Genome‐phenotype‐environment associations identify signatures of selection in a panmictic population of threespine stickleback

Abstract Adaptive genetic divergence occurs when selection imposed by the environment causes the genomic component of the phenotype to differentiate. However, genomic signatures of natural selection are usually identified without information on which trait is responding to selection by which selecti...

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Published in:Molecular Ecology
Main Authors: Strickland, Kasha, Räsänen, Katja, Kristjánsson, Bjarni Kristofer, Phillips, Joseph S., Einarsson, Arni, Snorradóttir, Ragna G., Bartrons, Mireia, Jónsson, Zophonías Oddur
Other Authors: Icelandic Centre for Research
Format: Article in Journal/Newspaper
Language:English
Published: Wiley 2023
Subjects:
Online Access:http://dx.doi.org/10.1111/mec.16845
https://onlinelibrary.wiley.com/doi/pdf/10.1111/mec.16845
https://onlinelibrary.wiley.com/doi/full-xml/10.1111/mec.16845
id crwiley:10.1111/mec.16845
record_format openpolar
spelling crwiley:10.1111/mec.16845 2024-03-31T07:53:33+00:00 Genome‐phenotype‐environment associations identify signatures of selection in a panmictic population of threespine stickleback Strickland, Kasha Räsänen, Katja Kristjánsson, Bjarni Kristofer Phillips, Joseph S. Einarsson, Arni Snorradóttir, Ragna G. Bartrons, Mireia Jónsson, Zophonías Oddur Icelandic Centre for Research 2023 http://dx.doi.org/10.1111/mec.16845 https://onlinelibrary.wiley.com/doi/pdf/10.1111/mec.16845 https://onlinelibrary.wiley.com/doi/full-xml/10.1111/mec.16845 en eng Wiley http://creativecommons.org/licenses/by/4.0/ Molecular Ecology volume 32, issue 7, page 1708-1725 ISSN 0962-1083 1365-294X Genetics Ecology, Evolution, Behavior and Systematics journal-article 2023 crwiley https://doi.org/10.1111/mec.16845 2024-03-04T13:00:35Z Abstract Adaptive genetic divergence occurs when selection imposed by the environment causes the genomic component of the phenotype to differentiate. However, genomic signatures of natural selection are usually identified without information on which trait is responding to selection by which selective agent(s). Here, we integrate whole‐genome sequencing with phenomics and measures of putative selective agents to assess the extent of adaptive divergence in threespine stickleback occupying the highly heterogeneous lake Mývatn, NE Iceland. We find negligible genome wide divergence, yet multiple traits (body size, gill raker structure and defence traits) were divergent along known ecological gradients (temperature, predatory bird densities and water depth). SNP based heritability of all measured traits was high ( h 2 = 0.42–0.65), indicating adaptive potential for all traits. Environment‐association analyses further identified thousands of loci putatively involved in selection, related to genes linked to, for instance, neuron development and protein phosphorylation. Finally, we found that loci linked to water depth were concurrently associated with pelvic spine length variation ‐ supporting the conclusion that divergence in pelvic spine length occurred in the face of gene flow. Our results suggest that whilst there is substantial genetic variation in the traits measured, phenotypic divergence of Mývatn stickleback is mostly weakly associated with environmental gradients, potentially as a result of substantial gene flow. Our study illustrates the value of integrative studies that combine genomic assays of multivariate trait variation with landscape genomics. Article in Journal/Newspaper Iceland Mývatn Wiley Online Library Mývatn ENVELOPE(-16.985,-16.985,65.600,65.600) Molecular Ecology 32 7 1708 1725
institution Open Polar
collection Wiley Online Library
op_collection_id crwiley
language English
topic Genetics
Ecology, Evolution, Behavior and Systematics
spellingShingle Genetics
Ecology, Evolution, Behavior and Systematics
Strickland, Kasha
Räsänen, Katja
Kristjánsson, Bjarni Kristofer
Phillips, Joseph S.
Einarsson, Arni
Snorradóttir, Ragna G.
Bartrons, Mireia
Jónsson, Zophonías Oddur
Genome‐phenotype‐environment associations identify signatures of selection in a panmictic population of threespine stickleback
topic_facet Genetics
Ecology, Evolution, Behavior and Systematics
description Abstract Adaptive genetic divergence occurs when selection imposed by the environment causes the genomic component of the phenotype to differentiate. However, genomic signatures of natural selection are usually identified without information on which trait is responding to selection by which selective agent(s). Here, we integrate whole‐genome sequencing with phenomics and measures of putative selective agents to assess the extent of adaptive divergence in threespine stickleback occupying the highly heterogeneous lake Mývatn, NE Iceland. We find negligible genome wide divergence, yet multiple traits (body size, gill raker structure and defence traits) were divergent along known ecological gradients (temperature, predatory bird densities and water depth). SNP based heritability of all measured traits was high ( h 2 = 0.42–0.65), indicating adaptive potential for all traits. Environment‐association analyses further identified thousands of loci putatively involved in selection, related to genes linked to, for instance, neuron development and protein phosphorylation. Finally, we found that loci linked to water depth were concurrently associated with pelvic spine length variation ‐ supporting the conclusion that divergence in pelvic spine length occurred in the face of gene flow. Our results suggest that whilst there is substantial genetic variation in the traits measured, phenotypic divergence of Mývatn stickleback is mostly weakly associated with environmental gradients, potentially as a result of substantial gene flow. Our study illustrates the value of integrative studies that combine genomic assays of multivariate trait variation with landscape genomics.
author2 Icelandic Centre for Research
format Article in Journal/Newspaper
author Strickland, Kasha
Räsänen, Katja
Kristjánsson, Bjarni Kristofer
Phillips, Joseph S.
Einarsson, Arni
Snorradóttir, Ragna G.
Bartrons, Mireia
Jónsson, Zophonías Oddur
author_facet Strickland, Kasha
Räsänen, Katja
Kristjánsson, Bjarni Kristofer
Phillips, Joseph S.
Einarsson, Arni
Snorradóttir, Ragna G.
Bartrons, Mireia
Jónsson, Zophonías Oddur
author_sort Strickland, Kasha
title Genome‐phenotype‐environment associations identify signatures of selection in a panmictic population of threespine stickleback
title_short Genome‐phenotype‐environment associations identify signatures of selection in a panmictic population of threespine stickleback
title_full Genome‐phenotype‐environment associations identify signatures of selection in a panmictic population of threespine stickleback
title_fullStr Genome‐phenotype‐environment associations identify signatures of selection in a panmictic population of threespine stickleback
title_full_unstemmed Genome‐phenotype‐environment associations identify signatures of selection in a panmictic population of threespine stickleback
title_sort genome‐phenotype‐environment associations identify signatures of selection in a panmictic population of threespine stickleback
publisher Wiley
publishDate 2023
url http://dx.doi.org/10.1111/mec.16845
https://onlinelibrary.wiley.com/doi/pdf/10.1111/mec.16845
https://onlinelibrary.wiley.com/doi/full-xml/10.1111/mec.16845
long_lat ENVELOPE(-16.985,-16.985,65.600,65.600)
geographic Mývatn
geographic_facet Mývatn
genre Iceland
Mývatn
genre_facet Iceland
Mývatn
op_source Molecular Ecology
volume 32, issue 7, page 1708-1725
ISSN 0962-1083 1365-294X
op_rights http://creativecommons.org/licenses/by/4.0/
op_doi https://doi.org/10.1111/mec.16845
container_title Molecular Ecology
container_volume 32
container_issue 7
container_start_page 1708
op_container_end_page 1725
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