Bringing together evolution on serpentine and polyploidy: spatiotemporal history of the diploid-tetraploid complex of Knautia arvensis (Dipsacaceae)
Polyploidization is one of the leading forces in the evolution of land plants, providing opportunities for instant speciation and rapid gain of evolutionary novelties. Highly selective conditions of serpentine environments act as an important evolutionary trigger that can be involved in various spec...
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Published in | PloS one Vol. 7; no. 7; p. e39988 |
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Main Authors | , , , , , , |
Format | Journal Article |
Language | English |
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Public Library of Science
05.07.2012
Public Library of Science (PLoS) |
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Abstract | Polyploidization is one of the leading forces in the evolution of land plants, providing opportunities for instant speciation and rapid gain of evolutionary novelties. Highly selective conditions of serpentine environments act as an important evolutionary trigger that can be involved in various speciation processes. Whereas the significance of both edaphic speciation on serpentine and polyploidy is widely acknowledged in plant evolution, the links between polyploid evolution and serpentine differentiation have not yet been examined. To fill this gap, we investigated the evolutionary history of the perennial herb Knautia arvensis (Dipsacaceae), a diploid-tetraploid complex that exhibits an intriguing pattern of eco-geographic differentiation. Using plastid DNA sequencing and AFLP genotyping of 336 previously cytotyped individuals from 40 populations from central Europe, we unravelled the patterns of genetic variation among the cytotypes and the edaphic types. Diploids showed the highest levels of genetic differentiation, likely as a result of long term persistence of several lineages in ecologically distinct refugia and/or independent immigration. Recurrent polyploidization, recorded in one serpentine island, seems to have opened new possibilities for the local serpentine genotype. Unlike diploids, the serpentine tetraploids were able to escape from the serpentine refugium and spread further; this was also attributable to hybridization with the neighbouring non-serpentine tetraploid lineages. The spatiotemporal history of K. arvensis allows tracing the interplay of polyploid evolution and ecological divergence on serpentine, resulting in a complex evolutionary pattern. Isolated serpentine outcrops can act as evolutionary capacitors, preserving distinct karyological and genetic diversity. The serpentine lineages, however, may not represent evolutionary 'dead-ends' but rather dynamic systems with a potential to further influence the surrounding populations, e.g., via independent polyplodization and hybridization. The complex eco-geographical pattern together with the incidence of both primary and secondary diploid-tetraploid contact zones makes K. arvensis a unique system for addressing general questions of polyploid research. |
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AbstractList | Polyploidization is one of the leading forces in the evolution of land plants, providing opportunities for instant speciation and rapid gain of evolutionary novelties. Highly selective conditions of serpentine environments act as an important evolutionary trigger that can be involved in various speciation processes. Whereas the significance of both edaphic speciation on serpentine and polyploidy is widely acknowledged in plant evolution, the links between polyploid evolution and serpentine differentiation have not yet been examined. To fill this gap, we investigated the evolutionary history of the perennial herb Knautia arvensis (Dipsacaceae), a diploid-tetraploid complex that exhibits an intriguing pattern of eco-geographic differentiation. Using plastid DNA sequencing and AFLP genotyping of 336 previously cytotyped individuals from 40 populations from central Europe, we unravelled the patterns of genetic variation among the cytotypes and the edaphic types. Diploids showed the highest levels of genetic differentiation, likely as a result of long term persistence of several lineages in ecologically distinct refugia and/or independent immigration. Recurrent polyploidization, recorded in one serpentine island, seems to have opened new possibilities for the local serpentine genotype. Unlike diploids, the serpentine tetraploids were able to escape from the serpentine refugium and spread further; this was also attributable to hybridization with the neighbouring non-serpentine tetraploid lineages. The spatiotemporal history of K. arvensis allows tracing the interplay of polyploid evolution and ecological divergence on serpentine, resulting in a complex evolutionary pattern. Isolated serpentine outcrops can act as evolutionary capacitors, preserving distinct karyological and genetic diversity. The serpentine lineages, however, may not represent evolutionary ‘dead-ends’ but rather dynamic systems with a potential to further influence the surrounding populations, e.g., via independent polyplodization and hybridization. The complex eco-geographical pattern together with the incidence of both primary and secondary diploid-tetraploid contact zones makes K. arvensis a unique system for addressing general questions of polyploid research. Polyploidization is one of the leading forces in the evolution of land plants, providing opportunities for instant speciation and rapid gain of evolutionary novelties. Highly selective conditions of serpentine environments act as an important evolutionary trigger that can be involved in various speciation processes. Whereas the significance of both edaphic speciation on serpentine and polyploidy is widely acknowledged in plant evolution, the links between polyploid evolution and serpentine differentiation have not yet been examined. To fill this gap, we investigated the evolutionary history of the perennial herb Knautia arvensis (Dipsacaceae), a diploid-tetraploid complex that exhibits an intriguing pattern of eco-geographic differentiation. Using plastid DNA sequencing and AFLP genotyping of 336 previously cytotyped individuals from 40 populations from central Europe, we unravelled the patterns of genetic variation among the cytotypes and the edaphic types. Diploids showed the highest levels of genetic differentiation, likely as a result of long term persistence of several lineages in ecologically distinct refugia and/or independent immigration. Recurrent polyploidization, recorded in one serpentine island, seems to have opened new possibilities for the local serpentine genotype. Unlike diploids, the serpentine tetraploids were able to escape from the serpentine refugium and spread further; this was also attributable to hybridization with the neighbouring non-serpentine tetraploid lineages. The spatiotemporal history of K. arvensis allows tracing the interplay of polyploid evolution and ecological divergence on serpentine, resulting in a complex evolutionary pattern. Isolated serpentine outcrops can act as evolutionary capacitors, preserving distinct karyological and genetic diversity. The serpentine lineages, however, may not represent evolutionary ‘dead-ends’ but rather dynamic systems with a potential to further influence the surrounding populations, e.g., via independent polyplodization and hybridization. The complex eco-geographical pattern together with the incidence of both primary and secondary diploid-tetraploid contact zones makes K. arvensis a unique system for addressing general questions of polyploid research. |
Audience | Academic |
Author | Schönswetter, Peter Kolář, Filip Trávníček, Pavel Štech, Milan Dušková, Eva Fér, Tomáš Suda, Jan |
AuthorAffiliation | 4 Institute of Botany, University of Innsbruck, Innsbruck, Austria 1 Department of Botany, Faculty of Science, Charles University in Prague, Prague, Czech Republic 2 Institute of Botany, Academy of Sciences of the Czech Republic, Průhonice, Czech Republic University of Lausanne, Switzerland 3 Department of Botany, Faculty of Science, University of South Bohemia, České Budějovice, Czech Republic |
AuthorAffiliation_xml | – name: 2 Institute of Botany, Academy of Sciences of the Czech Republic, Průhonice, Czech Republic – name: University of Lausanne, Switzerland – name: 3 Department of Botany, Faculty of Science, University of South Bohemia, České Budějovice, Czech Republic – name: 4 Institute of Botany, University of Innsbruck, Innsbruck, Austria – name: 1 Department of Botany, Faculty of Science, Charles University in Prague, Prague, Czech Republic |
Author_xml | – sequence: 1 givenname: Filip surname: Kolář fullname: Kolář, Filip email: filip.kolar@gmail.com organization: Department of Botany, Faculty of Science, Charles University in Prague, Prague, Czech Republic. filip.kolar@gmail.com – sequence: 2 givenname: Tomáš surname: Fér fullname: Fér, Tomáš – sequence: 3 givenname: Milan surname: Štech fullname: Štech, Milan – sequence: 4 givenname: Pavel surname: Trávníček fullname: Trávníček, Pavel – sequence: 5 givenname: Eva surname: Dušková fullname: Dušková, Eva – sequence: 6 givenname: Peter surname: Schönswetter fullname: Schönswetter, Peter – sequence: 7 givenname: Jan surname: Suda fullname: Suda, Jan |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/22792207$$D View this record in MEDLINE/PubMed |
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ContentType | Journal Article |
Copyright | COPYRIGHT 2012 Public Library of Science 2012 Kolář et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. Kolář et al. 2012 |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Conceived and designed the experiments: JS MS. Performed the experiments: FK TF MS ED PT. Analyzed the data: FK TF. Contributed reagents/materials/analysis tools: PS. Wrote the paper: FK JS TF PS. |
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SubjectTerms | Amplified fragment length polymorphism Amplified Fragment Length Polymorphism Analysis Asbestos, Serpentine Biodiversity Biological Evolution Biology Chromosomes Consumer goods Deoxyribonucleic acid Differentiation Diploids Dipsacaceae Dipsacaceae - genetics Dipsacaceae - metabolism Divergence DNA DNA sequencing Ecological effects Ecology Ecosystem Europe Evolution Evolutionary biology Evolutionary genetics Flowers & plants Gene sequencing Genetic diversity Genome, Plant Genomes Genotyping Haplotypes Heavy metal content Hybridization Immigration Knautia arvensis Outcrops Phenotype Phylogeny Plant evolution Plastids - genetics Polyploidy Populations Refugia Science Serpentine Soil - chemistry Speciation Trends |
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Title | Bringing together evolution on serpentine and polyploidy: spatiotemporal history of the diploid-tetraploid complex of Knautia arvensis (Dipsacaceae) |
URI | https://www.ncbi.nlm.nih.gov/pubmed/22792207 https://www.proquest.com/docview/1325396089 https://search.proquest.com/docview/1024935305 https://pubmed.ncbi.nlm.nih.gov/PMC3390331 https://doaj.org/article/ad915237d32e4c77806623c744978bbe http://dx.doi.org/10.1371/journal.pone.0039988 |
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