Nejvíce citovaný článek - PubMed ID 28335715
Cytotype coexistence in the field cannot be explained by inter-cytotype hybridization alone: linking experiments and computer simulations in the sexual species Pilosella echioides (Asteraceae)
The triploid block, primarily caused by endosperm developmental issues, is known as a significant barrier to interploidy hybridization among flowering plants and, thereby, polyploid speciation. However, its strength varies across taxa, with some instances of leakiness, questioning its universal role as a barrier. We conducted a literature survey to explore the causes of the variation in the strength of the triploid block across 11 angiosperm families. We assessed the impact of interploidy cross direction, types of endosperm development, endosperm persistence at seed maturity, and divergence between cytotypes using a Bayesian meta-analysis. We found a significant influence of the type of endosperm in shaping variation in triploid block strength. Other factors tested had no impact on triploid seed viability, probably due to limited data and inconsistencies in estimation methods across the literature. In addition, triploid seed viability in experimental crosses was sometimes correlated to the occurrence of triploid hybrids in nature, sometimes not, suggesting a mixed role for the triploid block in shaping interspecies gene flow. Altogether, our study highlights the need for unified approaches in future studies on the triploid block to advance our understanding of its variation and evolutionary implications.
- Klíčová slova
- Endosperm development, hybrid seed lethality, interploidy gene flow, natural variation, polyploidy speciation, triploid block,
- MeSH
- biologická evoluce * MeSH
- endosperm genetika růst a vývoj MeSH
- hybridizace genetická MeSH
- Magnoliopsida * genetika MeSH
- polyploidie * MeSH
- semena rostlinná genetika MeSH
- tok genů MeSH
- triploidie * MeSH
- vznik druhů (genetika) * MeSH
- Publikační typ
- časopisecké články MeSH
- metaanalýza MeSH
- přehledy MeSH
Polyploidisation is a significant reproductive barrier, yet genetic evidence indicates that interploidy admixture is more common than previously thought. Theoretical models and controlled crosses support the 'triploid bridge' hypothesis, proposing that hybrids of intermediate ploidy facilitate gene flow. However, comprehensive evidence combining experimental and genetic data from natural mixed-ploidy species is missing. Here, we investigated the rates and directionality of gene flow within a diploid-autotetraploid contact zone of Cardamine amara, a species with abundant natural triploids. We cytotyped over 400 individuals in the field, conducted reciprocal interploidy crosses, and inferred gene flow based on genome-wide sequencing of 84 individuals. Triploids represent a conspicuous entity in mixed-ploidy populations (5%), yet only part of them arose through interploidy hybridisation. Despite being rarely formed, triploid hybrids can backcross with their parental cytotypes, producing viable offspring that are often euploid (in 42% of cases). In correspondence, D-statistics and coalescent simulations documented a significant genome-wide signal of bidirectional gene flow in sympatric but not allopatric populations. Triploids, though rare, thus seem to play a key role in overcoming polyploidy-related reproductive barriers in C. amara. In sum, we present integrative evidence for interploidy gene flow mediated by a triploid bridge in natural populations.
- Klíčová slova
- introgression, polyploidy, population genomics, speciation, whole genome duplication,
- MeSH
- Cardamine * genetika MeSH
- genová introgrese * MeSH
- hybridizace genetická MeSH
- ploidie * MeSH
- polyploidie MeSH
- populační genetika MeSH
- tok genů * MeSH
- triploidie * MeSH
- Publikační typ
- časopisecké články MeSH
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.
- Klíčová slova
- Adaptation, evolution, genetic introgression, polyploidy, speciation, whole-genome duplication,
- MeSH
- biologická evoluce MeSH
- genom rostlinný genetika MeSH
- ploidie MeSH
- polyploidie * MeSH
- rostliny genetika MeSH
- rozmnožování genetika MeSH
- tok genů * MeSH
- vznik druhů (genetika) MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
Exploring the fitness consequences of whole-genome multiplication (WGM) is essential for understanding the establishment of autopolyploids in diploid parental populations, but suitable model systems are rare. We examined the impact of WGM on reproductive traits in three major cytotypes (2x, 3x, 4x) of Pilosella rhodopea, a species with recurrent formation of neo-autopolyploids in mixed-ploidy populations. We found that diploids had normal female sporogenesis and gametogenesis, high fertility, and produced predominantly euploid seed progeny. By contrast, autopolyploids had highly disturbed developmental programs that resulted in significantly lower seed set and a high frequency of aneuploid progeny. All cytotypes, but particularly triploids, produced gametes of varying ploidy, including unreduced ones, that participated in frequent intercytotype mating. Noteworthy, the reduced investment in sexual reproduction in autopolyploids was compensated by increased production of axillary rosettes and the novel expression of two clonal traits: adventitious rosettes on roots (root-sprouting), and aposporous initial cells in ovules which, however, do not result in functional apomixis. The combination of increased vegetative clonal growth in autopolyploids and frequent intercytotype mating are key mechanisms involved in the formation and maintenance of the largest diploid-autopolyploid primary contact zone ever recorded in angiosperms.
- Klíčová slova
- aneuploidy, apospory, clonality, mixed-ploidy, root-sprouting, unreduced gametes,
- MeSH
- diploidie MeSH
- fertilita * MeSH
- ploidie * MeSH
- polyploidie MeSH
- rozmnožování MeSH
- semena rostlinná MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Spatial segregation of cytotypes reduces the negative effect of frequency-dependent mating on the fitness of minority cytotype(s) and thus allows its establishment and coexistence with the majority cytotype in mixed-ploidy populations. Despite its evolutionary importance, the stability of spatial segregation is largely unknown. Furthermore, closely related sympatric cytotypes that differ in their life histories might exhibit contrasting spatial dynamics over time. We studied the temporal stability of spatial structure at a secondary contact zone of co-occurring monocarpic diploids and polycarpic tetraploids of Centaurea stoebe, whose tetraploid cytotype has undergone a rapid range expansion in Europe and became invasive in North America. Eleven years after the initial screening, we re-assessed the microspatial distribution of diploids and tetraploids and their affinities to varying vegetation-cover density in three mixed-ploidy populations in Central Europe. We found that overall, spatial patterns and frequencies of both cytotypes in all sites were very similar over time, with one exception. At one site, in one previously purely 2x patch, diploids completely disappeared due to intensive succession by shrubby vegetation. The remaining spatial patterns, however, showed the same cytotype clumping and higher frequency of 2x despite subtle changes in vegetation-cover densities. In contrast to the expected expansion of polycarpic tetraploids having higher colonization ability when compared to diploids, the tetraploids remained confined to their former microsites and showed no spatial expansion. Spatial patterns of coexisting diploids and tetraploids, which exhibit contrasting life histories, did not change over more than a decade. Such temporal stability is likely caused by relatively stable habitat conditions and very limited seed dispersal. Our results thus imply that in the absence of a disturbance regime connected with frequent human- or animal-mediated seed dispersal, spatial patterns may be very stable over time, thus contributing to the long-term coexistence of cytotypes.
- Klíčová slova
- Centaurea stoebe, colonization, cytotype coexistence, disturbance, flow cytometry, invasion, mixed-ploidy population, polycarpy, polyploidy, secondary contact zone, spatial cytotype structure, spatial segregation,
- Publikační typ
- časopisecké články MeSH
BACKGROUND AND AIMS: Polyploidy has played an important role in the evolution of ferns. However, the dearth of data on cytotype diversity, cytotype distribution patterns and ecology in ferns is striking in comparison with angiosperms and prevents an assessment of whether cytotype coexistence and its mechanisms show similar patterns in both plant groups. Here, an attempt to fill this gap was made using the ploidy-variable and widely distributed Cystopteris fragilis complex. METHODS: Flow cytometry was used to assess DNA ploidy level and monoploid genome size (Cx value) of 5518 C. fragilis individuals from 449 populations collected over most of the species' global distributional range, supplemented with data from 405 individuals representing other related species from the complex. Ecological preferences of C. fragilis tetraploids and hexaploids were compared using field-recorded parameters and database-extracted climate data. KEY RESULTS: Altogether, five different ploidy levels (2x, 4x, 5x, 6x, 8x) were detected and three species exhibited intraspecific ploidy-level variation: C. fragilis, C. alpina and C. diaphana. Two predominant C. fragilis cytotypes, tetraploids and hexaploids, co-occur over most of Europe in a diffuse, mosaic-like pattern. Within this contact zone, 40 % of populations were mixed-ploidy and most also contained pentaploid hybrids. Environmental conditions had only a limited effect on the distribution of cytotypes. Differences were found in the Cx value of tetraploids and hexaploids: between-cytotype divergence was higher in uniform-ploidy than in mixed-ploidy populations. CONCLUSIONS: High ploidy-level diversity and widespread cytotype coexistence in the C. fragilis complex match the well-documented patterns in some angiosperms. While ploidy coexistence in C. fragilis is not driven by environmental factors, it could be facilitated by the perennial life-form of the species, its reproductive modes and efficient wind dispersal of spores. Independent origins of hexaploids and/or inter-ploidy gene flow may be expected in mixed-ploidy populations according to Cx value comparisons.
- Klíčová slova
- Cystopteris fragilis, Bladder ferns, Cx value, contact zone, cytotype coexistence, ecological preferences, flow cytometry, genome size, ploidy distribution, pteridophytes,
- MeSH
- ekologie MeSH
- hybridizace genetická MeSH
- kapradiny * MeSH
- lidé MeSH
- ploidie MeSH
- polyploidie MeSH
- Check Tag
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Evropa MeSH