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Rapid Increase in frequency of gene copy-number variants during experimental evolution in Caenorhabditis elegans

BACKGROUND: Gene copy-number variation (CNVs), which provides the raw material for the evolution of novel genes, is widespread in natural populations. We investigated whether CNVs constitute a common mechanism of genetic change during adaptation in experimental Caenorhabditis elegans populations. Ou...

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Autores principales: Farslow, James C., Lipinski, Kendra J., Packard, Lucille B., Edgley, Mark L., Taylor, Jon, Flibotte, Stephane, Moerman, Donald G., Katju, Vaishali, Bergthorsson, Ulfar
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4673709/
https://www.ncbi.nlm.nih.gov/pubmed/26645535
http://dx.doi.org/10.1186/s12864-015-2253-2
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author Farslow, James C.
Lipinski, Kendra J.
Packard, Lucille B.
Edgley, Mark L.
Taylor, Jon
Flibotte, Stephane
Moerman, Donald G.
Katju, Vaishali
Bergthorsson, Ulfar
author_facet Farslow, James C.
Lipinski, Kendra J.
Packard, Lucille B.
Edgley, Mark L.
Taylor, Jon
Flibotte, Stephane
Moerman, Donald G.
Katju, Vaishali
Bergthorsson, Ulfar
author_sort Farslow, James C.
collection PubMed
description BACKGROUND: Gene copy-number variation (CNVs), which provides the raw material for the evolution of novel genes, is widespread in natural populations. We investigated whether CNVs constitute a common mechanism of genetic change during adaptation in experimental Caenorhabditis elegans populations. Outcrossing C. elegans populations with low fitness were evolved for >200 generations. The frequencies of CNVs in these populations were analyzed by oligonucleotide array comparative genome hybridization, quantitative PCR, PCR, DNA sequencing across breakpoints, and single-worm PCR. RESULTS: Multiple duplications and deletions rose to intermediate or high frequencies in independent populations. Several lines of evidence suggest that these changes were adaptive: (i) copy-number changes reached high frequency or were fixed in a short time, (ii) many independent populations harbored CNVs spanning the same genes, and (iii) larger average size of CNVs in adapting populations relative to spontaneous CNVs. The latter is expected if larger CNVs are more likely to encompass genes under selection for a change in gene dosage. Several convergent CNVs originated in populations descended from different low fitness ancestors as well as high fitness controls. CONCLUSIONS: We show that gene copy-number changes are a common class of adaptive genetic change. Due to the high rates of origin of spontaneous duplications and deletions, copy-number changes containing the same genes arose readily in independent populations. Duplications that reached high frequencies in these adapting populations were significantly larger in span. Many convergent CNVs may be general adaptations to laboratory conditions. These results demonstrate the great potential borne by CNVs for evolutionary adaptation. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-015-2253-2) contains supplementary material, which is available to authorized users.
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spelling pubmed-46737092015-12-10 Rapid Increase in frequency of gene copy-number variants during experimental evolution in Caenorhabditis elegans Farslow, James C. Lipinski, Kendra J. Packard, Lucille B. Edgley, Mark L. Taylor, Jon Flibotte, Stephane Moerman, Donald G. Katju, Vaishali Bergthorsson, Ulfar BMC Genomics Research Article BACKGROUND: Gene copy-number variation (CNVs), which provides the raw material for the evolution of novel genes, is widespread in natural populations. We investigated whether CNVs constitute a common mechanism of genetic change during adaptation in experimental Caenorhabditis elegans populations. Outcrossing C. elegans populations with low fitness were evolved for >200 generations. The frequencies of CNVs in these populations were analyzed by oligonucleotide array comparative genome hybridization, quantitative PCR, PCR, DNA sequencing across breakpoints, and single-worm PCR. RESULTS: Multiple duplications and deletions rose to intermediate or high frequencies in independent populations. Several lines of evidence suggest that these changes were adaptive: (i) copy-number changes reached high frequency or were fixed in a short time, (ii) many independent populations harbored CNVs spanning the same genes, and (iii) larger average size of CNVs in adapting populations relative to spontaneous CNVs. The latter is expected if larger CNVs are more likely to encompass genes under selection for a change in gene dosage. Several convergent CNVs originated in populations descended from different low fitness ancestors as well as high fitness controls. CONCLUSIONS: We show that gene copy-number changes are a common class of adaptive genetic change. Due to the high rates of origin of spontaneous duplications and deletions, copy-number changes containing the same genes arose readily in independent populations. Duplications that reached high frequencies in these adapting populations were significantly larger in span. Many convergent CNVs may be general adaptations to laboratory conditions. These results demonstrate the great potential borne by CNVs for evolutionary adaptation. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-015-2253-2) contains supplementary material, which is available to authorized users. BioMed Central 2015-12-09 /pmc/articles/PMC4673709/ /pubmed/26645535 http://dx.doi.org/10.1186/s12864-015-2253-2 Text en © Farslow et al. 2015 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Farslow, James C.
Lipinski, Kendra J.
Packard, Lucille B.
Edgley, Mark L.
Taylor, Jon
Flibotte, Stephane
Moerman, Donald G.
Katju, Vaishali
Bergthorsson, Ulfar
Rapid Increase in frequency of gene copy-number variants during experimental evolution in Caenorhabditis elegans
title Rapid Increase in frequency of gene copy-number variants during experimental evolution in Caenorhabditis elegans
title_full Rapid Increase in frequency of gene copy-number variants during experimental evolution in Caenorhabditis elegans
title_fullStr Rapid Increase in frequency of gene copy-number variants during experimental evolution in Caenorhabditis elegans
title_full_unstemmed Rapid Increase in frequency of gene copy-number variants during experimental evolution in Caenorhabditis elegans
title_short Rapid Increase in frequency of gene copy-number variants during experimental evolution in Caenorhabditis elegans
title_sort rapid increase in frequency of gene copy-number variants during experimental evolution in caenorhabditis elegans
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4673709/
https://www.ncbi.nlm.nih.gov/pubmed/26645535
http://dx.doi.org/10.1186/s12864-015-2253-2
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