Bringing Together Evolution on Serpentine and Polyploidy: Spatiotemporal History of the Diploid-Tetraploid Complex of Knautia arvensis (Dipsacaceae)

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.

Large and variable genome size unrelated to serpentine adaptation but supportive of cryptic sexuality in Cenococcum geophilum

“…Differential selection across ploidy levels has been observed in different abiotic environments (e.g., Dhar et al 2011) and increased ploidy has been suggested to provide a selective advantage in adaptation to new environmental conditions (Pawlowska and Taylor 2004;Ma et al 2009). However, despite the strong selection pressure that is expected in serpentine soils and a report of possible influences of serpentine on the evolution of polyploids in K. arvensis (Kolář et al 2012), we did not find significant differentiation in genome size between the C. geophilum populations included in this study, suggesting that genetic and demographic processes are more important in shaping the genome size variation of this species than environmental selection in the form of home soil chemistry. While these results suggest that variation in ploidy level is not related to serpentine tolerance in C. geophilum, the relatively large genome size-providing the potential for local adaptation to develop in vastly different environments-may still contribute to the wide ecological breadth, including the occurrence in serpentine soils, reported for this species.…”

“…Although many studies have been performed on serpentine flora and systematics, natural history, ecology, and physiology, possible relationships between adaptation to serpentine soil conditions and genome size variation have not received much attention. Nevertheless, independent polyploid evolution in serpentine populations of Knautia arvensis (Dipsacaceae) that promoted further evolution of serpentine lineages has recently been reported (Kolář et al 2012).…”

Polyploidy and novelty: Gottlieb's legacy

“…Other prominent examples include changes in phenology [109], salt accumulation [110], pollinator assemblages [111] and mineral-related stress (e.g. serpentine soil) [112]. Taken together, these studies illustrate some of the many ways in which a nascent polyploid might escape minority cytotype exclusion and become established though a shift in niche space, temporal isolation or otherwise [113].…”

Evolution of nickel hyperaccumulation and serpentine adaptation in the Alyssum serpyllifolium species complex

“…However, glacial ice covered parts of the current range of A. serpyllifolium, including southern Spain, certain regions in central Spain, as well as the Pyrenees and the south of France (Levin, 2013), and hence the Last Glacial Maximum cannot be entirely ruled out as a factor in the phylogenetic history of this taxon. Indeed, an influence of climatic fluctuations can be important for the population dynamics of serpentine species (Kolář et al, 2012). One scenario envisages formerly widespread metallophyte species being excluded from non-serpentine sites during post-glacial reforestation because of their low competitiveness on nonmetalliferous soils; the serpentine populations would become separated and disjunct, and because of reduced gene flow progressively differentiate owing to drift and selection.…”