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

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(...

Full description

Bibliographic Details
Main Authors: Strickland, K., Räsänen, K., Kristjánsson, B. K., Phillips, J. S., Einarsson, A., Snorradóttir, R. G., Bartrons, M., Jónsson, Z. O.
Format: Article in Journal/Newspaper
Language:English
Published: Wiley-Blackwell 2023
Subjects:
DNA
Online Access:http://urn.fi/URN:NBN:fi:jyu-202304062423
id ftjyvaeskylaenun:oai:jyx.jyu.fi:123456789/86292
record_format openpolar
spelling ftjyvaeskylaenun:oai:jyx.jyu.fi:123456789/86292 2024-05-19T07:42:55+00:00 Genome‐phenotype‐environment associations identify signatures of selection in a panmictic population of threespine stickleback Strickland, K. Räsänen, K. Kristjánsson, B. K. Phillips, J. S. Einarsson, A. Snorradóttir, R. G. Bartrons, M. Jónsson, Z. O. 2023 application/pdf 1708-1725 fulltext http://urn.fi/URN:NBN:fi:jyu-202304062423 eng eng Wiley-Blackwell Molecular Ecology 0962-1083 7 32 10.1111/mec.16845 Strickland, K., Räsänen, K., Kristjánsson, B. K., Phillips, J. S., Einarsson, A., Snorradóttir, R. G., Bartrons, M., & Jónsson, Z. O. (2023). Genome‐phenotype‐environment associations identify signatures of selection in a panmictic population of threespine stickleback. Molecular Ecology , 32 (7), 1708-1725. https://doi.org/10.1111/mec.16845 CONVID_172617005 URN:NBN:fi:jyu-202304062423 http://urn.fi/URN:NBN:fi:jyu-202304062423 CC BY 4.0 © 2023 the Authors openAccess https://creativecommons.org/licenses/by/4.0/ adaptive divergence gene flow environmental gradients genome scans landscape genomics gasterosteus aculeatus populaatiogenetiikka rakenne (ominaisuudet) perimä DNA ominaisuudet geenit periytyvyys fenotyyppi article http://purl.org/eprint/type/JournalArticle http://purl.org/coar/resource_type/c_2df8fbb1 publishedVersion A1 2023 ftjyvaeskylaenun 2024-04-23T23:38:28Z 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 (h2 = 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 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. peerReviewed Article in Journal/Newspaper Iceland Mývatn JYX - Jyväskylä University Digital Archive
institution Open Polar
collection JYX - Jyväskylä University Digital Archive
op_collection_id ftjyvaeskylaenun
language English
topic adaptive divergence
gene flow
environmental gradients
genome scans
landscape genomics
gasterosteus aculeatus
populaatiogenetiikka
rakenne (ominaisuudet)
perimä
DNA
ominaisuudet
geenit
periytyvyys
fenotyyppi
spellingShingle adaptive divergence
gene flow
environmental gradients
genome scans
landscape genomics
gasterosteus aculeatus
populaatiogenetiikka
rakenne (ominaisuudet)
perimä
DNA
ominaisuudet
geenit
periytyvyys
fenotyyppi
Strickland, K.
Räsänen, K.
Kristjánsson, B. K.
Phillips, J. S.
Einarsson, A.
Snorradóttir, R. G.
Bartrons, M.
Jónsson, Z. O.
Genome‐phenotype‐environment associations identify signatures of selection in a panmictic population of threespine stickleback
topic_facet adaptive divergence
gene flow
environmental gradients
genome scans
landscape genomics
gasterosteus aculeatus
populaatiogenetiikka
rakenne (ominaisuudet)
perimä
DNA
ominaisuudet
geenit
periytyvyys
fenotyyppi
description 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 (h2 = 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 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. peerReviewed
format Article in Journal/Newspaper
author Strickland, K.
Räsänen, K.
Kristjánsson, B. K.
Phillips, J. S.
Einarsson, A.
Snorradóttir, R. G.
Bartrons, M.
Jónsson, Z. O.
author_facet Strickland, K.
Räsänen, K.
Kristjánsson, B. K.
Phillips, J. S.
Einarsson, A.
Snorradóttir, R. G.
Bartrons, M.
Jónsson, Z. O.
author_sort Strickland, K.
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-Blackwell
publishDate 2023
url http://urn.fi/URN:NBN:fi:jyu-202304062423
genre Iceland
Mývatn
genre_facet Iceland
Mývatn
op_relation Molecular Ecology
0962-1083
7
32
10.1111/mec.16845
Strickland, K., Räsänen, K., Kristjánsson, B. K., Phillips, J. S., Einarsson, A., Snorradóttir, R. G., Bartrons, M., & Jónsson, Z. O. (2023). Genome‐phenotype‐environment associations identify signatures of selection in a panmictic population of threespine stickleback. Molecular Ecology , 32 (7), 1708-1725. https://doi.org/10.1111/mec.16845
CONVID_172617005
URN:NBN:fi:jyu-202304062423
http://urn.fi/URN:NBN:fi:jyu-202304062423
op_rights CC BY 4.0
© 2023 the Authors
openAccess
https://creativecommons.org/licenses/by/4.0/
_version_ 1799482623594070016