Reticulate evolution in glacial refuge areas : the genus Arabidopsis in the eastern Austrian Danube Valley (Wachau)

Hybridisierung und Polyploidisierung tragen wesentlich zur Artbildung im Pflanzenreich bei. Innerhalb der Gattung Arabidopsis ist Hybridisierung nur von Arabidopsis suecica aus Fennoskandinavien und Arabidopsis kamchatica aus Japan bekannt. Diese Studie befasst sich mit den Artkomplexen von Arabidopsis lyrata und Arabidopsis arenosa. Unser Ziel war es, herauszufinden, ob und in welchem Ausmaß Hybridisierung an der Artbildung beteiligt war, und ob Polyploidisierung durch Selbstverdopplung des Genoms stattfand. Zudem waren wir an der evolutionären Historie von Di- und Tetraploiden der beiden Artkomplexe interessiert. Wir näherten uns der Lösung dieser Fragestellungen sowohl auf weltweiter Ebene der Gesamtverbreitungsareale beider Artkomplexe als auch auf regionaler Ebene einer mitteleuropäischen Kontaktzone. Im ersten Kapitel „Amphi-beringische, allopolyploide Arabidopsis und die evolutionäre Historie des Arabidopsis lyrata Komplexes“ charakterisierten wir drei genetische Hauptlinien, eine eurasiatische, nordamerikanische und amphi-pazifische, mit den molekularen Markern ntDNA ITS, ntDNA PgiC und cpDNA trnL/F. Allopolyploidisierung zwischen eurasiatischer Arabidopsis lyrata ssp. petraea und ostasiatischer Arabidopsis halleri ssp. gemmifera in der amphi-pazifischen Linie ereignete sich dreimal unabhängig voneinander in Japan, China und Kamtschatka. Wir identifizierten die unvergletscherten Bereiche der ostösterreichischen Alpen und das arktische Eurasien einschließlich Beringias als eiszeitliche Hauptrefugialgebiete der eurasiatischen Linie. Die nordamerikanische Linie überdauerte die Vereisungen im Südosten Nordamerikas. Genfluss zwischen der eurasiatischen und nordamerikanischen Linie fand wahrscheinlich sowohl zwischen den Perioden der Vergletscherung als auch nach der letzten Vereisung statt. Im zweiten Kapitel „Autopolyploidisierung in Arabidopsis und die evolutionäre Historie des Arabidopsis arenosa Komplexes“ fanden wir das Zentrum der Artbildung innerhalb des Arabidopsis arenosa Komplexes auf der Balkanhalbinsel und in den Karpaten mit vorwiegend diploiden neben vereinzelten tetraploiden Populationen. Polyploidisierung erfolgte durch Selbstverdopplung des Genoms. Sowohl die unvergletscherten ostösterreichischen Alpen als auch die Westkarpaten dienten als pleistozäne Refugialgebiete, was anhand des molekularen Markers cpDNA trnL/F ermittelt wurde. Diese beiden Gebirgsstöcke wurden von Arabidopsis arenosa einst unabhängig voneinander von der Balkanhalbinsel aus kolonisiert. Im dritten Kapitel „Retikulate Evolution in eiszeitlichen Refugialgebieten – die Gattung Arabidopsis im ostösterreichischen Donautal (Wachau)“ fanden wir rezente Introgression von Arabidopsis arenosa in Arabidopsis lyrata ssp. petraea in zwei Hybridzonen, eine in der nördlichen Wachau, die andere am Fuße der Ostalpen. In diesen beiden Gebieten liegen die Populationen beider Arten nahe beieinander, was zur Annahme von aktuellem Genfluss zwischen ihnen führte. Die Hybridzone in der nördlichen Wachau wurde sowohl mit molekularen Markern (cpDNA trnL/F Sequenzdaten und sieben Mikrosatelliten) als auch morphologischen Daten charakterisiert. Die Hybridzone am Fuße der Ostalpen wurde mit Hilfe von Mikrosatelliten entdeckt. Tetraploide, besonders von Arabidopsis lyrata ssp. petraea, zeigten stark erhöhte geno- und phänotypische Plastizität im Gegensatz zu Diploiden. Polyploidisierung innerhalb von Arabidopsis arenosa und Arabidopsis lyrata ssp. petraea fand vermutlich durch Selbstverdopplung des Genoms statt

The evolutionary history of the Arabidopsis arenosa complex : diverse tetraploids mask the Western Carpathian center of species and genetic diversity

The Arabidopsis arenosa complex is closely related to the model plant Arabidopsis thaliana. Species and subspecies in the complex are mainly biennial, predominantly outcrossing, herbaceous, and with a distribution range covering most parts of latitudes and the eastern reaches of Europe. In this study we present the first comprehensive evolutionary history of the A. arenosa species complex, covering its natural range, by using chromosome counts, nuclear AFLP data, and a maternally inherited marker from the chloroplast genome [trnL intron (trnL) and trnL/F intergenic spacer (trnL/F-IGS) of tRNALeu and tRNAPhe, respectively]. We unravel the broad-scale cytogeographic and phylogeographic patterns of diploids and tetraploids. Diploid cytotypes were exclusively found on the Balkan Peninsula and in the Carpathians while tetraploid cytotypes were found throughout the remaining distribution range of the A. arenosa complex. Three centers of genetic diversity were identified: the Balkan Peninsula, the Carpathians, and the unglaciated Eastern and Southeastern Alps. All three could have served as long-term refugia during Pleistocene climate oscillations. We hypothesize that the Western Carpathians were and still are the cradle of speciation within the A. arenosa complex due to the high species number and genetic diversity and the concurrence of both cytotypes there

Adaptive introgression: how polyploidy reshapes gene flow landscapes

© 2021 The Authors. New Phytologist © 2021 New Phytologist Foundation Rare yet accumulating evidence in both plants and animals shows that whole genome duplication (WGD, leading to polyploidy) can break down reproductive barriers, facilitating gene flow between otherwise isolated species. Recent population genomic studies in wild, outcrossing Arabidopsis arenosa and Arabidopsis lyrata indicate that this WGD-potentiated gene flow can be adaptive and highly specific in response to particular environmental and intracellular challenges. The mechanistic basis of WGD-mediated easing of species barrier strength seems to primarily lie in the relative dosage of each parental genome in the endosperm. While generalisations about polyploids can be fraught, this evidence indicates that the breakdown of these barriers, combined with diploid to polyploid gene flow and gene flow between polyploids, allows some polyploids to act as adaptable ‘allelic sponges’, enjoying increased potential to respond to challenging environments

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

<p>Abstract</p> <p>Background</p> <p>The genomes of higher plants are, on the majority, polyploid, and hybridisation is more frequent in plants than in animals. Both polyploidisation and hybridisation contribute to increased variability within species, and may transfer adaptations between species in a changing environment. Studying these aspects of evolution within a diversified species complex could help to clarify overall spatial and temporal patterns of plant speciation. The <it>Arabidopsis lyrata </it>complex, which is closely related to the model plant <it>Arabidopsis thaliana</it>, is a perennial, outcrossing, herbaceous species complex with a circumpolar distribution in the Northern Hemisphere as well as a disjunct Central European distribution in relictual habitats. This species complex comprises three species and four subspecies, mainly diploids but also several tetraploids, including one natural hybrid. The complex is ecologically, but not fully geographically, separated from members of the closely related species complex of <it>Arabidopsis halleri</it>, and the evolutionary histories of both species compexes have largely been influenced by Pleistocene climate oscillations.</p> <p>Results</p> <p>Using DNA sequence data from the nuclear encoded cytosolic phosphoglucoisomerase and Internal Transcribed Spacers 1 and 2 of the ribosomal DNA, as well as the <it>trn</it>L/F region from the chloroplast genome, we unravelled the phylogeography of the various taxonomic units of the <it>A. lyrata </it>complex. We demonstrate the existence of two major gene pools in Central Europe and Northern America. These two major gene pools are constructed from different taxonomic units. We also confirmed that <it>A. kamchatica </it>is the allotetraploid hybrid between <it>A. lyrata </it>and <it>A. halleri</it>, occupying the amphi-Beringian area in Eastern Asia and Northern America. This species closes the large distribution gap of the various other <it>A. lyrata </it>segregates. Furthermore, we revealed a threefold independent allopolyploid origin of this hybrid species in Japan, China, and Kamchatka.</p> <p>Conclusions</p> <p>Unglaciated parts of the Eastern Austrian Alps and arctic Eurasia, including Beringia, served as major glacial refugia of the Eurasian <it>A. lyrata </it>lineage, whereas <it>A. halleri </it>and its various subspecies probably survived in refuges in Central Europe and Eastern Asia with a large distribution gap in between. The North American <it>A. lyrata </it>lineage probably survived the glaciation in the southeast of North America. The dramatic climatic changes during glaciation and deglaciation cycles promoted not only secondary contact and formation of the allopolyploid hybrid <it>A. kamchatica</it>, but also provided the environment that allowed this species to fill a large geographic gap separating the two genetically different <it>A. lyrata </it>lineages from Eurasia and North America. With our example focusing on the evolutionary history of the <it>A. lyrata </it>species complex, we add substantial information to a broad evolutionary framework for future investigations within this emerging model system in molecular and evolutionary biology.</p

Interspecific and interploidal gene flow in Central European Arabidopsis (Brassicaceae)

Background Effects of polyploidisation on gene flow between natural populations are little known. Central European diploid and tetraploid populations of Arabidopsis arenosa and A. lyrata are here used to study interspecific and interploidal gene flow, using a combination of nuclear and plastid markers. Results Ploidal levels were confirmed by flow cytometry. Network analyses clearly separated diploids according to species. Tetraploids and diploids were highly intermingled within species, and some tetraploids intermingled with the other species, as well. Isolation with migration analyses suggested interspecific introgression from tetraploid A. arenosa to tetraploid A. lyrata and vice versa, and some interploidal gene flow, which was unidirectional from diploid to tetraploid in A. arenosa and bidirectional in A. lyrata. Conclusions Interspecific genetic isolation at diploid level combined with introgression at tetraploid level indicates that polyploidy may buffer against negative consequences of interspecific hybridisation. The role of introgression in polyploid systems may, however, differ between plant species, and even within the small genus Arabidopsis, we find very different evolutionary fates when it comes to introgression

De Novo Mutation and Rapid Protein (Co-)evolution during Meiotic Adaptation in Arabidopsis arenosa

A sudden shift in environment or cellular context necessitates rapid adaptation. A dramatic example is genome duplication, which leads to polyploidy. In such situations, the waiting time for new mutations might be prohibitive; theoretical and empirical studies suggest that rapid adaptation will largely rely on standing variation already present in source populations. Here, we investigate the evolution of meiosis proteins in Arabidopsis arenosa, some of which were previously implicated in adaptation to polyploidy, and in a diploid, habitat. A striking and unexplained feature of prior results was the large number of amino acid changes in multiple interacting proteins, especially in the relatively young tetraploid. Here, we investigate whether selection on meiosis genes is found in other lineages, how the polyploid may have accumulated so many differences, and whether derived variants were selected from standing variation. We use a range-wide sample of 145 resequenced genomes of diploid and tetraploid A. arenosa, with new genome assemblies. We confirmed signals of positive selection in the polyploid and diploid lineages they were previously reported in and find additional meiosis genes with evidence of selection. We show that the polyploid lineage stands out both qualitatively and quantitatively. Compared with diploids, meiosis proteins in the polyploid have more amino acid changes and a higher proportion affecting more strongly conserved sites. We find evidence that in tetraploids, positive selection may have commonly acted on de novo mutations. Several tests provide hints that coevolution, and in some cases, multinucleotide mutations, might contribute to rapid accumulation of changes in meiotic proteins

Hyb-Seq: Combining target enrichment and genome skimming for plant phylogenomics

PREMISE OF THE STUDY: Hyb-Seq, the combination of target enrichment and genome skimming allows simultaneous data collection for low-copy nuclear genes and high-copy genomic targets for plant systematics and evolution studies. METHODS AND RESULTS: Genome and transcriptome assemblies for milkweed (Asclepias syriaca) were utilized to design enrichment probes for 3385 exons from 768 genes (>1.6 Mbp) followed by Illumina sequencing of enriched libraries. Hyb-Seq of twelve individuals (ten Asclepias species and two related genera) resulted in at least partial assembly of 92.6% of exons and 99.7% of genes and an average assembly length >2 Mbp. Importantly, complete plastomes and nrDNA cistrons were assembled using off-target reads. Phylogenomic analyses demonstrated signal conflict between genomes. CONCLUSIONS: The Hyb-Seq approach enables targeted sequencing of thousands of low-copy nuclear exons and flanking regions, as well as genome skimming of high-copy repeats and organellar genomes, to efficiently produce genome-scale datasets for phylogenomics.This is an author's peer-reviewed final manuscript, as accepted by the publisher. The article is in press and will be published in Applications in Plant Sciences, Vol. 2, no. 9, September 2014.Keywords: Genome skimming, Hyb-Seq, Target enrichment, Phylogenomics, Species tree, Nuclear lociKeywords: Genome skimming, Hyb-Seq, Target enrichment, Phylogenomics, Species tree, Nuclear loc

Phylogenetic marker development for target enrichment from transcriptome and genome skim data: the pipeline and its application in southern African Oxalis (Oxalidaceae)

Phylogenetics benefits from using a large number of putatively independent nuclear loci and their combination with other sources of information, such as the plastid and mitochondrial genomes. To facilitate the selection of orthologous low‐copy nuclear (LCN) loci for phylogenetics in nonmodel organisms, we created an automated and interactive script to select hundreds of LCN loci by a comparison between transcriptome and genome skim data. We used our script to obtain LCN genes for southern African Oxalis (Oxalidaceae), a speciose plant lineage in the Greater Cape Floristic Region. This resulted in 1164 LCN genes greater than 600 bp. Using target enrichment combined with genome skimming (Hyb‐Seq), we obtained on average 1141 LCN loci, nearly the whole plastid genome and the nrDNA cistron from 23 southern African Oxalis species. Despite a wide range of gene trees, the phylogeny based on the LCN genes was very robust, as retrieved through various gene and species tree reconstruction methods as well as concatenation. Cytonuclear discordance was strong. This indicates that organellar phylogenies alone are unlikely to represent the species tree and stresses the utility of Hyb‐Seq in phylogenetics

Repeatedly Northwards and Upwards: Southern African Grasslands Fuel the Colonization of the African Sky Islands in Helichrysum (Compositae)

The Afromontane and Afroalpine areas constitute some of the main biodiversity hotspots of Africa. They are particularly rich in plant endemics, but the biogeographic origins and evolutionary processes leading to this outstanding diversity are poorly understood. We performed phylogenomic and biogeographic analyses of one of the most species-rich plant genera in these mountains, Helichrysum (Compositae-Gnaphalieae). Most previous studies have focused on Afroalpine elements of Eurasian origin, and the southern African origin of Helichrysum provides an interesting counterexample. We obtained a comprehensive nuclear dataset from 304 species (≈50% of the genus) using target-enrichment with the Compositae1061 probe set. Summary-coalescent and concatenation approaches combined with paralog recovery yielded congruent, well-resolved phylogenies. Ancestral range estimations revealed that Helichrysum originated in arid southern Africa, whereas the southern African grasslands were the source of most lineages that dispersed within and outside Africa. Colonization of the tropical Afromontane and Afroalpine areas occurred repeatedly throughout the Miocene-Pliocene. This timing coincides with mountain uplift and the onset of glacial cycles, which together may have facilitated both speciation and intermountain gene flow, contributing to the evolution of the Afroalpine flora.This work received financial support from the Spanish Ministry of Science, Innovation and Universities (PID2019-105583GB-C22/AEI/10.13039/501100011033) and the Catalan government (“Ajuts a grups consolidats” 2021SGR00315 and FI grant to C.B.-G. 2022FI_B 00150). The Ph.D. thesis was carried out under the Ph.D. program “Plant Biology and Biotechnology” of the Autonomous University of Barcelona (UAB). Additional support was provided by the Czech Science Foundation GAČR project no. 20-10878S to R.S. and F.K. and long-term research development project (RVO 67985939) of the Czech Academy of Sciences. Additional funds were obtained from the Norwegian Programme for Development, Research and Higher Education (NUFU; project AFROALP-II, no 2007/1058) and the Research Council of Norway (project SpeciationClock, no 274607) to C.B.Abstract 1. Introduction 2. Materials and Methods 2.1. Taxon Sampling 2.2. DNA Extraction, Library Preparation, Target Capture, and Sequencing 2.3. Molecular Data Processing and Phylogenetic Analyses 2.4. Divergence Time Estimation 2.5. Ancestral Range Estimation 3. Results 3.1. Alignment Processing and Filtering 3.2. Phylogenetic Analyses 3.3. Divergence Time and Ancestral Range Estimation 3.4. Number, Type, and Directionality Estimation of Biogeographical Events 4. Discussion 4.1. Utility of Target-Enrichment Strategies in Reconstructing the Radiation of Helichrysum 4.2. The Early History of Helichrysum and Colonization of Madagascar 4.3. Repeatedly Northwards 4.4. Repeatedly Upwards 5. Conclusions Supplementary Materials Author Contributions Funding Data Availability Statement Acknowledgments Conflicts of Interest Reference