RAD-Seq Reveals Patterns of Additive Polygenic Variation Caused by Spatially-Varying Selection in the American Eel (Anguilla rostrata)

International audience The American Eel (Anguilla rostrata) has an exceptional life cycle characterized by panmictic reproduction at the species scale, random dispersal, and selection in a highly heterogeneous habitat extending from subtropical to subarctic latitudes. The genetic consequences of spa...

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Published in:Genome Biology and Evolution
Main Authors: Babin, Charles, Gagnaire, Pierre-Alexandre, Pavey, Scott, Bernatchez, Louis
Other Authors: Institut de Biologie Intégrative et des Systèmes Québec (IBIS), Institut des Sciences de l'Evolution de Montpellier (UMR ISEM), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-École Pratique des Hautes Études (EPHE), Université Paris Sciences et Lettres (PSL)-Université Paris Sciences et Lettres (PSL)-Université de Montpellier (UM)-Institut de recherche pour le développement IRD : UR226-Centre National de la Recherche Scientifique (CNRS), University of New Brunswick (UNB)
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2017
Subjects:
Online Access:https://hal.science/hal-02395860
https://hal.science/hal-02395860/document
https://hal.science/hal-02395860/file/Babin,%20GBE,%202017.%20RAD-Seq%20reveals%20patterns%20of%20additive%20polygenic%20variation%20caused%20by%20spatially%20varying%20selection%20in%20the%20Americal%20eel.pdf
https://doi.org/10.1093/gbe/evx226
id ftecolephe:oai:HAL:hal-02395860v1
record_format openpolar
institution Open Polar
collection EPHE (Ecole pratique des hautes études, Paris): HAL
op_collection_id ftecolephe
language English
topic panmixia
spatially-varying selection
environmental association
RAD-sequencing
genome scan
polygenic selection
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
[SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE]
[SDV.GEN.GPO]Life Sciences [q-bio]/Genetics/Populations and Evolution [q-bio.PE]
spellingShingle panmixia
spatially-varying selection
environmental association
RAD-sequencing
genome scan
polygenic selection
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
[SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE]
[SDV.GEN.GPO]Life Sciences [q-bio]/Genetics/Populations and Evolution [q-bio.PE]
Babin, Charles
Gagnaire, Pierre-Alexandre
Pavey, Scott
Bernatchez, Louis
RAD-Seq Reveals Patterns of Additive Polygenic Variation Caused by Spatially-Varying Selection in the American Eel (Anguilla rostrata)
topic_facet panmixia
spatially-varying selection
environmental association
RAD-sequencing
genome scan
polygenic selection
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
[SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE]
[SDV.GEN.GPO]Life Sciences [q-bio]/Genetics/Populations and Evolution [q-bio.PE]
description International audience The American Eel (Anguilla rostrata) has an exceptional life cycle characterized by panmictic reproduction at the species scale, random dispersal, and selection in a highly heterogeneous habitat extending from subtropical to subarctic latitudes. The genetic consequences of spatially-varying selection in this species have been investigated for decades, revealing subtle clines in allele frequency at a few loci that contrast with complete panmixia on the vast majority of the genome. Because reproduction homogenizes allele frequencies every generation, sampling size, and genomic coverage are critical to reach sufficient power to detect selected loci in this context. Here, we used a total of 710 individuals from 12 sites and 12,098 high-quality single nucleotide polymorphisms to re-evaluate the extent to which local selection affects the spatial distribution of genetic diversity in this species. We used environmental association methods to identify markers under spatially-varying selection, which indicated that selection affects $1.5% of the genome. We then evaluated the extent to which candidate markers collectively vary with environmental factors using additive polygenic scores. We found significant correlations between polygenic scores and latitude, longitude and temperature which are consistent with polygenic selection acting against maladapted genotypes in different habitats occupied by eels throughout their range of distribution. Gene functions associated with outlier markers were significantly enriched for the insulin signaling pathway, indicating that the trade-offs inherent to occupying such a large distribution range involve the regulation of metabolism. Overall, this study highlights the potential of the additive polygenic scores approach in detecting selective effects in a complex environment.
author2 Institut de Biologie Intégrative et des Systèmes Québec (IBIS)
Institut des Sciences de l'Evolution de Montpellier (UMR ISEM)
Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-École Pratique des Hautes Études (EPHE)
Université Paris Sciences et Lettres (PSL)-Université Paris Sciences et Lettres (PSL)-Université de Montpellier (UM)-Institut de recherche pour le développement IRD : UR226-Centre National de la Recherche Scientifique (CNRS)
University of New Brunswick (UNB)
format Article in Journal/Newspaper
author Babin, Charles
Gagnaire, Pierre-Alexandre
Pavey, Scott
Bernatchez, Louis
author_facet Babin, Charles
Gagnaire, Pierre-Alexandre
Pavey, Scott
Bernatchez, Louis
author_sort Babin, Charles
title RAD-Seq Reveals Patterns of Additive Polygenic Variation Caused by Spatially-Varying Selection in the American Eel (Anguilla rostrata)
title_short RAD-Seq Reveals Patterns of Additive Polygenic Variation Caused by Spatially-Varying Selection in the American Eel (Anguilla rostrata)
title_full RAD-Seq Reveals Patterns of Additive Polygenic Variation Caused by Spatially-Varying Selection in the American Eel (Anguilla rostrata)
title_fullStr RAD-Seq Reveals Patterns of Additive Polygenic Variation Caused by Spatially-Varying Selection in the American Eel (Anguilla rostrata)
title_full_unstemmed RAD-Seq Reveals Patterns of Additive Polygenic Variation Caused by Spatially-Varying Selection in the American Eel (Anguilla rostrata)
title_sort rad-seq reveals patterns of additive polygenic variation caused by spatially-varying selection in the american eel (anguilla rostrata)
publisher HAL CCSD
publishDate 2017
url https://hal.science/hal-02395860
https://hal.science/hal-02395860/document
https://hal.science/hal-02395860/file/Babin,%20GBE,%202017.%20RAD-Seq%20reveals%20patterns%20of%20additive%20polygenic%20variation%20caused%20by%20spatially%20varying%20selection%20in%20the%20Americal%20eel.pdf
https://doi.org/10.1093/gbe/evx226
genre Subarctic
genre_facet Subarctic
op_source ISSN: 1759-6653
EISSN: 1759-6653
Genome Biology and Evolution
https://hal.science/hal-02395860
Genome Biology and Evolution, 2017, 9 (11), pp.2974-2986. ⟨10.1093/gbe/evx226⟩
op_relation info:eu-repo/semantics/altIdentifier/doi/10.1093/gbe/evx226
hal-02395860
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https://hal.science/hal-02395860/file/Babin,%20GBE,%202017.%20RAD-Seq%20reveals%20patterns%20of%20additive%20polygenic%20variation%20caused%20by%20spatially%20varying%20selection%20in%20the%20Americal%20eel.pdf
doi:10.1093/gbe/evx226
op_rights info:eu-repo/semantics/OpenAccess
op_doi https://doi.org/10.1093/gbe/evx226
container_title Genome Biology and Evolution
container_volume 9
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spelling ftecolephe:oai:HAL:hal-02395860v1 2024-05-19T07:49:15+00:00 RAD-Seq Reveals Patterns of Additive Polygenic Variation Caused by Spatially-Varying Selection in the American Eel (Anguilla rostrata) Babin, Charles Gagnaire, Pierre-Alexandre Pavey, Scott Bernatchez, Louis Institut de Biologie Intégrative et des Systèmes Québec (IBIS) Institut des Sciences de l'Evolution de Montpellier (UMR ISEM) Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-École Pratique des Hautes Études (EPHE) Université Paris Sciences et Lettres (PSL)-Université Paris Sciences et Lettres (PSL)-Université de Montpellier (UM)-Institut de recherche pour le développement IRD : UR226-Centre National de la Recherche Scientifique (CNRS) University of New Brunswick (UNB) 2017-11-01 https://hal.science/hal-02395860 https://hal.science/hal-02395860/document https://hal.science/hal-02395860/file/Babin,%20GBE,%202017.%20RAD-Seq%20reveals%20patterns%20of%20additive%20polygenic%20variation%20caused%20by%20spatially%20varying%20selection%20in%20the%20Americal%20eel.pdf https://doi.org/10.1093/gbe/evx226 en eng HAL CCSD Society for Molecular Biology and Evolution info:eu-repo/semantics/altIdentifier/doi/10.1093/gbe/evx226 hal-02395860 https://hal.science/hal-02395860 https://hal.science/hal-02395860/document https://hal.science/hal-02395860/file/Babin,%20GBE,%202017.%20RAD-Seq%20reveals%20patterns%20of%20additive%20polygenic%20variation%20caused%20by%20spatially%20varying%20selection%20in%20the%20Americal%20eel.pdf doi:10.1093/gbe/evx226 info:eu-repo/semantics/OpenAccess ISSN: 1759-6653 EISSN: 1759-6653 Genome Biology and Evolution https://hal.science/hal-02395860 Genome Biology and Evolution, 2017, 9 (11), pp.2974-2986. ⟨10.1093/gbe/evx226⟩ panmixia spatially-varying selection environmental association RAD-sequencing genome scan polygenic selection [SDE.BE]Environmental Sciences/Biodiversity and Ecology [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE] [SDV.GEN.GPO]Life Sciences [q-bio]/Genetics/Populations and Evolution [q-bio.PE] info:eu-repo/semantics/article Journal articles 2017 ftecolephe https://doi.org/10.1093/gbe/evx226 2024-05-02T00:20:10Z International audience The American Eel (Anguilla rostrata) has an exceptional life cycle characterized by panmictic reproduction at the species scale, random dispersal, and selection in a highly heterogeneous habitat extending from subtropical to subarctic latitudes. The genetic consequences of spatially-varying selection in this species have been investigated for decades, revealing subtle clines in allele frequency at a few loci that contrast with complete panmixia on the vast majority of the genome. Because reproduction homogenizes allele frequencies every generation, sampling size, and genomic coverage are critical to reach sufficient power to detect selected loci in this context. Here, we used a total of 710 individuals from 12 sites and 12,098 high-quality single nucleotide polymorphisms to re-evaluate the extent to which local selection affects the spatial distribution of genetic diversity in this species. We used environmental association methods to identify markers under spatially-varying selection, which indicated that selection affects $1.5% of the genome. We then evaluated the extent to which candidate markers collectively vary with environmental factors using additive polygenic scores. We found significant correlations between polygenic scores and latitude, longitude and temperature which are consistent with polygenic selection acting against maladapted genotypes in different habitats occupied by eels throughout their range of distribution. Gene functions associated with outlier markers were significantly enriched for the insulin signaling pathway, indicating that the trade-offs inherent to occupying such a large distribution range involve the regulation of metabolism. Overall, this study highlights the potential of the additive polygenic scores approach in detecting selective effects in a complex environment. Article in Journal/Newspaper Subarctic EPHE (Ecole pratique des hautes études, Paris): HAL Genome Biology and Evolution 9 11 2974 2986