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.
Highlights
IntroductionSerpentine soils, characterized by specific chemical (i.e., low Ca/Mg ratio, high heavy metal content, low nutrient availability) and physical (e.g., drought) properties, strongly influence the plant life that grows on them [1,2]
Serpentine soils, characterized by specific chemical and physical properties, strongly influence the plant life that grows on them [1,2]
We addressed the following questions: (1) What are the genetic relationships among the species, cytotypes, genome size groups, and edaphic types within central Europe? (2) Is there any genetic differentiation at the diploid level? Do the two diploid groups with distinct genome sizes and divergent habitat preferences represent separate genetic lineages? If so, is there any further genetic sub-structuring, e.g., according to geography and/or occupied habitat? (3) Did the serpentine tetraploids originate by recurrentpolyploidization or by colonization of serpentine sites by non-serpentine tetraploids? (4) What are the relationships among serpentine and surrounding non-serpentine tetraploids? Is there indication of hybridization across the borders of serpentine areas?
Summary
Serpentine soils, characterized by specific chemical (i.e., low Ca/Mg ratio, high heavy metal content, low nutrient availability) and physical (e.g., drought) properties, strongly influence the plant life that grows on them [1,2]. The unique features of serpentine soils can shape plant evolution in two main ways [5,6,7]. They can act as a selective factor, picking tolerant genotypes out of mainly non-tolerant gene pools of potential colonizers. Such disruptive selection may result in ecotypic differentiation [8,9,10] and, provided that reproductive isolation is achieved, it may lead to sympatric or parapatric speciation of serpentine endemics on the border of serpentine area [5,7,11]. The evolutionary history becomes even more complicated if the serpentine populations come into secondary contact with their non-serpentine counterparts (e.g., after the progenitor’s re-invasion) and hybridize [15]
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