Most cited article - PubMed ID 23169557
Absence of gene flow between diploids and hexaploids of Aster amellus at multiple spatial scales
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.
- Keywords
- Adaptation, evolution, genetic introgression, polyploidy, speciation, whole-genome duplication,
- MeSH
- Biological Evolution MeSH
- Genome, Plant genetics MeSH
- Ploidies MeSH
- Polyploidy * MeSH
- Plants genetics MeSH
- Reproduction genetics MeSH
- Gene Flow * MeSH
- Genetic Speciation MeSH
- Publication type
- Journal Article MeSH
- Review MeSH
BACKGROUND AND AIMS: The origin of different cytotypes by autopolyploidy may be an important mechanism in plant diversification. Although cryptic autopolyploids probably comprise the largest fraction of overlooked plant diversity, our knowledge of their origin and evolution is still rather limited. Here we study the presumed autopolyploid aggregate of Aster amellus, which encompasses diploid and hexaploid cytotypes. Although the cytotypes of A. amellus are not morphologically distinguishable, previous studies showed spatial segregation and limited gene flow between them, which could result in different evolutionary trajectories for each cytotype. METHODS: We combine macroevolutionary, microevolutionary and niche modelling tools to disentangle the origin and the demographic history of the cytotypes, using chloroplast and nuclear markers in a dense population sampling in central Europe. KEY RESULTS: Our results revealed a segregation between diploid and hexaploid cytotypes in the nuclear genome, where each cytotype represents a monophyletic lineage probably homogenized by concerted evolution. In contrast, the chloroplast genome showed intermixed connections between the cytotypes, which may correspond to shared ancestral relationships. Phylogeny, demographic analyses and ecological niche modelling supported an ongoing differentiation of the cytotypes, where the hexaploid cytotype is experiencing a demographic expansion and niche differentiation with respect to its diploid relative. CONCLUSIONS: The two cytotypes may be considered as two different lineages at the onset of their evolutionary diversification. Polyploidization led to the occurrence of hexaploids, which expanded and changed their ecological niche.
- MeSH
- Aster Plant genetics MeSH
- Biological Evolution * MeSH
- Models, Biological MeSH
- DNA, Chloroplast analysis MeSH
- Phylogeny * MeSH
- Phylogeography MeSH
- Genetic Markers MeSH
- DNA, Ribosomal Spacer analysis MeSH
- Polyploidy * MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Geographicals
- Europe MeSH
- Names of Substances
- DNA, Chloroplast MeSH
- Genetic Markers MeSH
- DNA, Ribosomal Spacer MeSH
BACKGROUND AND AIMS: Understanding the consequences of polyploidization is a major step towards assessing the importance of this mode of speciation. Most previous studies comparing different cytotypes, however, did so only within a single environment and considered only one group of traits. To take a step further, we need to explore multiple environments and a wide range of traits. The aim of this study was to assess response of diploid and autotetraploid individuals of Knautia arvensis (Dipsacaceae) to two stress conditions, shade or drought. METHODS: We studied eleven photosynthetic, morphological and fitness parameters of the plants over three years in a common garden under ambient conditions and two types of stress. KEY RESULTS: The results indicate strong differences in performance and physiology between cytotypes in ambient conditions. Interestingly, higher fitness in diploids contrasted with more efficient photosynthesis in tetraploids in ambient conditions. However, stress, especially drought, strongly reduced fitness and disrupted function of the photosystems in both cytotypes reducing the between cytotype differences. The results indicate that drought stress reduced function of the photosynthetic processes in both cytotypes but particularly in tetraploids, while fitness reduction was stronger in diploids. CONCLUSIONS: The photosynthesis related traits show higher plasticity in polyploids as theoretically expected, while the fitness related traits show higher plasticity in diploids especially in response to drought. This suggests that between cytotype comparisons need to consider multiple traits and multiple environments to understand the breath of possible responses of different cytotypes to stress. They also show that integrating results based on different traits is not straightforward and call for better mechanistic understanding of the relationships between species photosynthetic activity and fitness. Still, considering multiple environments and multiple species traits is crucial for understanding the drivers of niche differentiation between cytotypes in future studies.
- MeSH
- Stress, Physiological * MeSH
- Plant Physiological Phenomena * MeSH
- Grassland * MeSH
- Publication type
- Journal Article MeSH
Areas of immediate contact of different cytotypes offer a unique opportunity to study evolutionary dynamics within heteroploid species and to assess isolation mechanisms governing coexistence of cytotypes of different ploidy. The degree of reproductive isolation of cytotypes, that is, the frequency of heteroploid crosses and subsequent formation of viable and (partly) fertile hybrids, plays a crucial role for the long-term integrity of lineages in contact zones. Here, we assessed fine-scale distribution, spatial clustering, and ecological niches as well as patterns of gene flow in parental and hybrid cytotypes in zones of immediate contact of di-, tetra-, and hexaploid Senecio carniolicus (Asteraceae) in the Eastern Alps. Cytotypes were spatially separated also at the investigated microscale; the strongest spatial separation was observed for the fully interfertile tetra- and hexaploids. The three main cytotypes showed highly significant niche differences, which were, however, weaker than across their entire distribution ranges in the Eastern Alps. Individuals with intermediate ploidy levels were found neither in the diploid/tetraploid nor in the diploid/hexaploid contact zones indicating strong reproductive barriers. In contrast, pentaploid individuals were frequent in the tetraploid/hexaploid contact zone, albeit limited to a narrow strip in the immediate contact zone of their parental cytotypes. AFLP fingerprinting data revealed introgressive gene flow mediated by pentaploid hybrids from tetra- to hexaploid individuals, but not vice versa. The ecological niche of pentaploids differed significantly from that of tetraploids but not from hexaploids.
- Keywords
- Asymmetric gene flow, Senecio carniolicus (Asteraceae), contact zone, ecological niche, hybrid cytotypes, polyploidy,
- Publication type
- Journal Article MeSH
BACKGROUND AND AIMS: Despite the great importance of autopolyploidy in the evolution of angiosperms, relatively little attention has been devoted to autopolyploids in natural polyploid systems. Several hypotheses have been proposed to explain why autopolyploids are so common and successful, for example increased genetic diversity and heterozygosity and the transition towards selfing. However, case studies on patterns of genetic diversity and on mating systems in autopolyploids are scarce. In this study allozymes were employed to investigate the origin, population genetic diversity and mating system in the contact zone between diploid and assumed autotetraploid cytotypes of Vicia cracca in Central Europe. METHODS: Four enzyme systems resolved in six putative loci were investigated in ten diploid, ten tetraploid and five mixed-ploidy populations. Genetic diversity and heterozygosity, partitioning of genetic diversity among populations and cytotypes, spatial genetic structure and fixed heterozygosity were analysed. These studies were supplemented by a pollination experiment and meiotic chromosome observation. KEY RESULTS AND CONCLUSIONS: Weak evidence of fixed heterozygosity, a low proportion of unique alleles and genetic variation between cytotypes similar to the variation among populations within cytotypes supported the autopolyploid origin of tetraploids, although no multivalent formation was observed. Tetraploids possessed more alleles than diploids and showed higher observed zygotic heterozygosity than diploids, but the observed gametic heterozygosity was similar to the value observed in diploids and smaller than expected under panmixis. Values of the inbreeding coefficient and differentiation among populations (ρST) suggested that the breeding system in both cytotypes of V. cracca is mixed mating with prevailing outcrossing. The reduction in seed production of tetraploids after selfing was less than that in diploids. An absence of correlation between genetic and geographic distances and high differentiation among neighbouring tetraploid populations supports the secondary contact hypothesis with tetraploids of several independent origins in Central Europe. Nevertheless, the possibility of a recent in situ origin of tetraploids through a triploid bridge in some regions is also discussed.
- Keywords
- Autopolyploidy, F-statistics, Vicia cracca, allozymes, artificial pollination, fixed heterozygosity, genetic differentiation, genetic diversity, heterozygosity, inbreeding depression, mating system, meiotic chromosomes,
- MeSH
- Alleles MeSH
- Diploidy * MeSH
- Genetic Variation * MeSH
- Heterozygote MeSH
- Isoenzymes genetics MeSH
- Pollination genetics MeSH
- Genetics, Population * MeSH
- Self-Fertilization genetics MeSH
- Seeds genetics MeSH
- Tetraploidy * MeSH
- Vicia genetics MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Geographicals
- Czech Republic MeSH
- Europe MeSH
- Slovakia MeSH
- Names of Substances
- Isoenzymes MeSH