Genomic signatures of local directional selection in a high gene flow marine organism; the Atlantic cod (Gadus morhua)
Marine fishes have been shown to display low levels of genetic structuring and associated high levels of gene flow, suggesting shallow evolutionary trajectories and, possibly, limited or lacking adaptive divergence among local populations. We investigated variation in 98 gene-associated single nucle...
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Published in | BMC evolutionary biology Vol. 9; no. 1; p. 276 |
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Main Authors | , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
England
BioMed Central Ltd
01.12.2009
BioMed Central BMC |
Subjects | |
Online Access | Get full text |
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Abstract | Marine fishes have been shown to display low levels of genetic structuring and associated high levels of gene flow, suggesting shallow evolutionary trajectories and, possibly, limited or lacking adaptive divergence among local populations. We investigated variation in 98 gene-associated single nucleotide polymorphisms (SNPs) for evidence of selection in local populations of Atlantic cod (Gadus morhua L.) across the species distribution.
Our global genome scan analysis identified eight outlier gene loci with very high statistical support, likely to be subject to directional selection in local demes, or closely linked to loci under selection. Likewise, on a regional south/north transect of central and eastern Atlantic populations, seven loci displayed strongly elevated levels of genetic differentiation. Selection patterns among populations appeared to be relatively widespread and complex, i.e. outlier loci were generally not only associated with one of a few divergent local populations. Even on a limited geographical scale between the proximate North Sea and Baltic Sea populations four loci displayed evidence of adaptive evolution. Temporal genome scan analysis applied to DNA from archived otoliths from a Faeroese population demonstrated stability of the intra-population variation over 24 years. An exploratory landscape genetic analysis was used to elucidate potential effects of the most likely environmental factors responsible for the signatures of local adaptation. We found that genetic variation at several of the outlier loci was better correlated with temperature and/or salinity conditions at spawning grounds at spawning time than with geographic distance per se.
These findings illustrate that adaptive population divergence may indeed be prevalent despite seemingly high levels of gene flow, as found in most marine fishes. Thus, results have important implications for our understanding of the interplay of evolutionary forces in general, and for the conservation of marine biodiversity under rapidly increasing evolutionary pressure from climate and fisheries induced changes in local environments. |
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AbstractList | Marine fishes have been shown to display low levels of genetic structuring and associated high levels of gene flow, suggesting shallow evolutionary trajectories and, possibly, limited or lacking adaptive divergence among local populations. We investigated variation in 98 gene-associated single nucleotide polymorphisms (SNPs) for evidence of selection in local populations of Atlantic cod (Gadus morhua L.) across the species distribution.
Our global genome scan analysis identified eight outlier gene loci with very high statistical support, likely to be subject to directional selection in local demes, or closely linked to loci under selection. Likewise, on a regional south/north transect of central and eastern Atlantic populations, seven loci displayed strongly elevated levels of genetic differentiation. Selection patterns among populations appeared to be relatively widespread and complex, i.e. outlier loci were generally not only associated with one of a few divergent local populations. Even on a limited geographical scale between the proximate North Sea and Baltic Sea populations four loci displayed evidence of adaptive evolution. Temporal genome scan analysis applied to DNA from archived otoliths from a Faeroese population demonstrated stability of the intra-population variation over 24 years. An exploratory landscape genetic analysis was used to elucidate potential effects of the most likely environmental factors responsible for the signatures of local adaptation. We found that genetic variation at several of the outlier loci was better correlated with temperature and/or salinity conditions at spawning grounds at spawning time than with geographic distance per se.
These findings illustrate that adaptive population divergence may indeed be prevalent despite seemingly high levels of gene flow, as found in most marine fishes. Thus, results have important implications for our understanding of the interplay of evolutionary forces in general, and for the conservation of marine biodiversity under rapidly increasing evolutionary pressure from climate and fisheries induced changes in local environments. BACKGROUND: Marine fishes have been shown to display low levels of genetic structuring and associated high levels of gene flow, suggesting shallow evolutionary trajectories and, possibly, limited or lacking adaptive divergence among local populations. We investigated variation in 98 gene-associated single nucleotide polymorphisms (SNPs) for evidence of selection in local populations of Atlantic cod (Gadus morhua L.) across the species distribution. RESULTS: Our global genome scan analysis identified eight outlier gene loci with very high statistical support, likely to be subject to directional selection in local demes, or closely linked to loci under selection. Likewise, on a regional south/north transect of central and eastern Atlantic populations, seven loci displayed strongly elevated levels of genetic differentiation. Selection patterns among populations appeared to be relatively widespread and complex, i.e. outlier loci were generally not only associated with one of a few divergent local populations. Even on a limited geographical scale between the proximate North Sea and Baltic Sea populations four loci displayed evidence of adaptive evolution. Temporal genome scan analysis applied to DNA from archived otoliths from a Faeroese population demonstrated stability of the intra-population variation over 24 years. An exploratory landscape genetic analysis was used to elucidate potential effects of the most likely environmental factors responsible for the signatures of local adaptation. We found that genetic variation at several of the outlier loci was better correlated with temperature and/or salinity conditions at spawning grounds at spawning time than with geographic distance per se. CONCLUSION: These findings illustrate that adaptive population divergence may indeed be prevalent despite seemingly high levels of gene flow, as found in most marine fishes. Thus, results have important implications for our understanding of the interplay of evolutionary forces in general, and for the conservation of marine biodiversity under rapidly increasing evolutionary pressure from climate and fisheries induced changes in local environments. Marine fishes have been shown to display low levels of genetic structuring and associated high levels of gene flow, suggesting shallow evolutionary trajectories and, possibly, limited or lacking adaptive divergence among local populations. We investigated variation in 98 gene-associated single nucleotide polymorphisms (SNPs) for evidence of selection in local populations of Atlantic cod (Gadus morhua L.) across the species distribution. Our global genome scan analysis identified eight outlier gene loci with very high statistical support, likely to be subject to directional selection in local demes, or closely linked to loci under selection. Likewise, on a regional south/north transect of central and eastern Atlantic populations, seven loci displayed strongly elevated levels of genetic differentiation. Selection patterns among populations appeared to be relatively widespread and complex, i.e. outlier loci were generally not only associated with one of a few divergent local populations. Even on a limited geographical scale between the proximate North Sea and Baltic Sea populations four loci displayed evidence of adaptive evolution. Temporal genome scan analysis applied to DNA from archived otoliths from a Faeroese population demonstrated stability of the intra-population variation over 24 years. An exploratory landscape genetic analysis was used to elucidate potential effects of the most likely environmental factors responsible for the signatures of local adaptation. We found that genetic variation at several of the outlier loci was better correlated with temperature and/or salinity conditions at spawning grounds at spawning time than with geographic distance per se. These findings illustrate that adaptive population divergence may indeed be prevalent despite seemingly high levels of gene flow, as found in most marine fishes. Thus, results have important implications for our understanding of the interplay of evolutionary forces in general, and for the conservation of marine biodiversity under rapidly increasing evolutionary pressure from climate and fisheries induced changes in local environments. Abstract Background: Marine fishes have been shown to display low levels of genetic structuring and associated high levels of gene flow, suggesting shallow evolutionary trajectories and, possibly, limited or lacking adaptive divergence among local populations. We investigated variation in 98 gene-associated single nucleotide polymorphisms (SNPs) for evidence of selection in local populations of Atlantic cod (Gadus morhua L.) across the species distribution. Results: Our global genome scan analysis identified eight outlier gene loci with very high statistical support, likely to be subject to directional selection in local demes, or closely linked to loci under selection. Likewise, on a regional south/north transect of central and eastern Atlantic populations, seven loci displayed strongly elevated levels of genetic differentiation. Selection patterns among populations appeared to be relatively widespread and complex, i.e. outlier loci were generally not only associated with one of a few divergent local populations. Even on a limited geographical scale between the proximate North Sea and Baltic Sea populations four loci displayed evidence of adaptive evolution. Temporal genome scan analysis applied to DNA from archived otoliths from a Faeroese population demonstrated stability of the intra-population variation over 24 years. An exploratory landscape genetic analysis was used to elucidate potential effects of the most likely environmental factors responsible for the signatures of local adaptation. We found that genetic variation at several of the outlier loci was better correlated with temperature and/or salinity conditions at spawning grounds at spawning time than with geographic distance per se . Conclusion: These findings illustrate that adaptive population divergence may indeed be prevalent despite seemingly high levels of gene flow, as found in most marine fishes. Thus, results have important implications for our understanding of the interplay of evolutionary forces in general, and for the conservation of marine biodiversity under rapidly increasing evolutionary pressure from climate and fisheries induced changes in local environments. Marine fishes have been shown to display low levels of genetic structuring and associated high levels of gene flow, suggesting shallow evolutionary trajectories and, possibly, limited or lacking adaptive divergence among local populations. We investigated variation in 98 gene-associated single nucleotide polymorphisms (SNPs) for evidence of selection in local populations of Atlantic cod (Gadus morhua L.) across the species distribution.BACKGROUNDMarine fishes have been shown to display low levels of genetic structuring and associated high levels of gene flow, suggesting shallow evolutionary trajectories and, possibly, limited or lacking adaptive divergence among local populations. We investigated variation in 98 gene-associated single nucleotide polymorphisms (SNPs) for evidence of selection in local populations of Atlantic cod (Gadus morhua L.) across the species distribution.Our global genome scan analysis identified eight outlier gene loci with very high statistical support, likely to be subject to directional selection in local demes, or closely linked to loci under selection. Likewise, on a regional south/north transect of central and eastern Atlantic populations, seven loci displayed strongly elevated levels of genetic differentiation. Selection patterns among populations appeared to be relatively widespread and complex, i.e. outlier loci were generally not only associated with one of a few divergent local populations. Even on a limited geographical scale between the proximate North Sea and Baltic Sea populations four loci displayed evidence of adaptive evolution. Temporal genome scan analysis applied to DNA from archived otoliths from a Faeroese population demonstrated stability of the intra-population variation over 24 years. An exploratory landscape genetic analysis was used to elucidate potential effects of the most likely environmental factors responsible for the signatures of local adaptation. We found that genetic variation at several of the outlier loci was better correlated with temperature and/or salinity conditions at spawning grounds at spawning time than with geographic distance per se.RESULTSOur global genome scan analysis identified eight outlier gene loci with very high statistical support, likely to be subject to directional selection in local demes, or closely linked to loci under selection. Likewise, on a regional south/north transect of central and eastern Atlantic populations, seven loci displayed strongly elevated levels of genetic differentiation. Selection patterns among populations appeared to be relatively widespread and complex, i.e. outlier loci were generally not only associated with one of a few divergent local populations. Even on a limited geographical scale between the proximate North Sea and Baltic Sea populations four loci displayed evidence of adaptive evolution. Temporal genome scan analysis applied to DNA from archived otoliths from a Faeroese population demonstrated stability of the intra-population variation over 24 years. An exploratory landscape genetic analysis was used to elucidate potential effects of the most likely environmental factors responsible for the signatures of local adaptation. We found that genetic variation at several of the outlier loci was better correlated with temperature and/or salinity conditions at spawning grounds at spawning time than with geographic distance per se.These findings illustrate that adaptive population divergence may indeed be prevalent despite seemingly high levels of gene flow, as found in most marine fishes. Thus, results have important implications for our understanding of the interplay of evolutionary forces in general, and for the conservation of marine biodiversity under rapidly increasing evolutionary pressure from climate and fisheries induced changes in local environments.CONCLUSIONThese findings illustrate that adaptive population divergence may indeed be prevalent despite seemingly high levels of gene flow, as found in most marine fishes. Thus, results have important implications for our understanding of the interplay of evolutionary forces in general, and for the conservation of marine biodiversity under rapidly increasing evolutionary pressure from climate and fisheries induced changes in local environments. |
Audience | Academic |
Author | Taranger, Geir-Lasse Ogden, Rob Poulsen, Nina A Loeschcke, Volker Johansen, Torild Moen, Thomas Mittelholzer, Christian Carvalho, Gary R Nielsen, Einar E Hemmer-Hansen, Jakob |
AuthorAffiliation | 5 Institute of Marine Research, PO Box 1870, Nordnes N-5817 Bergen, Norway 4 Institute of Marine Research Tromsø, PO Box 6404, N-9294 Tromsø, Norway 2 Department of Biological Sciences, Genetics and Ecology, University of Aarhus, Building 1540, Ny Munkegade, DK-8000 Aarhus C, Denmark 7 Molecular Ecology & Fisheries Genetics Laboratory, School of Biological Sciences, Environment Centre Wales, Bangor University, Bangor, Gwynedd LL57 2UW, UK 8 Current address: University of Basel, Klingelbergstrasse 50/70, CH-4056 Basel, Switzerland 1 National Institute of Aquatic Resources, Technical University of Denmark, Vejlsøvej 39, DK-8600 Silkeborg, Denmark 3 CIGENE, PO Box 5003, N-1434 Ås, Norway 6 Tepnel Research Products and Services, Appleton Place, Livingston, EH54 7EZ, UK |
AuthorAffiliation_xml | – name: 5 Institute of Marine Research, PO Box 1870, Nordnes N-5817 Bergen, Norway – name: 7 Molecular Ecology & Fisheries Genetics Laboratory, School of Biological Sciences, Environment Centre Wales, Bangor University, Bangor, Gwynedd LL57 2UW, UK – name: 4 Institute of Marine Research Tromsø, PO Box 6404, N-9294 Tromsø, Norway – name: 3 CIGENE, PO Box 5003, N-1434 Ås, Norway – name: 6 Tepnel Research Products and Services, Appleton Place, Livingston, EH54 7EZ, UK – name: 2 Department of Biological Sciences, Genetics and Ecology, University of Aarhus, Building 1540, Ny Munkegade, DK-8000 Aarhus C, Denmark – name: 1 National Institute of Aquatic Resources, Technical University of Denmark, Vejlsøvej 39, DK-8600 Silkeborg, Denmark – name: 8 Current address: University of Basel, Klingelbergstrasse 50/70, CH-4056 Basel, Switzerland |
Author_xml | – sequence: 1 givenname: Einar E surname: Nielsen fullname: Nielsen, Einar E – sequence: 2 givenname: Jakob surname: Hemmer-Hansen fullname: Hemmer-Hansen, Jakob – sequence: 3 givenname: Nina A surname: Poulsen fullname: Poulsen, Nina A – sequence: 4 givenname: Volker surname: Loeschcke fullname: Loeschcke, Volker – sequence: 5 givenname: Thomas surname: Moen fullname: Moen, Thomas – sequence: 6 givenname: Torild surname: Johansen fullname: Johansen, Torild – sequence: 7 givenname: Christian surname: Mittelholzer fullname: Mittelholzer, Christian – sequence: 8 givenname: Geir-Lasse surname: Taranger fullname: Taranger, Geir-Lasse – sequence: 9 givenname: Rob surname: Ogden fullname: Ogden, Rob – sequence: 10 givenname: Gary R surname: Carvalho fullname: Carvalho, Gary R |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/19948077$$D View this record in MEDLINE/PubMed |
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ContentType | Journal Article |
Copyright | COPYRIGHT 2009 BioMed Central Ltd. 2009 Nielsen et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Copyright ©2009 Nielsen et al; licensee BioMed Central Ltd. 2009 Nielsen et al; licensee BioMed Central Ltd. |
Copyright_xml | – notice: COPYRIGHT 2009 BioMed Central Ltd. – notice: 2009 Nielsen et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. – notice: Copyright ©2009 Nielsen et al; licensee BioMed Central Ltd. 2009 Nielsen et al; licensee BioMed Central Ltd. |
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Snippet | Marine fishes have been shown to display low levels of genetic structuring and associated high levels of gene flow, suggesting shallow evolutionary... Background Marine fishes have been shown to display low levels of genetic structuring and associated high levels of gene flow, suggesting shallow evolutionary... Abstract Background: Marine fishes have been shown to display low levels of genetic structuring and associated high levels of gene flow, suggesting shallow... BACKGROUND: Marine fishes have been shown to display low levels of genetic structuring and associated high levels of gene flow, suggesting shallow evolutionary... Abstract Background Marine fishes have been shown to display low levels of genetic structuring and associated high levels of gene flow, suggesting shallow... |
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SubjectTerms | Adaptation, Physiological - genetics Animals Atlantic Ocean Bayes Theorem Biological diversity Cod Design Environmental conditions Environmental factors Evolution & development Evolution, Molecular Fish Fishing Gadus morhua Gadus morhua - genetics Gene Flow Genes Genetic aspects Genetic diversity Genetic research Genetics, Population Genome Genomes Influence Local population Marine Marine fish North Sea Organisms Otoliths Polymorphism, Single Nucleotide Research article Salinity Sequence Analysis, DNA Spawning Spawning grounds Studies Variables |
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Title | Genomic signatures of local directional selection in a high gene flow marine organism; the Atlantic cod (Gadus morhua) |
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