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.
BACKGROUND AND AIMS: Polyploidy is an important driver of plant diversification and adaptation to novel environments. As a consequence of genome doubling, polyploids often exhibit greater colonizing ability or occupy a wider ecological niche than diploids. Although elevation has been traditionally considered as a key driver structuring ploidy variation, we do not know if environmental and phenotypic differentiation among ploidy cytotypes varies along an elevational gradient. Here, we tested for the consequences of genome duplication on genetic diversity, phenotypic variation and habitat preferences on closely related diploid and tetraploid populations that coexist along approx. 2300 m of varying elevation. METHODS: We sampled and phenotyped 45 natural diploid and tetraploid populations of Arabidopsis arenosa in one mountain range in Central Europe (Western Carpathians) and recorded abiotic and biotic variables at each collection site. We inferred genetic variation, population structure and demographic history in a sub-set of 29 populations genotyped for approx. 36 000 single nucleotide polymorphisms. KEY RESULTS: We found minor effects of polyploidy on colonization of alpine stands and low genetic differentiation between the two cytotypes, mirroring recent divergence of the polyploids from the local diploid lineage and repeated reticulation events among the cytotypes. This pattern was corroborated by the absence of ecological niche differentiation between the two cytotypes and overall phenotypic similarity at a given elevation. CONCLUSIONS: The case of A. arenosa contrasts with previous studies that frequently showed clear niche differentiation between cytotypes. Our work stresses the importance of considering genetic structure and past demographic processes when interpreting the patterns of ploidy distributions, especially in species that underwent recent polyploidization events.
- MeSH
- Arabidopsis * MeSH
- ekosystém MeSH
- lidé MeSH
- ploidie MeSH
- polyploidie MeSH
- Check Tag
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Evropa MeSH
Whole genome duplication is a key process in plant evolution and has direct phenotypic consequences. However, it remains unclear whether ploidy-related phenotypic changes can significantly alter the fitness of polyploids in nature and thus contribute to establishment of new polyploid mutants in diploid populations. We addressed this question using a unique natural system encompassing a diploid and its sympatric locally established autotetraploid derivative. By setting a common garden experiment with two manipulated environmental factors (presence/absence of serpentine substrate and competition), we tested whether these two locally important factors differently shape the phenotypic response of the two ploidy levels. Tetraploids attained significantly higher values of both above- and below-ground biomass, and root : shoot ratio compared to their diploid progenitors. Tetraploid superiority in vegetative fitness indicators was most prominent when they were cultivated together with a competitor in nutrient-rich nonserpentine substrate. We show that even genetically very closely related diploids and tetraploids can respond differently to key environmental factors. Provided there are sufficient nutrients, tetraploids can be more successful in tolerating interspecific competition than their diploid progenitors. Such superior performance might have provided an adaptive advantage for the newly established tetraploid promoting colonisation of new (micro-)habitats, which was indeed observed at the natural site.
Analysis of population genetic structure has become a standard approach in population genetics. In polyploid complexes, clustering analyses can elucidate the origin of polyploid populations and patterns of admixture between different cytotypes. However, combining diploid and polyploid data can theoretically lead to biased inference with (artefactual) clustering by ploidy. We used simulated mixed-ploidy (diploid-autotetraploid) data to systematically compare the performance of k-means clustering and the model-based clustering methods implemented in STRUCTURE, ADMIXTURE, FASTSTRUCTURE and INSTRUCT under different scenarios of differentiation and with different marker types. Under scenarios of strong population differentiation, the tested applications performed equally well. However, when population differentiation was weak, STRUCTURE was the only method that allowed unbiased inference with markers with limited genotypic information (co-dominant markers with unknown dosage or dominant markers). Still, since STRUCTURE was comparatively slow, the much faster but less powerful FASTSTRUCTURE provides a reasonable alternative for large datasets. Finally, although bias makes k-means clustering unsuitable for markers with incomplete genotype information, for large numbers of loci (>1000) with known dosage k-means clustering was superior to FASTSTRUCTURE in terms of power and speed. We conclude that STRUCTURE is the most robust method for the analysis of genetic structure in mixed-ploidy populations, although alternative methods should be considered under some specific conditions.
- MeSH
- diploidie MeSH
- genetická variace genetika MeSH
- genetické markery genetika MeSH
- genotyp MeSH
- jednonukleotidový polymorfismus genetika MeSH
- mikrosatelitní repetice genetika MeSH
- ploidie * MeSH
- populační genetika statistika a číselné údaje MeSH
- shluková analýza MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
The island-like distribution of subalpine habitats across mountain ranges can trigger the parallel evolution of locally adapted ecotypes. Such naturally replicated scenarios allow testing hypotheses on how elevational differentiation structures genetic diversity within species. Nevertheless, the parallel colonization of subalpine habitats across different mountain ranges has only rarely been documented with molecular data. We chose Primula elatior (Primulaceae), naturally spanning entire elevation range in multiple mountain regions of central Europe, to test for the origin of its scattered subalpine populations. Nuclear microsatellite variation revealed three genetic groups corresponding with the distinct study regions. We found that genetic differentiation between foothill and subalpine populations within each region was relatively low, suggesting that the colonization of subalpine habitats occurred independently within each mountain range. Furthermore, the strongest differentiation was usually found between the subalpine populations suggesting that mountain ridges may act as migration barriers that can reduce gene flow more strongly than elevational differences between foothill and subalpine populations. Finally, we found that subalpine colonization did not result in a loss of genetic diversity relative to foothill populations in agreement with the high migration rates that we document here between the subalpine and the foothill populations. In summary, our study shows subalpine Primula elatior populations are genetically diverse and distinct results of parallel colonization events from multiple foothill gene pools.
- MeSH
- ekosystém * MeSH
- genetická variace * MeSH
- mikrosatelitní repetice * MeSH
- Primula genetika MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Evropa MeSH
Mixed-ploidy species harbor a unique form of genomic and phenotypic variation that influences ecological interactions, facilitates genetic divergence, and offers insights into the mechanisms of polyploid evolution. However, there have been few attempts to synthesize this literature. We review here research on the cytotype distribution, diversity, and dynamics of intensively studied mixed-ploidy species and consider the implications for understanding mechanisms of polyploidization such as cytotype formation, establishment, coexistence, and post-polyploid divergence. In general, mixed-ploidy species are unevenly represented among families: they exhibit high cytotype diversity, often within populations, and frequently comprise rare and odd-numbered ploidies. Odd-ploidies often occur in association with asexuality. We highlight research hypotheses and opportunities that take advantage of the unique properties of ploidy variation.
- MeSH
- chromozomy rostlin * MeSH
- genetická variace * MeSH
- ploidie MeSH
- polyploidie * MeSH
- rostliny genetika MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
Background and Aims: Despite the recent wealth of studies targeted at contact zones of cytotypes in various species, some aspects of polyploid evolution are still poorly understood. This is especially the case for the frequency and success rate of spontaneous neopolyploidization or the temporal dynamics of ploidy coexistence, requiring massive ploidy screening and repeated observations, respectively. To fill this gap, an extensive study of spatio-temporal patterns of ploidy coexistence was initiated in the widespread annual weed Tripleurospermum inodorum (Asteraceae). Methods: DNA flow cytometry along with confirmatory chromosome counts was employed to assess ploidy levels of 11 018 adult individuals and 1263 ex situ germinated seedlings from 1209 Central European populations. The ploidy screening was conducted across three spatial scales and supplemented with observations of temporal development of 37 mixed-ploidy populations. Key Results: The contact zone between the diploid and tetraploid cytotypes has a diffuse, mosaic-like structure enabling common cytotype coexistence from the within-population to the landscape level. A marked difference in monoploid genome size between the two cytotypes enabled the easy distinction of neotetraploid mutants from long-established tetraploids. Neotetraploids were extremely rare (0·03 %) and occurred solitarily. Altogether five ploidy levels (2 x -6 x ) and several aneuploids were discovered; the diversity in nuclear DNA content was highest in early ontogenetic stages (seedlings) and among individuals from mixed-ploidy populations. In spite of profound temporal oscillations in cytotype frequencies in mixed-ploidy populations, both diploids and tetraploids usually persisted up to the last census. Conclusions: Diploids and tetraploids commonly coexist at all spatial scales and exhibit considerable temporal stability in local ploidy mixtures. Mixed-ploidy populations containing fertile triploid hybrids probaby act as effective generators of cytogenetic novelty and may facilitate inter-ploidy gene flow. Neopolyploid mutants were incapable of local establishment.
- MeSH
- Asteraceae genetika MeSH
- biologická evoluce * MeSH
- diploidie MeSH
- polyploidie * MeSH
- tetraploidie MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Evropa MeSH
The tropical Andes represent one of the world's biodiversity hot spots, but the evolutionary drivers generating their striking species diversity still remain poorly understood. In the treeless high-elevation Andean environments, Pleistocene glacial oscillations and niche differentiation are frequently hypothesized diversification mechanisms; however, sufficiently densely sampled population genetic data supporting this are still lacking. Here, we reconstruct the evolutionary history of Loricaria (Asteraceae), a plant genus endemic to the Andean treeless alpine zone, based on comprehensive population-level sampling of 289 individuals from 67 populations across the entire distribution ranges of its northern Andean species. Partly incongruent AFLP and plastid DNA markers reveal that the distinct genetic structure was shaped by a complex interplay of biogeography (spread along and across the cordilleras), history (Pleistocene glacial oscillations) and local ecological conditions. While plastid variation documents an early split or colonization of the northern Andes by at least two lineages, one of which further diversified, a major split in the AFLP data correlate with altitudinal ecological differentiation. This suggests that niche shifts may be important drivers of Andean diversification not only in forest-alpine transitions, but also within the treeless alpine zone itself. The patterns of genetic differentiation at the intraspecific level reject the hypothesized separation in spatially isolated cordilleras and instead suggest extensive gene flow among populations from distinct mountain chains. Our study highlights that leveraging highly variable markers against extensive population-level sampling is a promising approach to address mechanisms of rapid species diversifications.
- MeSH
- analýza polymorfismu délky amplifikovaných restrikčních fragmentů MeSH
- Asteraceae klasifikace MeSH
- biodiverzita * MeSH
- biologická evoluce * MeSH
- DNA chloroplastová genetika MeSH
- fylogeneze * MeSH
- nadmořská výška MeSH
- tropické klima MeSH
- Publikační typ
- časopisecké články MeSH
- Geografické názvy
- Ekvádor MeSH
- Kolumbie MeSH
Quaternary climatic oscillations profoundly impacted temperate biodiversity. For many diverse yet undersampled areas, however, the consequences of this impact are still poorly known. In Europe, particular uncertainty surrounds the role of Balkans, a major hotspot of European diversity, in postglacial recolonization of more northerly areas, and the Carpathians, a debatable candidate for a northern 'cryptic' glacial refugium. Using genome-wide SNPs and microsatellites, we examined how the interplay of historical processes and niche shifts structured genetic diversity of diploid Arabidopsis arenosa, a little-known member of the plant model genus that occupies a wide niche range from sea level to alpine peaks across eastern temperate Europe. While the northern Balkans hosted one isolated endemic lineage, most of the genetic diversity was concentrated further north in the Pannonian Basin and the Carpathians, where it likely survived the last glaciation in northern refugia. Finally, a distinct postglacial environment in northern Europe was colonized by populations of admixed origin from the two Carpathian lineages. Niche differentiation along altitude-related bioclimatic gradients was the main trend in the phylogeny of A. arenosa. The most prominent niche shifts, however, characterized genetically only slightly divergent populations that expanded into narrowly defined alpine and northern coastal postglacial environments. Our study highlights the role of eastern central European mountains not only as refugia for unique temperate diversity but also sources for postglacial expansion into novel high-altitude and high-latitude niches. Knowledge of distinct genetic substructure of diploid A. arenosa also opens new opportunities for follow-up studies of this emerging model of evolutionary biology.
- MeSH
- Arabidopsis genetika MeSH
- ekosystém MeSH
- fylogeneze MeSH
- jednonukleotidový polymorfismus MeSH
- mikrosatelitní repetice MeSH
- populační genetika * MeSH
- refugium * MeSH
- Publikační typ
- časopisecké články MeSH
- Geografické názvy
- Balkánský poloostrov MeSH
- východní Evropa MeSH
