Most cited article - PubMed ID 31740675
Interspecific introgression mediates adaptation to whole genome duplication
Understanding the relationship between macro- and microevolutionary processes and their delimitation remains a challenge. This review focuses on the role of chromosomal rearrangements in plant population differentiation and lineage diversification resulting in speciation, helping bridge the gap between macro- and microevolution through chromosomal evolution. We focus on angiosperms, a group that comprises the majority of extant plant species diversity and exhibits the largest chromosomal and genomic variations. Here, we address the following questions: Are macroevolutionary patterns of chromosome evolution the result of accumulated microevolutionary changes, or do chromosomal dynamics drive larger shifts along the speciation continuum? At the macroevolutionary level, we investigated the association between karyotype diversity and diversification rates using evidence from comparative genomics, chromosomal evolution modelling across phylogenies, and the association with several traits across different angiosperm lineages. At the microevolutionary level, we explore if different karyotypes are linked to morphological changes and population genetic differentiation in the same lineages. Polyploidy (autopolyploidy and allopolyploidy) and dysploidy are known drivers of speciation, with karyotypic differences often leading to reproductive barriers. We found that dysploidy, involving gains and losses of single chromosomes with no significant change in overall content of the genome, appears to be relatively more frequent and persistent across macroevolutionary histories than polyploidy. Additionally, chromosomal rearrangements that do not entail change in chromosome number, such as insertions, deletions, inversions, and duplications of chromosome fragments, as well as translocations between chromosomes, are increasingly recognized for their role in local adaptation and speciation. We argue that there is more evidence linking chromosomal rearrangements with genetic and morphological trait differentiation at microevolutionary scales than at macroevolutionary ones. Our findings highlight the importance of selection across evolutionary scales, where certain chromosomal dynamics become fixed over macroevolutionary time. Consequently, at microevolutionary scales, chromosome rearrangements are frequent and diverse, serving as key drivers of plant diversification and adaptation by providing a pool of variation from which beneficial chromosomal changes can be selected and fixed by evolutionary forces.
- Keywords
- angiosperms, chromosome, dysploidy, evolution, polyploidy, speciation,
- Publication type
- Journal Article MeSH
- Review MeSH
Abundance of established polyploid lineages varies across lineages, evolutionary time, and geography, suggesting both genetics and environment play a role in polyploid persistence. We show Arabidopsis lyrata is the most polyploid-rich species complex in the Arabidopsis genus, with multiple origins of autotetraploidy. This is revealed by genomic data from over 400 A. lyrata samples across Eurasia. We found over 30 previously undescribed autotetraploid populations in Siberia with a minimum of two separate origins, independent of those previously reported in Central Europe. The establishment of Siberian tetraploids is mediated by meiotic adaptation at the same genes as in European tetraploid A. lyrata and Arabidopsis arenosa, despite their genomic divergence and geographical separation. Haplotype analysis based on synthetic long-read assemblies supports the long-range introgression of adaptive alleles from the tetraploid interspecific pool of European A. lyrata and A. arenosa to tetraploid Siberian A. lyrata. Once adaptations to polyploidy emerge, they promote the establishment of new polyploid lineages through adaptive inter- and intraspecific introgression.
- Keywords
- Arabidopsis lyrata, adaptation, introgression, polyploid,
- MeSH
- Arabidopsis * genetics MeSH
- Genome, Plant MeSH
- Genetic Introgression * MeSH
- Haplotypes MeSH
- Polyploidy * MeSH
- Tetraploidy MeSH
- Publication type
- Journal Article MeSH
- Geographicals
- Europe MeSH
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.
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.
- Keywords
- Adaptation, evolution, genetic introgression, polyploidy, speciation, whole-genome duplication,
- MeSH
- Biological Evolution MeSH
- Genome, Plant genetics MeSH
- Ploidies MeSH
- Polyploidy * MeSH
- Plants genetics MeSH
- Reproduction genetics MeSH
- Gene Flow * MeSH
- Genetic Speciation MeSH
- Publication type
- Journal Article MeSH
- Review 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.
- Keywords
- Allopolyploidy, Betula, autopolyploidy, gene flow, genomic polarization, homoeologs, interploidal, introgressive hybridization, polyploid phylogenetics, polyploidization simulation, reticulate evolution,
- MeSH
- Alleles * MeSH
- Betula * genetics classification MeSH
- Phylogeny * MeSH
- Genome, Plant * MeSH
- Genetic Introgression MeSH
- Hybridization, Genetic MeSH
- Polyploidy * MeSH
- Publication type
- Journal Article 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.
- Keywords
- chromosomal structural variation, desert plants, microhabitat divergence, polyploidization,
- MeSH
- Brassicaceae classification genetics physiology MeSH
- Ecosystem * MeSH
- Phylogeny MeSH
- Adaptation, Physiological genetics MeSH
- Genome, Plant * MeSH
- Polyploidy MeSH
- Genetic Speciation * MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't 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.
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
- Alleles * MeSH
- Arabidopsis drug effects genetics MeSH
- Adaptation, Physiological drug effects genetics MeSH
- Genome, Plant * MeSH
- Polymorphism, Single Nucleotide MeSH
- Mutation MeSH
- Polyploidy * MeSH
- Arabidopsis Proteins genetics metabolism MeSH
- Soil chemistry MeSH
- Secologanin Tryptamine Alkaloids metabolism MeSH
- Calcium Channels metabolism MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Arabidopsis Proteins MeSH
- Soil MeSH
- Secologanin Tryptamine Alkaloids MeSH
- serpentine (alkaloid) MeSH Browser
- TPC1 protein, Arabidopsis MeSH Browser
- Calcium Channels 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.
- Keywords
- Arabidopsis, alpine adaptation, evolution, genomics, parallelism,
- MeSH
- Molecular Sequence Annotation MeSH
- Arabidopsis classification genetics metabolism radiation effects MeSH
- Biological Evolution * MeSH
- Herbivory physiology MeSH
- Adaptation, Physiological genetics MeSH
- Stress, Physiological MeSH
- Genetic Variation * MeSH
- Genetic Drift MeSH
- Genome, Plant * MeSH
- Genetic Introgression MeSH
- Gene Ontology MeSH
- Radiation, Ionizing MeSH
- Models, Genetic MeSH
- Cold Temperature MeSH
- Plant Proteins genetics metabolism MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Plant Proteins 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.
- Keywords
- Erythranthe, Mimulus, allopolyploid, polyploidy, speciation, whole-genome duplication,
- MeSH
- Gene Duplication * MeSH
- Phenotype MeSH
- Fertility genetics MeSH
- Genome, Plant * MeSH
- Hybridization, Genetic * MeSH
- Mimulus genetics MeSH
- Evolution, Molecular * MeSH
- Polyploidy * MeSH
- Reproductive Isolation MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
