Polyploidy, the result of whole genome duplication (WGD), is widespread across the tree of life and is often associated with speciation and adaptability. It is thought that adaptation in autopolyploids (within-species polyploids) may be facilitated by increased access to genetic variation. This variation may be sourced from gene flow with sister diploids and new access to other tetraploid lineages, as well as from increased mutational targets provided by doubled DNA content. Here, we deconstruct in detail the origins of haplotypes displaying the strongest selection signals in established, successful autopolyploids, Arabidopsis lyrata and Arabidopsis arenosa. We see strong signatures of selection in 17 genes implied in meiosis, cell cycle, and transcription across all four autotetraploid lineages present in our expanded sampling of 983 sequenced genomes. Most prominent in our results is the finding that the tetraploid-characteristic haplotypes with the most robust signals of selection were completely absent in all diploid sisters. In contrast, the fine-scaled variant 'mosaics' in the tetraploids originated from highly diverse evolutionary sources. These include widespread novel reassortments of trans-specific polymorphism from diploids, new mutations, and tetraploid-specific inter-species hybridization-a pattern that is in line with the broad-scale acquisition and reshuffling of potentially adaptive variation in tetraploids.

• MeSH
• Arabidopsis * genetika   MeSH
• diploidie MeSH
• genetická variace MeSH
• genom rostlinný MeSH
• haplotypy * genetika   MeSH
• meióza genetika   MeSH
• molekulární evoluce MeSH
• polyploidie * MeSH
• selekce (genetika) genetika   MeSH
• tetraploidie MeSH
• Publikační typ
• časopisecké články MeSH

BACKGROUND: Whole-genome duplication (polyploidization) is a dominant force in sympatric speciation, particularly in plants. Genome doubling instantly poses a barrier to gene flow owing to the strong crossing incompatibilities between individuals differing in ploidy. The strength of the barrier, however, varies from species to species and recent genetic investigations revealed cases of rampant interploidy introgression in multiple ploidy-variable species. SCOPE: Here, we review novel insights into the frequency of interploidy gene flow in natural systems and summarize the underlying mechanisms promoting interploidy gene flow. Field surveys, occasionally complemented by crossing experiments, suggest frequent opportunities for interploidy gene flow, particularly in the direction from diploid to tetraploid, and between (higher) polyploids. However, a scarcity of accompanying population genetic evidence and a virtual lack of integration of these approaches leave the underlying mechanisms and levels of realized interploidy gene flow in nature largely unknown. Finally, we discuss potential consequences of interploidy genome permeability on polyploid speciation and adaptation and highlight novel avenues that have just recently been opened by the very first genomic studies of ploidy-variable species. Standing in stark contrast with rapidly accumulating evidence for evolutionary importance of homoploid introgression, similar cases in ploidy-variable systems are yet to be documented. CONCLUSIONS: The genomics era provides novel opportunity to re-evaluate the role of interploidy introgression in speciation and adaptation. To achieve this goal, interdisciplinary studies bordering ecology and population genetics and genomics are needed.

• Klíčová slova
• Adaptation, evolution, genetic introgression, polyploidy, speciation, whole-genome duplication,
• MeSH
• biologická evoluce MeSH
• genom rostlinný genetika   MeSH
• ploidie MeSH
• polyploidie * MeSH
• rostliny genetika   MeSH
• rozmnožování genetika   MeSH
• tok genů * MeSH
• vznik druhů (genetika) MeSH
• Publikační typ
• časopisecké články MeSH
• přehledy MeSH

Introgression allows polyploid species to acquire new genomic content from diploid progenitors or from other unrelated diploid or polyploid lineages, contributing to genetic diversity and facilitating adaptive allele discovery. In some cases, high levels of introgression elicit the replacement of large numbers of alleles inherited from the polyploid's ancestral species, profoundly reshaping the polyploid's genomic composition. In such complex polyploids, it is often difficult to determine which taxa were the progenitor species and which taxa provided additional introgressive blocks through subsequent hybridization. Here, we use population-level genomic data to reconstruct the phylogenetic history of Betula pubescens (downy birch), a tetraploid species often assumed to be of allopolyploid origin and which is known to hybridize with at least four other birch species. This was achieved by modeling polyploidization and introgression events under the multispecies coalescent and then using an approximate Bayesian computation rejection algorithm to evaluate and compare competing polyploidization models. We provide evidence that B. pubescens is the outcome of an autoploid genome doubling event in the common ancestor of B. pendula and its extant sister species, B. platyphylla, that took place approximately 178,000-188,000 generations ago. Extensive hybridization with B. pendula, B. nana, and B. humilis followed in the aftermath of autopolyploidization, with the relative contribution of each of these species to the B. pubescens genome varying markedly across the species' range. Functional analysis of B. pubescens loci containing alleles introgressed from B. nana identified multiple genes involved in climate adaptation, while loci containing alleles derived from B. humilis revealed several genes involved in the regulation of meiotic stability and pollen viability in plant species.

• Klíčová slova
• Allopolyploidy, Betula, autopolyploidy, gene flow, genomic polarization, homoeologs, interploidal, introgressive hybridization, polyploid phylogenetics, polyploidization simulation, reticulate evolution,
• MeSH
• alely * MeSH
• bříza * genetika   klasifikace   MeSH
• fylogeneze * MeSH
• genom rostlinný * MeSH
• genová introgrese MeSH
• hybridizace genetická MeSH
• polyploidie * MeSH
• Publikační typ
• časopisecké články MeSH

Deserts exert strong selection pressures on plants, but the underlying genomic drivers of ecological adaptation and subsequent speciation remain largely unknown. Here, we generated de novo genome assemblies and conducted population genomic analyses of the psammophytic genus Pugionium (Brassicaceae). Our results indicated that this bispecific genus had undergone an allopolyploid event, and the two parental genomes were derived from two ancestral lineages with different chromosome numbers and structures. The postpolyploid expansion of gene families related to abiotic stress responses and lignin biosynthesis facilitated environmental adaptations of the genus to desert habitats. Population genomic analyses of both species further revealed their recent divergence with continuous gene flow, and the most divergent regions were found to be centered on three highly structurally reshuffled chromosomes. Genes under selection in these regions, which were mainly located in one of the two subgenomes, contributed greatly to the interspecific divergence in microhabitat adaptation.

• Klíčová slova
• chromosomal structural variation, desert plants, microhabitat divergence, polyploidization,
• MeSH
• Brassicaceae klasifikace   genetika   fyziologie   MeSH
• ekosystém * MeSH
• fylogeneze MeSH
• fyziologická adaptace genetika   MeSH
• genom rostlinný * MeSH
• polyploidie MeSH
• vznik druhů (genetika) * MeSH
• Publikační typ
• časopisecké články MeSH
• práce podpořená grantem MeSH

Whole genome duplication (WGD) can promote adaptation but is disruptive to conserved processes, especially meiosis. Studies in Arabidopsis arenosa revealed a coordinated evolutionary response to WGD involving interacting proteins controlling meiotic crossovers, which are minimized in an autotetraploid (within-species polyploid) to avoid missegregation. Here, we test whether this surprising flexibility of a conserved essential process, meiosis, is recapitulated in an independent WGD system, Cardamine amara, 17 My diverged from A. arenosa. We assess meiotic stability and perform population-based scans for positive selection, contrasting the genomic response to WGD in C. amara with that of A. arenosa. We found in C. amara the strongest selection signals at genes with predicted functions thought important to adaptation to WGD: meiosis, chromosome remodeling, cell cycle, and ion transport. However, genomic responses to WGD in the two species differ: minimal ortholog-level convergence emerged, with none of the meiosis genes found in A. arenosa exhibiting strong signal in C. amara. This is consistent with our observations of lower meiotic stability and occasional clonal spreading in diploid C. amara, suggesting that nascent C. amara autotetraploid lineages were preadapted by their diploid lifestyle to survive while enduring reduced meiotic fidelity. However, in contrast to a lack of ortholog convergence, we see process-level and network convergence in DNA management, chromosome organization, stress signaling, and ion homeostasis processes. This gives the first insight into the salient adaptations required to meet the challenges of a WGD state and shows that autopolyploids can utilize multiple evolutionary trajectories to adapt to WGD.

• Klíčová slova
• adaptation, convergence, genome duplication, polyploidy,
• MeSH
• Arabidopsis * genetika   MeSH
• duplikace genu * MeSH
• genom rostlinný MeSH
• meióza genetika   MeSH
• polyploidie MeSH
• segregace chromozomů MeSH
• Publikační typ
• časopisecké články MeSH
• práce podpořená grantem MeSH

Relative contributions of pre-existing vs de novo genomic variation to adaptation are poorly understood, especially in polyploid organisms. We assess this in high resolution using autotetraploid Arabidopsis arenosa, which repeatedly adapted to toxic serpentine soils that exhibit skewed elemental profiles. Leveraging a fivefold replicated serpentine invasion, we assess selection on SNPs and structural variants (TEs) in 78 resequenced individuals and discover significant parallelism in candidate genes involved in ion homeostasis. We further model parallel selection and infer repeated sweeps on a shared pool of variants in nearly all these loci, supporting theoretical expectations. A single striking exception is represented by TWO PORE CHANNEL 1, which exhibits convergent evolution from independent de novo mutations at an identical, otherwise conserved site at the calcium channel selectivity gate. Taken together, this suggests that polyploid populations can rapidly adapt to environmental extremes, calling on both pre-existing variation and novel polymorphisms.

• MeSH
• alely * MeSH
• Arabidopsis účinky léků   genetika   MeSH
• fyziologická adaptace účinky léků   genetika   MeSH
• genom rostlinný * MeSH
• jednonukleotidový polymorfismus MeSH
• mutace MeSH
• polyploidie * MeSH
• proteiny huseníčku genetika   metabolismus   MeSH
• půda chemie   MeSH
• sekologanin-tryptaminové alkaloidy metabolismus   MeSH
• vápníkové kanály metabolismus   MeSH
• Publikační typ
• časopisecké články MeSH
• práce podpořená grantem MeSH
• Názvy látek
• proteiny huseníčku MeSH
• půda MeSH
• sekologanin-tryptaminové alkaloidy MeSH
• serpentine (alkaloid) MeSH Prohlížeč
• TPC1 protein, Arabidopsis MeSH Prohlížeč
• vápníkové kanály MeSH

Parallel adaptation provides valuable insight into the predictability of evolutionary change through replicated natural experiments. A steadily increasing number of studies have demonstrated genomic parallelism, yet the magnitude of this parallelism varies depending on whether populations, species, or genera are compared. This led us to hypothesize that the magnitude of genomic parallelism scales with genetic divergence between lineages, but whether this is the case and the underlying evolutionary processes remain unknown. Here, we resequenced seven parallel lineages of two Arabidopsis species, which repeatedly adapted to challenging alpine environments. By combining genome-wide divergence scans with model-based approaches, we detected a suite of 151 genes that show parallel signatures of positive selection associated with alpine colonization, involved in response to cold, high radiation, short season, herbivores, and pathogens. We complemented these parallel candidates with published gene lists from five additional alpine Brassicaceae and tested our hypothesis on a broad scale spanning ∼0.02 to 18 My of divergence. Indeed, we found quantitatively variable genomic parallelism whose extent significantly decreased with increasing divergence between the compared lineages. We further modeled parallel evolution over the Arabidopsis candidate genes and showed that a decreasing probability of repeated selection on the same standing or introgressed alleles drives the observed pattern of divergence-dependent parallelism. We therefore conclude that genetic divergence between populations, species, and genera, affecting the pool of shared variants, is an important factor in the predictability of genome evolution.

• Klíčová slova
• Arabidopsis, alpine adaptation, evolution, genomics, parallelism,
• MeSH
• anotace sekvence MeSH
• Arabidopsis klasifikace   genetika   metabolismus   účinky záření   MeSH
• biologická evoluce * MeSH
• býložravci fyziologie   MeSH
• fyziologická adaptace genetika   MeSH
• fyziologický stres MeSH
• genetická variace * MeSH
• genetický drift MeSH
• genom rostlinný * MeSH
• genová introgrese MeSH
• genová ontologie MeSH
• ionizující záření MeSH
• modely genetické MeSH
• nízká teplota MeSH
• rostlinné proteiny genetika   metabolismus   MeSH
• zvířata MeSH
• Check Tag
• zvířata MeSH
• Publikační typ
• časopisecké články MeSH
• práce podpořená grantem MeSH
• Názvy látek
• rostlinné proteiny MeSH

Hybridization is a creative evolutionary force, increasing genomic diversity and facilitating adaptation and even speciation. Hybrids often face significant challenges to establishment, including reduced fertility that arises from genomic incompatibilities between their parents. Whole-genome duplication in hybrids (allopolyploidy) can restore fertility, cause immediate phenotypic changes, and generate reproductive isolation. Yet the survival of polyploid lineages is uncertain, and few studies have compared the performance of recently formed allopolyploids and their parents under field conditions. Here, we use natural and synthetically produced hybrid and polyploid monkeyflowers (Mimulus spp.) to study how polyploidy contributes to the fertility, reproductive isolation, phenotype, and performance of hybrids in the field. We find that polyploidization restores fertility and that allopolyploids are reproductively isolated from their parents. The phenotype of allopolyploids displays the classic gigas effect of whole-genome duplication, in which plants have larger organs and are slower to flower. Field experiments indicate that survival of synthetic hybrids before and after polyploidization is intermediate between that of the parents, whereas natural hybrids have higher survival than all other taxa. We conclude that hybridization and polyploidy can act as sources of genomic novelty, but adaptive evolution is key in mediating the establishment of young allopolyploid lineages.

• Klíčová slova
• Erythranthe, Mimulus, allopolyploid, polyploidy, speciation, whole-genome duplication,
• MeSH
• duplikace genu * MeSH
• fenotyp MeSH
• fertilita genetika   MeSH
• genom rostlinný * MeSH
• hybridizace genetická * MeSH
• Mimulus genetika   MeSH
• molekulární evoluce * MeSH
• polyploidie * MeSH
• reprodukční izolace MeSH
• Publikační typ
• časopisecké články MeSH
• práce podpořená grantem MeSH

In this study we performed a genotype-phenotype association analysis of meiotic stability in 10 autotetraploid Arabidopsis lyrata and A. lyrata/A. arenosa hybrid populations collected from the Wachau region and East Austrian Forealps. The aim was to determine the effect of eight meiosis genes under extreme selection upon adaptation to whole genome duplication. Individual plants were genotyped by high-throughput sequencing of the eight meiosis genes (ASY1, ASY3, PDS5b, PRD3, REC8, SMC3, ZYP1a/b) implicated in synaptonemal complex formation and phenotyped by assessing meiotic metaphase I chromosome configurations. Our results reveal that meiotic stability varied greatly (20-100%) between individual tetraploid plants and associated with segregation of a novel ASYNAPSIS3 (ASY3) allele derived from A. lyrata. The ASY3 allele that associates with meiotic stability possesses a putative in-frame tandem duplication (TD) of a serine-rich region upstream of the coiled-coil domain that appears to have arisen at sites of DNA microhomology. The frequency of multivalents observed in plants homozygous for the ASY3 TD haplotype was significantly lower than in plants heterozygous for ASY3 TD/ND (non-duplicated) haplotypes. The chiasma distribution was significantly altered in the stable plants compared to the unstable plants with a shift from proximal and interstitial to predominantly distal locations. The number of HEI10 foci at pachytene that mark class I crossovers was significantly reduced in a plant homozygous for ASY3 TD compared to a plant heterozygous for ASY3 ND/TD. Fifty-eight alleles of the 8 meiosis genes were identified from the 10 populations analysed, demonstrating dynamic population variability at these loci. Widespread chimerism between alleles originating from A. lyrata/A. arenosa and diploid/tetraploids indicates that this group of rapidly evolving genes may provide precise adaptive control over meiotic recombination in the tetraploids, the very process that gave rise to them.

• MeSH
• alely MeSH
• Arabidopsis genetika   růst a vývoj   MeSH
• chromozomální proteiny, nehistonové genetika   MeSH
• chromozomy rostlin genetika   MeSH
• diploidie MeSH
• DNA vazebné proteiny genetika   MeSH
• meióza genetika   MeSH
• párování chromozomů genetika   MeSH
• proteiny huseníčku genetika   MeSH
• segregace chromozomů MeSH
• tetraploidie MeSH
• Publikační typ
• časopisecké články MeSH
• práce podpořená grantem MeSH
• Názvy látek
• ASY3 protein, Arabidopsis MeSH Prohlížeč
• chromozomální proteiny, nehistonové MeSH
• DNA vazebné proteiny MeSH
• HEI10 protein, Arabidopsis MeSH Prohlížeč
• proteiny huseníčku MeSH