Bringing together evolution on serpentine and polyploidy: spatiotemporal history of the diploid-tetraploid complex of Knautia arvensis (Dipsacaceae)

Our plain-English summary of Bringing together evolution on serpentine and polyploidy: spatiotemporal history of the diploid-tetraploid complex of Knautia arvensis (Dipsacaceae), by F. Kolář, T. Fér, M. Štech, et al (PloS One, 2012).

The study

• Authors: F. Kolář, T. Fér, M. Štech, P. Trávníček, E. Dušková, P. Schönswetter, J. Suda
• Journal: PloS One
• Published: 2012;7(7):e39988
• Cited by: 31 articles, as counted by NIH iCite
• Read it: PubMed · Publisher · Free full text

Abstract

Polyploidization is one of the leading forces in the evolution of land plants, providing opportunities for instant speciation and rapid gain of evolutionary novelties. Highly selective conditions of serpentine environments act as an important evolutionary trigger that can be involved in various speciation processes. Whereas the significance of both edaphic speciation on serpentine and polyploidy is widely acknowledged in plant evolution, the links between polyploid evolution and serpentine differentiation have not yet been examined. To fill this gap, we investigated the evolutionary history of the perennial herb Knautia arvensis (Dipsacaceae), a diploid-tetraploid complex that exhibits an intriguing pattern of eco-geographic differentiation. Using plastid DNA sequencing and AFLP genotyping of 336 previously cytotyped individuals from 40 populations from central Europe, we unravelled the patterns of genetic variation among the cytotypes and the edaphic types. Diploids showed the highest levels of genetic differentiation, likely as a result of long term persistence of several lineages in ecologically distinct refugia and/or independent immigration. Recurrent polyploidization, recorded in one serpentine island, seems to have opened new possibilities for the local serpentine genotype. Unlike diploids, the serpentine tetraploids were able to escape from the serpentine refugium and spread further; this was also attributable to hybridization with the neighbouring non-serpentine tetraploid lineages. The spatiotemporal history of K. arvensis allows tracing the interplay of polyploid evolution and ecological divergence on serpentine, resulting in a complex evolutionary pattern. Isolated serpentine outcrops can act as evolutionary capacitors, preserving distinct karyological and genetic diversity. The serpentine lineages, however, may not represent evolutionary 'dead-ends' but rather dynamic systems with a potential to further influence the surrounding populations, e.g., via independent polyplodization and hybridization. The complex eco-geographical pattern together with the incidence of both primary and secondary diploid-tetraploid contact zones makes K. arvensis a unique system for addressing general questions of polyploid research.

In plain English

This was a genetic study of a wild flowering plant, Knautia arvensis, and its close relatives. It is not a study of asbestos or human health, and asbestos is not mentioned. The authors studied plants growing on serpentine soils and on other soils in central Europe, where the plant has diploid and tetraploid forms (two or four sets of chromosomes). They analysed DNA markers (AFLPs) in 336 plants from 40 populations collected from 2005 to 2008 in six countries, and sequenced a plastid DNA region in 77 plants. Genetic diversity was higher in diploid than in tetraploid populations (mean values 0.162 and 0.137). The highest scores for rare genetic markers belonged to four diploid populations from relict serpentine sites. In one serpentine area, the Slavkovský les Mts., the diploids and tetraploids growing together differed very little: the difference explained only 0.7% of the genetic variation there. Some of these plants also shared a unique plastid haplotype. The authors concluded that the serpentine tetraploids there arose at least once from local diploids, and that these serpentine lineages are not evolutionary dead-ends.

We wrote this plain-English summary from the full article with the help of AI, and a second AI model checked each sentence against the article. It is not the authors' wording; the abstract and the article are their own account.

What the study did and found

• Design: Population genetic (phylogeographic) study of a plant species complex using AFLP genotyping and plastid DNA sequencing
• Who was studied: 336 plants from 40 populations of Knautia arvensis agg. (34 populations of K. arvensis s.s., two each of K. kitaibelii and K. slovaca, two of the hybrid K. arvensis x K. kitaibelii), sampled 2005 to 2008 in the Czech Republic, Slovakia, Hungary, Austria, Germany and Ukraine; 77 plants were sequenced for plastid DNA
• Exposure: Growth on serpentine soils compared with non-serpentine habitats (relict limestone sites, a subalpine glacial cirque, semiruderal grasslands), together with ploidy level (diploid vs tetraploid). No asbestos fibers or human exposure were studied.
• Main results:
  • Genetic diversity was significantly higher in diploid populations than in tetraploid populations (mean values 0.162 for diploids and 0.137 for tetraploids)
  • The highest rarity index values (rare genetic markers) belonged to four diploid populations from relict serpentine stands (P01, P02, P03 and P05)
  • K-means clustering divided the dataset into seven genetic groups, mostly reflecting ploidy level, genome size and habitat
  • In the Slavkovský les Mts. serpentine area, the difference between co-occurring diploids and tetraploids explained only 0.7% of the total genetic variation
  • 13 plastid DNA haplotypes were found in the 77 sequences; half of the plants had the widespread haplotype A
  • Haplotype D was found only in diploid and tetraploid plants from the same mixed-ploidy serpentine population, Planý vrch (P04 and P20)
• The authors' conclusion: The authors concluded that at least one independent autopolyploidization event took place in situ in the Slavkovský les Mts., giving rise to serpentine tetraploids from local relict diploids. They also concluded that these recurrently formed polyploids appear able to escape their serpentine refugia, so serpentine relicts are not evolutionary dead-ends.
• Limitations the authors state:
  • The relationships and history of the tetraploid and non-relict diploid lineages cannot be inferred without more intensive sampling in other parts of the plant's range
  • The plastid DNA data had low discriminative power and were generally not congruent with the AFLP data

Topics

The National Library of Medicine indexes this study under subjects our site covers: Chrysotile.

Medical terms in this study, explained in our Lexicon: Serpentine Group.

Related studies

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• Population resequencing reveals local adaptation of Arabidopsis lyrata to serpentine soils — T.L. Turner, E.C. Bourne, et al. (2010)
• Serpentine soils affect heavy metal tolerance but not genetic diversity in a common Mediterranean ant — F. Frizzi, A. Masoni, et al. (2017)
• Genetic analyses of nickel tolerance in a North American serpentine endemic plant, Caulanthus amplexicaulis var. barbarae (Brassicaceae) — A.M. Burrell, A.K. Hawkins, et al. (2012)
• Collinsia sparsiflora in serpentine and nonserpentine habitats: using F2 hybrids to detect the potential role of selection in ecotypic differentiation — J.W. Wright, M.L. Stanton (2007)

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