Variation in the genomic basis of parallel phenotypic and ecological divergence in benthic and pelagic morphs of Icelandic Arctic charr (Salvelinus alpinus)

Sympatric adaptive phenotypic divergence should be underlain by genomic differentiation between subpopulations. When divergence drives similar patterns of phenotypic and ecological variation within species we expect evolution to draw on common allelic variation. We investigated divergence histories...

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Published in:Molecular Ecology
Main Authors: Brachmann, Matthew K., Parsons, Kevin, Skúlason, Skúli, Gaggiotti, Oscar, Ferguson, Moira
Other Authors: University of St Andrews.School of Biology, University of St Andrews.Scottish Oceans Institute, University of St Andrews.St Andrews Bioinformatics Unit, University of St Andrews.Marine Alliance for Science & Technology Scotland
Format: Article in Journal/Newspaper
Language:English
Published: 2023
Subjects:
Online Access:https://hdl.handle.net/10023/28089
https://doi.org/10.1111/mec.16625
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author Brachmann, Matthew K.
Parsons, Kevin
Skúlason, Skúli
Gaggiotti, Oscar
Ferguson, Moira
author2 University of St Andrews.School of Biology
University of St Andrews.Scottish Oceans Institute
University of St Andrews.St Andrews Bioinformatics Unit
University of St Andrews.Marine Alliance for Science & Technology Scotland
author_facet Brachmann, Matthew K.
Parsons, Kevin
Skúlason, Skúli
Gaggiotti, Oscar
Ferguson, Moira
author_sort Brachmann, Matthew K.
collection University of St Andrews: Digital Research Repository
container_issue 18
container_start_page 4688
container_title Molecular Ecology
container_volume 31
description Sympatric adaptive phenotypic divergence should be underlain by genomic differentiation between subpopulations. When divergence drives similar patterns of phenotypic and ecological variation within species we expect evolution to draw on common allelic variation. We investigated divergence histories and genomic signatures of adaptive divergence between benthic and pelagic morphs of Icelandic Arctic charr. Divergence histories for each of four populations were reconstructed using coalescent modelling and 14,187 single nucleotide polymorphisms. Sympatric divergence with continuous gene flow was supported in two populations while allopatric divergence with secondary contact was supported in one population; we could not differentiate between demographic models in the fourth population. We detected parallel patterns of phenotypic divergence along benthic-pelagic evolutionary trajectories among populations. Patterns of genomic differentiation between benthic and pelagic morphs were characterized by outlier loci in many narrow peaks of differentiation throughout the genome, which may reflect the eroding effects of gene flow on nearby neutral loci. We then used genome-wide association analyses to relate both phenotypic (body shape and size) and ecological (carbon and nitrogen stable isotopes) variation to patterns of genomic differentiation. Many peaks of genomic differentiation were associated with phenotypic and ecological variation in the three highly divergent populations, suggesting a genomic basis for adaptive divergence. We detected little evidence for a parallel genomic basis of differentiation as most regions and outlier loci were not shared among populations. Our results show that adaptive divergence can have varied genomic consequences in populations with relatively recent common origins, similar divergence histories, and parallel phenotypic divergence. Peer reviewed
format Article in Journal/Newspaper
genre Arctic charr
Arctic
Salvelinus alpinus
genre_facet Arctic charr
Arctic
Salvelinus alpinus
geographic Arctic
geographic_facet Arctic
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institution Open Polar
language English
op_collection_id ftstandrewserep
op_container_end_page 4706
op_doi https://doi.org/10.1111/mec.16625
op_relation Molecular Ecology
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RIS: urn:C25BC25B70650655552D2BC479E620B6
https://hdl.handle.net/10023/28089
doi:10.1111/mec.16625
op_rights Copyright © 2022 John Wiley & Sons Ltd. This work has been made available online in accordance with publisher policies or with permission. Permission for further reuse of this content should be sought from the publisher or the rights holder. This is the author created accepted manuscript following peer review and may differ slightly from the final published version. The final published version of this work is available at https://doi.org/10.1111/mec.16625.
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spelling ftstandrewserep:oai:research-repository.st-andrews.ac.uk:10023/28089 2025-04-13T14:12:21+00:00 Variation in the genomic basis of parallel phenotypic and ecological divergence in benthic and pelagic morphs of Icelandic Arctic charr (Salvelinus alpinus) Brachmann, Matthew K. Parsons, Kevin Skúlason, Skúli Gaggiotti, Oscar Ferguson, Moira University of St Andrews.School of Biology University of St Andrews.Scottish Oceans Institute University of St Andrews.St Andrews Bioinformatics Unit University of St Andrews.Marine Alliance for Science & Technology Scotland 2023-08-03 19 1383428 application/pdf https://hdl.handle.net/10023/28089 https://doi.org/10.1111/mec.16625 eng eng Molecular Ecology 280560693 85135251765 000835802200001 RIS: urn:C25BC25B70650655552D2BC479E620B6 https://hdl.handle.net/10023/28089 doi:10.1111/mec.16625 Copyright © 2022 John Wiley & Sons Ltd. This work has been made available online in accordance with publisher policies or with permission. Permission for further reuse of this content should be sought from the publisher or the rights holder. This is the author created accepted manuscript following peer review and may differ slightly from the final published version. The final published version of this work is available at https://doi.org/10.1111/mec.16625. Adaptation Population genomics Fish Resource polymorphism Adaptive divergence Parallel evolution GC Oceanography QH301 Biology DAS MCC GC QH301 Journal article 2023 ftstandrewserep https://doi.org/10.1111/mec.16625 2025-03-19T08:01:33Z Sympatric adaptive phenotypic divergence should be underlain by genomic differentiation between subpopulations. When divergence drives similar patterns of phenotypic and ecological variation within species we expect evolution to draw on common allelic variation. We investigated divergence histories and genomic signatures of adaptive divergence between benthic and pelagic morphs of Icelandic Arctic charr. Divergence histories for each of four populations were reconstructed using coalescent modelling and 14,187 single nucleotide polymorphisms. Sympatric divergence with continuous gene flow was supported in two populations while allopatric divergence with secondary contact was supported in one population; we could not differentiate between demographic models in the fourth population. We detected parallel patterns of phenotypic divergence along benthic-pelagic evolutionary trajectories among populations. Patterns of genomic differentiation between benthic and pelagic morphs were characterized by outlier loci in many narrow peaks of differentiation throughout the genome, which may reflect the eroding effects of gene flow on nearby neutral loci. We then used genome-wide association analyses to relate both phenotypic (body shape and size) and ecological (carbon and nitrogen stable isotopes) variation to patterns of genomic differentiation. Many peaks of genomic differentiation were associated with phenotypic and ecological variation in the three highly divergent populations, suggesting a genomic basis for adaptive divergence. We detected little evidence for a parallel genomic basis of differentiation as most regions and outlier loci were not shared among populations. Our results show that adaptive divergence can have varied genomic consequences in populations with relatively recent common origins, similar divergence histories, and parallel phenotypic divergence. Peer reviewed Article in Journal/Newspaper Arctic charr Arctic Salvelinus alpinus University of St Andrews: Digital Research Repository Arctic Molecular Ecology 31 18 4688 4706
spellingShingle Adaptation
Population genomics
Fish
Resource polymorphism
Adaptive divergence
Parallel evolution
GC Oceanography
QH301 Biology
DAS
MCC
GC
QH301
Brachmann, Matthew K.
Parsons, Kevin
Skúlason, Skúli
Gaggiotti, Oscar
Ferguson, Moira
Variation in the genomic basis of parallel phenotypic and ecological divergence in benthic and pelagic morphs of Icelandic Arctic charr (Salvelinus alpinus)
title Variation in the genomic basis of parallel phenotypic and ecological divergence in benthic and pelagic morphs of Icelandic Arctic charr (Salvelinus alpinus)
title_full Variation in the genomic basis of parallel phenotypic and ecological divergence in benthic and pelagic morphs of Icelandic Arctic charr (Salvelinus alpinus)
title_fullStr Variation in the genomic basis of parallel phenotypic and ecological divergence in benthic and pelagic morphs of Icelandic Arctic charr (Salvelinus alpinus)
title_full_unstemmed Variation in the genomic basis of parallel phenotypic and ecological divergence in benthic and pelagic morphs of Icelandic Arctic charr (Salvelinus alpinus)
title_short Variation in the genomic basis of parallel phenotypic and ecological divergence in benthic and pelagic morphs of Icelandic Arctic charr (Salvelinus alpinus)
title_sort variation in the genomic basis of parallel phenotypic and ecological divergence in benthic and pelagic morphs of icelandic arctic charr (salvelinus alpinus)
topic Adaptation
Population genomics
Fish
Resource polymorphism
Adaptive divergence
Parallel evolution
GC Oceanography
QH301 Biology
DAS
MCC
GC
QH301
topic_facet Adaptation
Population genomics
Fish
Resource polymorphism
Adaptive divergence
Parallel evolution
GC Oceanography
QH301 Biology
DAS
MCC
GC
QH301
url https://hdl.handle.net/10023/28089
https://doi.org/10.1111/mec.16625