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Patterns of rapid diversification in heteroploid Knautia sect. Trichera (Caprifoliaceae, Dipsacoideae), one of the most intricate taxa of the European flora

BACKGROUND: Polyploidy is one of the most important evolutionary pathways in flowering plants and has significantly contributed to their diversification and radiation. Due to the prevalence of reticulate evolution spanning three ploidy levels, Knautia is considered one of the taxonomically most intr...

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Autores principales: Frajman, Božo, Rešetnik, Ivana, Niketić, Marjan, Ehrendorfer, Friedrich, Schönswetter, Peter
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5057222/
https://www.ncbi.nlm.nih.gov/pubmed/27724874
http://dx.doi.org/10.1186/s12862-016-0773-2
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author Frajman, Božo
Rešetnik, Ivana
Niketić, Marjan
Ehrendorfer, Friedrich
Schönswetter, Peter
author_facet Frajman, Božo
Rešetnik, Ivana
Niketić, Marjan
Ehrendorfer, Friedrich
Schönswetter, Peter
author_sort Frajman, Božo
collection PubMed
description BACKGROUND: Polyploidy is one of the most important evolutionary pathways in flowering plants and has significantly contributed to their diversification and radiation. Due to the prevalence of reticulate evolution spanning three ploidy levels, Knautia is considered one of the taxonomically most intricate groups in the European flora. On the basis of ITS and plastid DNA sequences as well as AFLP fingerprints obtained from 381 populations of almost all species of the genus we asked the following questions. (1) Where and when did the initial diversification in Knautia take place, and how did it proceed further? (2) Did Knautia undergo a similarly recent (Pliocene/Pleistocene) rapid radiation as other genera with similar ecology and overlapping distribution? (3) Did polyploids evolve within the previously recognised diploid groups or rather from hybridisation between groups? RESULTS: The diversification of Knautia was centred in the Eastern Mediterranean. According to our genetic data, the genus originated in the Early Miocene and started to diversify in the Middle Miocene, whereas the onset of radiation of sect. Trichera was in central parts of the Balkan Peninsula, roughly 4 Ma. Extensive spread out of the Balkans started in the Pleistocene about 1.5 Ma. Diversification of sect. Trichera was strongly fostered by polyploidisation, which occurred independently many times. Tetraploids are observed in almost all evolutionary lineages whereas hexaploids are rarer and restricted to a few phylogenetic groups. Whether polyploids originated via autopolyploidy or allopolyploidy is unclear due to the weak genetic separation among species. In spite of the complexity of sect. Trichera, we present nine AFLP-characterised informal species groups, which coincide only partly with former traditional groups. CONCLUSIONS: Knautia sect. Trichera is a prime example for rapid diversification, mostly taking place during Pliocene and Pleistocene. Numerous cycles of habitat fragmentation and subsequent reconnections likely promoted hybridisation and polyploidisation. Extensive haplotype sharing and unresolved phylogenetic relationships suggest that these processes occurred rapidly and extensively. Thus, the dynamic polyploid evolution, the lack of crossing barriers within ploidy levels supported by conserved floral morphology, the highly variable leaf morphology and unstable indumentum composition prevent establishing a well-founded taxonomic framework. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-016-0773-2) contains supplementary material, which is available to authorized users.
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spelling pubmed-50572222016-10-20 Patterns of rapid diversification in heteroploid Knautia sect. Trichera (Caprifoliaceae, Dipsacoideae), one of the most intricate taxa of the European flora Frajman, Božo Rešetnik, Ivana Niketić, Marjan Ehrendorfer, Friedrich Schönswetter, Peter BMC Evol Biol Research Article BACKGROUND: Polyploidy is one of the most important evolutionary pathways in flowering plants and has significantly contributed to their diversification and radiation. Due to the prevalence of reticulate evolution spanning three ploidy levels, Knautia is considered one of the taxonomically most intricate groups in the European flora. On the basis of ITS and plastid DNA sequences as well as AFLP fingerprints obtained from 381 populations of almost all species of the genus we asked the following questions. (1) Where and when did the initial diversification in Knautia take place, and how did it proceed further? (2) Did Knautia undergo a similarly recent (Pliocene/Pleistocene) rapid radiation as other genera with similar ecology and overlapping distribution? (3) Did polyploids evolve within the previously recognised diploid groups or rather from hybridisation between groups? RESULTS: The diversification of Knautia was centred in the Eastern Mediterranean. According to our genetic data, the genus originated in the Early Miocene and started to diversify in the Middle Miocene, whereas the onset of radiation of sect. Trichera was in central parts of the Balkan Peninsula, roughly 4 Ma. Extensive spread out of the Balkans started in the Pleistocene about 1.5 Ma. Diversification of sect. Trichera was strongly fostered by polyploidisation, which occurred independently many times. Tetraploids are observed in almost all evolutionary lineages whereas hexaploids are rarer and restricted to a few phylogenetic groups. Whether polyploids originated via autopolyploidy or allopolyploidy is unclear due to the weak genetic separation among species. In spite of the complexity of sect. Trichera, we present nine AFLP-characterised informal species groups, which coincide only partly with former traditional groups. CONCLUSIONS: Knautia sect. Trichera is a prime example for rapid diversification, mostly taking place during Pliocene and Pleistocene. Numerous cycles of habitat fragmentation and subsequent reconnections likely promoted hybridisation and polyploidisation. Extensive haplotype sharing and unresolved phylogenetic relationships suggest that these processes occurred rapidly and extensively. Thus, the dynamic polyploid evolution, the lack of crossing barriers within ploidy levels supported by conserved floral morphology, the highly variable leaf morphology and unstable indumentum composition prevent establishing a well-founded taxonomic framework. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-016-0773-2) contains supplementary material, which is available to authorized users. BioMed Central 2016-10-10 /pmc/articles/PMC5057222/ /pubmed/27724874 http://dx.doi.org/10.1186/s12862-016-0773-2 Text en © The Author(s). 2016 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
Frajman, Božo
Rešetnik, Ivana
Niketić, Marjan
Ehrendorfer, Friedrich
Schönswetter, Peter
Patterns of rapid diversification in heteroploid Knautia sect. Trichera (Caprifoliaceae, Dipsacoideae), one of the most intricate taxa of the European flora
title Patterns of rapid diversification in heteroploid Knautia sect. Trichera (Caprifoliaceae, Dipsacoideae), one of the most intricate taxa of the European flora
title_full Patterns of rapid diversification in heteroploid Knautia sect. Trichera (Caprifoliaceae, Dipsacoideae), one of the most intricate taxa of the European flora
title_fullStr Patterns of rapid diversification in heteroploid Knautia sect. Trichera (Caprifoliaceae, Dipsacoideae), one of the most intricate taxa of the European flora
title_full_unstemmed Patterns of rapid diversification in heteroploid Knautia sect. Trichera (Caprifoliaceae, Dipsacoideae), one of the most intricate taxa of the European flora
title_short Patterns of rapid diversification in heteroploid Knautia sect. Trichera (Caprifoliaceae, Dipsacoideae), one of the most intricate taxa of the European flora
title_sort patterns of rapid diversification in heteroploid knautia sect. trichera (caprifoliaceae, dipsacoideae), one of the most intricate taxa of the european flora
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5057222/
https://www.ncbi.nlm.nih.gov/pubmed/27724874
http://dx.doi.org/10.1186/s12862-016-0773-2
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