:00:00Z https://doi.org/10.1002/ece3.11068 https://doaj.org/article/50d593be9e0a45f99fc2b759a20bb5a4 EN eng Wiley https://doi.org/10.1002/ece3.11068 https://doaj.org/toc/2045-7758 2045-7758 doi:10.1002/ece3.11068 https://doaj.org/article/50d593be9e0a45f99fc2b759a20bb5a4 Ecology and Evolution, Vol 14, Iss 4, Pp n/a-n/a (2024) Atlantic Salmon genetic architecture genomics life history Ecology QH540-549.5 article 2024 ftdoajarticles https://doi.org/10.1002/ece3.11068 2024-08-05T17:49:19Z Abstract Complex traits often exhibit complex underlying genetic architectures resulting from a combination of evolution from standing variation, hard and soft sweeps, and alleles of varying effect size. Increasingly, studies implicate both large‐effect loci and polygenic patterns underpinning adaptation, but the extent that common genetic architectures are utilized during repeated adaptation is not well understood. Sea age or age at maturation represents a significant life history trait in Atlantic Salmon (Salmo salar), the genetic basis of which has been studied extensively in European Atlantic populations, with repeated identification of large‐effect loci. However, the genetic basis of sea age within North American Atlantic Salmon populations remains unclear, as does the potential for a parallel trans‐Atlantic genomic basis to sea age. Here, we used a large single‐nucleotide polymorphism (SNP) array and low‐coverage whole‐genome resequencing to explore the genomic basis of sea age variation in North American Atlantic Salmon. We found significant associations at the gene and SNP level with a large‐effect locus (vgll3) previously identified in European populations, indicating genetic parallelism, but found that this pattern varied based on both sex and geographic region. We also identified nonrepeated sets of highly predictive loci associated with sea age among populations and sexes within North America, indicating polygenicity and low rates of genomic parallelism. Despite low genome‐wide parallelism, we uncovered a set of conserved molecular pathways associated with sea age that were consistently enriched among comparisons, including calcium signaling, MapK signaling, focal adhesion, and phosphatidylinositol signaling. Together, our results indicate parallelism of the molecular basis of sea age in North American Atlantic Salmon across large‐effect genes and molecular pathways despite population‐specific patterns of polygenicity. These findings reveal roles for both contingency and repeated adaptation at the ... Article in Journal/Newspaper Atlantic salmon Salmo salar Directory of Open Access Journals: DOAJ Articles Ecology and Evolution 14 4
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic Atlantic Salmon
genetic architecture
genomics
life history
Ecology
QH540-549.5
spellingShingle Atlantic Salmon
genetic architecture
genomics
life history
Ecology
QH540-549.5
Tony Kess
Sarah J. Lehnert
Paul Bentzen
Steven Duffy
Amber Messmer
J. Brian Dempson
Jason Newport
Christopher Whidden
Martha J. Robertson
Gerald Chaput
Cindy Breau
Julien April
Carole‐Anne Gillis
Matthew Kent
Cameron M. Nugent
Ian R. Bradbury
Variable parallelism in the genomic basis of age at maturity across spatial scales in Atlantic Salmon
topic_facet Atlantic Salmon
genetic architecture
genomics
life history
Ecology
QH540-549.5
description Abstract Complex traits often exhibit complex underlying genetic architectures resulting from a combination of evolution from standing variation, hard and soft sweeps, and alleles of varying effect size. Increasingly, studies implicate both large‐effect loci and polygenic patterns underpinning adaptation, but the extent that common genetic architectures are utilized during repeated adaptation is not well understood. Sea age or age at maturation represents a significant life history trait in Atlantic Salmon (Salmo salar), the genetic basis of which has been studied extensively in European Atlantic populations, with repeated identification of large‐effect loci. However, the genetic basis of sea age within North American Atlantic Salmon populations remains unclear, as does the potential for a parallel trans‐Atlantic genomic basis to sea age. Here, we used a large single‐nucleotide polymorphism (SNP) array and low‐coverage whole‐genome resequencing to explore the genomic basis of sea age variation in North American Atlantic Salmon. We found significant associations at the gene and SNP level with a large‐effect locus (vgll3) previously identified in European populations, indicating genetic parallelism, but found that this pattern varied based on both sex and geographic region. We also identified nonrepeated sets of highly predictive loci associated with sea age among populations and sexes within North America, indicating polygenicity and low rates of genomic parallelism. Despite low genome‐wide parallelism, we uncovered a set of conserved molecular pathways associated with sea age that were consistently enriched among comparisons, including calcium signaling, MapK signaling, focal adhesion, and phosphatidylinositol signaling. Together, our results indicate parallelism of the molecular basis of sea age in North American Atlantic Salmon across large‐effect genes and molecular pathways despite population‐specific patterns of polygenicity. These findings reveal roles for both contingency and repeated adaptation at the ...
format Article in Journal/Newspaper
author Tony Kess
Sarah J. Lehnert
Paul Bentzen
Steven Duffy
Amber Messmer
J. Brian Dempson
Jason Newport
Christopher Whidden
Martha J. Robertson
Gerald Chaput
Cindy Breau
Julien April
Carole‐Anne Gillis
Matthew Kent
Cameron M. Nugent
Ian R. Bradbury
author_facet Tony Kess
Sarah J. Lehnert
Paul Bentzen
Steven Duffy
Amber Messmer
J. Brian Dempson
Jason Newport
Christopher Whidden
Martha J. Robertson
Gerald Chaput
Cindy Breau
Julien April
Carole‐Anne Gillis
Matthew Kent
Cameron M. Nugent
Ian R. Bradbury
author_sort Tony Kess
title Variable parallelism in the genomic basis of age at maturity across spatial scales in Atlantic Salmon
title_short Variable parallelism in the genomic basis of age at maturity across spatial scales in Atlantic Salmon
title_full Variable parallelism in the genomic basis of age at maturity across spatial scales in Atlantic Salmon
title_fullStr Variable parallelism in the genomic basis of age at maturity across spatial scales in Atlantic Salmon
title_full_unstemmed Variable parallelism in the genomic basis of age at maturity across spatial scales in Atlantic Salmon
title_sort variable parallelism in the genomic basis of age at maturity across spatial scales in atlantic salmon
publisher Wiley
publishDate 2024
url https://doi.org/10.1002/ece3.11068
https://doaj.org/article/50d593be9e0a45f99fc2b759a20bb5a4
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
op_source Ecology and Evolution, Vol 14, Iss 4, Pp n/a-n/a (2024)
op_relation https://doi.org/10.1002/ece3.11068
https://doaj.org/toc/2045-7758
2045-7758
doi:10.1002/ece3.11068
https://doaj.org/article/50d593be9e0a45f99fc2b759a20bb5a4
op_doi https://doi.org/10.1002/ece3.11068
container_title Ecology and Evolution
container_volume 14
container_issue 4
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