Nejvíce citovaný článek - PubMed ID 33783509
Novelty and Convergence in Adaptation to Whole Genome Duplication
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.
- Klíčová slova
- Arabidopsis lyrata, adaptation, introgression, polyploid,
- Publikační typ
- časopisecké články MeSH
Polyploidisation is a significant reproductive barrier, yet genetic evidence indicates that interploidy admixture is more common than previously thought. Theoretical models and controlled crosses support the 'triploid bridge' hypothesis, proposing that hybrids of intermediate ploidy facilitate gene flow. However, comprehensive evidence combining experimental and genetic data from natural mixed-ploidy species is missing. Here, we investigated the rates and directionality of gene flow within a diploid-autotetraploid contact zone of Cardamine amara, a species with abundant natural triploids. We cytotyped over 400 individuals in the field, conducted reciprocal interploidy crosses, and inferred gene flow based on genome-wide sequencing of 84 individuals. Triploids represent a conspicuous entity in mixed-ploidy populations (5%), yet only part of them arose through interploidy hybridisation. Despite being rarely formed, triploid hybrids can backcross with their parental cytotypes, producing viable offspring that are often euploid (in 42% of cases). In correspondence, D-statistics and coalescent simulations documented a significant genome-wide signal of bidirectional gene flow in sympatric but not allopatric populations. Triploids, though rare, thus seem to play a key role in overcoming polyploidy-related reproductive barriers in C. amara. In sum, we present integrative evidence for interploidy gene flow mediated by a triploid bridge in natural populations.
- Klíčová slova
- introgression, polyploidy, population genomics, speciation, whole genome duplication,
- MeSH
- Cardamine * genetika MeSH
- genová introgrese * MeSH
- hybridizace genetická MeSH
- ploidie * MeSH
- polyploidie MeSH
- populační genetika MeSH
- tok genů * MeSH
- triploidie * MeSH
- Publikační typ
- časopisecké články 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.
- 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
Polyploidy, the result of whole-genome duplication (WGD), is a major driver of eukaryote evolution. Yet WGDs are hugely disruptive mutations, and we still lack a clear understanding of their fitness consequences. Here, we study whether WGDs result in greater diversity of genomic structural variants (SVs) and how they influence evolutionary dynamics in a plant genus, Cochlearia (Brassicaceae). By using long-read sequencing and a graph-based pangenome, we find both negative and positive interactions between WGDs and SVs. Masking of recessive mutations due to WGDs leads to a progressive accumulation of deleterious SVs across four ploidal levels (from diploids to octoploids), likely reducing the adaptive potential of polyploid populations. However, we also discover putative benefits arising from SV accumulation, as more ploidy-specific SVs harbor signals of local adaptation in polyploids than in diploids. Together, our results suggest that SVs play diverse and contrasting roles in the evolutionary trajectories of young polyploids.
Gene flow between species in the genus Arabidopsis occurs in significant amounts, but how exactly gene flow is achieved is not well understood. Polyploidization may be one avenue to explain gene flow between species. One problem, however, with polyploidization as a satisfying explanation is the occurrence of lethal genomic instabilities in neopolyploids as a result of genomic exchange, erratic meiotic behavior, and genomic shock. We have created an autoallohexaploid by pollinating naturally co-occurring diploid Arabidopsis thaliana with allotetraploid Arabidopsis suecica (an allotetraploid composed of A. thaliana and Arabidopsis arenosa). Its triploid offspring underwent spontaneous genome duplication and was used to generate a multigenerational pedigree. Using genome resequencing, we show that 2 major mechanisms promote stable genomic exchange in this population. Legitimate meiotic recombination and chromosome segregation between the autopolyploid chromosomes of the 2 A. thaliana genomes occur without any obvious bias for the parental origin and combine the A. thaliana haplotypes from the A. thaliana parent with the A. thaliana haplotypes from A. suecica similar to purely autopolyploid plants. In addition, we repeatedly observed that occasional exchanges between regions of the homoeologous chromosomes are tolerated. The combination of these mechanisms may result in gene flow leading to stable introgression in natural populations. Unlike the previously reported resynthesized neoallotetraploid A. suecica, this population of autoallohexaploids contains mostly vigorous, and genetically, cytotypically, and phenotypically variable individuals. We propose that naturally formed autoallohexaploid populations might serve as an intermediate bridge between diploid and polyploid species, which can facilitate gene flow rapidly and efficiently.
- Klíčová slova
- Arabidopsis, aneuploidy, autoallopolyploidy, evolution, gene flow, hexaploid, homoeologous exchange, introgression, polyploidy,
- MeSH
- Arabidopsis * genetika MeSH
- chromozomy MeSH
- genom rostlinný MeSH
- genomika MeSH
- genová introgrese * MeSH
- polyploidie MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Non-inflammatory alopecia is a frequent skin problem in dogs, causing damaged coat integrity and compromised appearance of affected individuals. In this study, we examined the Cesky Fousek breed, which displays atypical recurrent flank alopecia (aRFA) at a high frequency. This type of alopecia can be quite severe and is characterized by seasonal episodes of well demarcated alopecic areas without hyperpigmentation. The genetic component responsible for aRFA remains unknown. Thus, here we aimed to identify variants involved in aRFA using a combination of histological, genomic, and transcriptomic data. We showed that aRFA is histologically similar to recurrent flank alopecia, characterized by a lack of anagen hair follicles and the presence of severely shortened telogen or kenogen hair follicles. We performed a genome-wide association study (GWAS) using 216 dogs phenotyped for aRFA and identified associations on chromosomes 19, 8, 30, 36, and 21, highlighting 144 candidate genes, which suggests a polygenic basis for aRFA. By comparing the skin cell transcription pattern of six aRFA and five control dogs, we identified 236 strongly differentially expressed genes (DEGs). We showed that the GWAS genes associated with aRFA are often predicted to interact with DEGs, suggesting their joint contribution to the development of the disease. Together, these genes affect four major metabolic pathways connected to aRFA: collagen formation, muscle structure/contraction, lipid metabolism, and the immune system.
- Klíčová slova
- Cesky Fousek, GWAS, RNA-seq, atypical recurrent flank alopecia, canine alopecia, differential gene expression, dog, skin biopsies,
- MeSH
- alopecie genetika patologie veterinární MeSH
- celogenomová asociační studie * MeSH
- kůže patologie MeSH
- psi MeSH
- transkriptom * genetika MeSH
- vlasový folikul MeSH
- zvířata MeSH
- Check Tag
- psi MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem 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
