Polyploid evolution and Pleistocene glacial cycles: A case study from the alpine primrose Primula marginata (Primulaceae)

BackgroundRecent studies highlighted the role of Pleistocene climatic cycles in polyploid speciation and of southern Alpine refugia as reservoirs of diversity during glacial maxima. The polyploid Primula marginata, endemic to the southwestern Alps, includes both hexaploid and dodecaploid cytotypes that show no ecological or morphological differences. We used flow cytometry to determine variation and geographic distribution of cytotypes within and between populations and analyses of chloroplast (cp) and nuclear ribosomal (nr) DNA sequences from the Internal Transcribed Spacer (ITS) region to infer the evolutionary history of the two cytotypes and the auto- vs. allopolyploid origin of dodecaploid populations.ResultsWe did not detect any intermediate cytotypes or variation of ploidy levels within populations. Hexaploids occur in the western and dodecaploids in the eastern part of the distributional range, respectively. The cpDNA and nrDNA topologies are in conflict, for the former supports shared ancestry between P. marginata and P. latifolia, while the latter implies common origins between at least some ITS clones of P. marginata and P. allionii.ConclusionsOur results suggest an initial episode of chloroplast capture involving ancestral lineages of P. latifolia and P. marginata, followed by polyploidization between P. marginata-like and P. allionii-like lineages in a southern refugium of the Maritime Alps. The higher proportion of ITS polymorphisms in dodecaploid than in hexaploid accessions of P. marginata and higher total nucleotide diversity of ITS clones in dodecaploid vs. hexaploid individuals sequences are congruent with the allopolyploid hypothesis of dodecaploid origin.

• Publication year

  2012

• Venue

  BMC Evolutionary Biology

• Publication date

  2012-04-24

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1186/1471-2148-12-56PMID 22530870PMCID 3444416
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

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  2012cited by this paper
• The stability of Quaternary speciation: a case study in Primula sect. Auricula

  2011cited by this paper
• Phenotypic consequences of polyploidy and genome size at the microevolutionary scale: a multivariate morphological approach.

  2011cited by this paper
• Ancestral polyploidy in seed plants and angiosperms

  2011cited by this paper
• Altered gene expression and ecological divergence in sibling allopolyploids of Dactylorhiza (Orchidaceae)

  2011cited by this paper
• Recently Formed Polyploid Plants Diversify at Lower Rates

  2011cited by this paper
• A molecular phylogenetic approach to western North America endemic Artemisia and allies (Asteraceae): untangling the sagebrushes.

  2011cited by this paper
• RDP3: a flexible and fast computer program for analyzing recombination

  2010influential reference
• Evolutionary dynamics across discontinuous freshwater systems: Rapid expansions and repeated allopolyploid origins in the Palearctic white water–lilies (Nymphaea)

  2010cited by this paper
• The evolutionary history of the Arabidopsis lyrata complex: a hybrid in the amphi-Beringian area closes a large distribution gap and builds up a genetic barrier

  2010cited by this paper
• Evolution of plant RNA polymerase IV/V genes: evidence of subneofunctionalization of duplicated NRPD2/NRPE2-like paralogs in Viola (Violaceae)

  2010cited by this paper
• Angiosperm polyploids and their road to evolutionary success

  2010cited by this paper
• Stable Epigenetic Effects Impact Adaptation in Allopolyploid Orchids (Dactylorhiza: Orchidaceae)

  2010cited by this paper
• Evolutionary consequences of autopolyploidy.

  2010cited by this paper
• Haplotype richness in refugial areas: phylogeographical structure of Saxifraga callosa

  2009cited by this paper
• Effects of Pleistocene glaciations on the genetic structure of Saxifraga florulenta (Saxifragaceae), a rare endemic of the Maritime Alps

  2009cited by this paper
• Polyploidy and angiosperm diversification.

  2009cited by this paper
• Disentangling reticulate evolution in an arctic-alpine polyploid complex.

  2009cited by this paper
• Reciprocal Pleistocene origin and postglacial range formation of an allopolyploid and its sympatric ancestors (Androsace adfinis group, Primulaceae).

  2009influential reference
• Genetic structure and evolution of Alpine polyploid complexes: Ranunculus kuepferi (Ranunculaceae) as a case study

  2009cited by this paper
• Intra-individual polymorphism in diploid and apomictic polyploid hawkweeds (Hieracium, Lactuceae, Asteraceae): disentangling phylogenetic signal, reticulation, and noise

  2009cited by this paper
• The frequency of polyploid speciation in vascular plants

  2009cited by this paper
• The role of hybridization in plant speciation.

  2009cited by this paper
• The polyploid series of Centaurea toletana: glacial migrations and introgression revealed by nrDNA and cpDNA sequence analyzes.

  2009cited by this paper
• An AFLP marker approach to lower-level systematics in Eucalyptus (Myrtaceae).

  2008cited by this paper
• Patterns of nucleotide variation and reproductive isolation between a Mimulus allotetraploid and its progenitor species

  2008cited by this paper
• Genomic origin and organization of the allopolyploid Primula egaliksensis investigated by in situ hybridization.

  2008cited by this paper
• Ecological and historical factors affecting distribution pattern and richness of endemic plant species: the case of the Maritime and Ligurian Alps hotspot

  2008influential reference
• AFLP trees versus scatterplots : evolution and phylogeography of the polyploid complex Achillea millefolium agg. (Asteraceae)

  2008cited by this paper
• Nuclear vs. plastid data: complex Pleistocene history of a circumpolar key species

  2007cited by this paper
• Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III.

  2007cited by this paper
• An Exact Nonparametric Method for Inferring Mosaic Structure in Sequence Triplets

  2007cited by this paper
• The importance of data partitioning and the utility of Bayes factors in Bayesian phylogenetics.

  2007cited by this paper
• Hybrid speciation

  2007cited by this paper
• Prediction of Protein-protein Interactions on the Basis of Evolutionary Conservation of Protein Functions

  2007cited by this paper
• Glacial in situ survival in the Western Alps and polytopic autopolyploidy in Biscutella laevigata L. (Brassicaceae)

  2007cited by this paper
• Untangling complex histories of genome mergings in high polyploids.

  2007cited by this paper
• Chromosomal variability in the genus Primula (Primulaceae)

  2006cited by this paper
• Evolution of biogeographic patterns, ploidy levels, and breeding systems in a diploid-polyploid species complex of Primula.

  2006cited by this paper
• Are any primroses (Primula) primitively monomorphic?

  2006cited by this paper
• A new scenario for the quaternary history of European beech populations: palaeobotanical evidence and genetic consequences.

  2006cited by this paper
• Natural hybridization in Saxifraga callosa Sm.

  2006cited by this paper
• Arlequin (version 3.0): An integrated software package for population genetics data analysis

  2005cited by this paper
• The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis.

  2005cited by this paper
• Molecular evidence for glacial refugia of mountain plants in the European Alps

  2005influential reference
• Geographic structure of molecular variation of Gentiana ligustica (Gentianaceae) in the Maritime and Ligurian regional hotspot, inferred from ITS sequences

  2005cited by this paper
• Ecological factors influencing tetraploid establishment in snow buttercups (Ranunculus adoneus , Ranunculaceae): minority cytotype exclusion and barriers to triploid formation.

  2005cited by this paper
• MrModeltest 2.2. Program Distributed by the Author

  2004cited by this paper
• MUSCLE: multiple sequence alignment with high accuracy and high throughput.

  2004influential reference
• Model selection and model averaging in phylogenetics: advantages of akaike information criterion and bayesian approaches over likelihood ratio tests.

  2004cited by this paper
• Polyploidy in arctic plants

  2004cited by this paper
• Isolation by distance and sharp discontinuities in gene frequencies: implications for the phylogeography of an alpine insect species, Carabus solieri

  2004influential reference
• Reconstructing patterns of reticulate evolution in plants.

  2004cited by this paper
• The Temporal Course of Quaternary Diversification in the European High Mountain Endemic Primula sect. Auricula (Primulaceae)

  2004influential reference
• Reconstructing patterns of reticulate evolution in plants.

  2004cited by this paper
• Intraspecific diversification in North American Boechera stricta (= Arabis drummondii), Boechera xdivaricarpa, and Boechera holboellii (Brassicaceae) inferred from nuclear and chloroplast molecular markers--an integrative approach.

  2004cited by this paper
• The importance of proper model assumption in bayesian phylogenetics.

  2004cited by this paper
• Advances in the study of polyploidy since Plant speciation

  2003cited by this paper
• GapCoder automates the use of indel characters in phylogenetic analysis

  2003cited by this paper
• MrBayes 3: Bayesian phylogenetic inference under mixed models

  2003cited by this paper
• Ribosomal ITS sequences and plant phylogenetic inference.

  2003influential reference
• Characterization of angiosperm nrDNA polymorphism, paralogy, and pseudogenes.

  2003cited by this paper
• Partitioned likelihood support and the evaluation of data set conflict.

  2003cited by this paper
• Additive polymorphisms and reticulation in an ITS phylogeny of thrifts (Armeria, Plumbaginaceae).

  2003cited by this paper
• History and evolution of the arctic flora: in the footsteps of Eric Hultén

  2003cited by this paper
• PREDICTING NUCLEAR GENE COALESCENCE FROM MITOCHONDRIAL DATA: THE THREE‐TIMES RULE

  2001cited by this paper
• Non-adaptive hypothesis of allopatric cytotype distribution inMyosotis lamottiana (Boraginaceae)

  2001cited by this paper
• Evaluation of methods for detecting recombination from DNA sequences: Computer simulations

  2001cited by this paper
• Bayesian selection of continuous-time Markov chain evolutionary models.

  2001cited by this paper
• Phylogenetic relationships and character evolution in Primula L.: The usefulness of ITS sequence data

  2000cited by this paper
• PAUP* Phylogenetic analysis using parsimony (*and other methods) Version 4

  2000cited by this paper
• Sister-Scanning: a Monte Carlo procedure for assessing signals in recombinant sequences

  2000cited by this paper
• Multiple origins of polyploidy and the geographic structure of Heuchera grossulariifolia

  1999cited by this paper
• Multiple Comparisons of Log-Likelihoods with Applications to Phylogenetic Inference

  1999cited by this paper
• Possible emergence of new geminiviruses by frequent recombination.

  1999cited by this paper
• Cytotype distribution at a diploid-tetraploid contact zone in Chamerion (Epilobium) angustifolium (Onagraceae).

  1998cited by this paper
• Biogeography and floral evolution of baobabs (Adansonia, Bombacaceae) as inferred from multiple data sets.

  1998cited by this paper
• PATHWAYS, MECHANISMS, AND RATES OF POLYPLOID FORMATION IN FLOWERING PLANTS

  1998cited by this paper
• Phylogenetic Incongruence: Window into Genome History and Molecular Evolution

  1998cited by this paper
• Chloroplast DNA phylogeography and cytotype geography in autopolyploid Plantago media

  1997cited by this paper
• Variation in flowering phenology and selfing rate across a contact zone between diploid and tetraploid Arrhenatherum elatius (Poaceae)

  1997influential reference
• Identification of Breakpoints in Intergenotypic Recombinants of HIV Type 1 by Bootscanning

  1995cited by this paper
• Surveys of Gene Families Using Polymerase Chain Reaction: PCR Selection and PCR Drift

  1994cited by this paper
• Molecular Markers, Natural History and Evolution

  1993cited by this paper
• Analyzing the mosaic structure of genes

  1992cited by this paper
• Gene Trees and Species Trees: Molecular Systematics as One-Character Taxonomy

  1992cited by this paper
• Molecular Systematics of Plants

  1992cited by this paper
• Inference from Iterative Simulation Using Multiple Sequences

  1992cited by this paper
• Ribosomal RNA as a Phylogenetic Tool in Plant Systematics

  1992cited by this paper
• SYN-TAX IV. Computer Programs for Data Analysis in Ecology and Systematics

  1991cited by this paper
• DAPI staining of fixed cells for high-resolution flow cytometry of nuclear DNA.

  1990cited by this paper
• SEGNALAZIONI FLORISTICHE ITALIANE

  1990cited by this paper
• CHLOROPLAST‐DNA VARIATION AND MULTIPLE ORIGINS OF AUTOPOLYPLOIDY IN HEUCHERA MICRANTHA (SAXIFRAGACEAE)

  1989cited by this paper
• Organelle gene diversity under migration, mutation, and drift: equilibrium expectations, approach to equilibrium, effects of heteroplasmic cells, and comparison to nuclear genes.

  1989cited by this paper
• SYN-TAX III-PC: computer programs for data analysis in ecology and systematics

  1989cited by this paper
• Polyploidy, hybridization, and the invasion of new habitats.

  1985cited by this paper
• Polyploidy and the distribution of the arctic-alpine flora: new evidence and a new approach

  1984cited by this paper
• Polyploidy and Novelty in Flowering Plants

  1983cited by this paper
• The neutral theory of molecular evolution.

  1983cited by this paper
• Evolutionary relationship of DNA sequences in finite populations.

  1983cited by this paper

• Co-occurring Luzula species (Juncaceae) of different ploidies exhibit weak ecological differentiation at local scale in alpine grasslands of the Eastern Alps

  2025cites this paper
• Out of Liguria: how polyploidy affected diversification of the sweet spurge (Euphorbia dulcis, Euphorbiaceae), European widespread forest species

  2025cites this paper
• Friends or foes? Polyploidy and competition in a grassland geophyte

  2025cites this paper
• Genome Size in the Arenaria ciliata Species Complex (Caryophyllaceae), with Special Focus on Northern Europe and the Arctic

  2024cites this paper
• Meeting in Liguria: hybridisation between Apennine endemic Euphorbia barrelieri and western Mediterranean E. nicaeensis led to the allopolyploid origin of E. ligustica.

  2023cites this paper
• Genus Primula and its role in Phytomedicine; a systematic review

  2023cites this paper
• Comparative analysis of chloroplast genomes of endangered heterostylous species Primula wilsonii and its closely related species

  2023cites this paper
• Introgression of an isolated Primula lineage suggests the existence of a glacial refugium in the Écrins range (Southwestern French Alps)

  2022cites this paper
• The Complete Chloroplast Genomes of Primula obconica Provide Insight That Neither Species nor Natural Section Represent Monophyletic Taxa in Primula (Primulaceae)

  2022cites this paper
• Biogeographic patterns of polyploid species for the angiosperm flora in China

  2022cites this paper
• Signatures of selection in recently domesticated macadamia

  2022cites this paper
• Asymmetries of reproductive isolation are reflected in directionalities of hybridization: Integrative evidence on the complexity of species boundaries.

  2020cites this paper
• Tracking the evolutionary history of the Allium ampeloprasum L. complex (section Allium) provides evidence of the contribution of North African diploids to the formation of allopolyploid horticultural groups

  2020cites this paper
• Diversification and distribution patterns of Luzula sect. Luzula (Juncaceae) in the Eastern Alps: a cytogenetic approach combined with extensive herbarium revisions

  2019cites this paper
• Does geography, evolutionary history or ecology drive ploidy and genome size variation in the Minuartia verna group (Caryophyllaceae) across Europe?

  2019cites this paper
• Polyploid Arabidopsis species originated around recent glaciation maxima.

  2018cites this paper
• Variability and evolutionary implications of repetitive DNA dynamics in genome of Astyanax scabripinnis (Teleostei, Characidae)

  2017cites this paper
• Do floral and niche shifts favour the establishment and persistence of newly arisen polyploids? A case study in an Alpine primrose

  2017cites this paper
• Frozen ploidies: a phylogeographical analysis of the Leucanthemopsis alpina polyploid complex (Asteraceae, Anthemideae)

  2017influential citation
• Are the responses of plant species to Quaternary climatic changes idiosyncratic? A demographic perspective from the Western Alps

  2017cites this paper
• Are species’ responses to Quaternary climatic changes idiosyncratic? A demographic perspective from the Western Alps

  2017cites this paper
• Anderson's and Stebbins' Prophecy Comes True: Genetic Exchange in Fluctuating Environments

  2016cites this paper
• Sequence capture using RAD probes clarifies phylogenetic relationships and species boundaries in Primula sect. Auricula.

  2016cites this paper
• Allopatric speciation with little niche divergence is common among alpine Primulaceae

  2016cites this paper
• Polyploidy and high mountain environments. Evolutionary processes at different scales in the subtribe Leucanthemopsidinae (Compositae, Anthemideae)

  2016influential citation
• The plant endemism in the Maritime and Ligurian Alps

  2016influential citation
• Polyploidisation and Geographic Differentiation Drive Diversification in a European High Mountain Plant Group (Doronicum clusii Aggregate, Asteraceae)

  2015cites this paper
• Phylogenomics of polyploid Fothergilla (Hamamelidaceae) by RAD‐tag based GBS—insights into species origin and effects of software pipelines

  2015cites this paper
• Reconstructing reticulate relationships in the polyploid complex of Leucanthemum Mill. (Compositae, Anthemideae)

  2015cites this paper
• Cytotype distribution and phylogeography of Hieracium intybaceum (Asteraceae)

  2015cites this paper
• Phylogeny and biogeography of Primula sect. Armerina: implications for plant evolution under climate change and the uplift of the Qinghai-Tibet Plateau

  2015cites this paper
• Reproducing under a warming climate: long winter flowering and extended flower longevity in the only Mediterranean and maritime Primula.

  2015cites this paper
• The draft genome of Primula veris yields insights into the molecular basis of heterostyly

  2015cites this paper
• Phylogeography of the Qinghai–Tibet Plateau endemic alpine herb Pomatosace filicula (Primulaceae)

  2014influential citation
• Species distinction within Campanula sect. Heterophylla in the SW Alps: Molecular, morphological and chemotaxonomic evidences

  2014cites this paper
• Allopolyploid origin of the Balkan endemic Ranunculus wettsteinii (Ranunculaceae) inferred from nuclear and plastid DNA sequences

  2014cites this paper
• Pollination ecology in the narrow endemic winter-flowering Primula allionii (Primulaceae)

  2013cites this paper
• Combining palaeodistribution modelling and phylogeographical approaches for identifying glacial refugia in Alpine Primula

  2013cites this paper
• Distribution range and ecological niche of Primula marginata Curtis (Primulaceae)

  2013cites this paper
• When polyploidy and hybridization produce a fuzzy taxon: the complex origin of the insular neoendemic Neotinea commutata (Orchidaceae)

  2013cites this paper
• Phylogeography of Primula allionii (Primulaceae), a narrow endemic of the Maritime Alps

  2013influential citation
• Indehiscent sporangia enable the accumulation of local fern diversity at the Qinghai-Tibetan Plateau

  2012cites this paper