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Examples of predicted time course of proportions of individual ploidy levels. Plants are assumed to be monocarpic with no clonal growth (Simple Model) and are parameterized with the data from the crossing experiment. a The initial proportion of diploids:tetraploids 0.5:0.5. b The initial proportion of diploids:tetraploids 0.45:0.55. These proportions have been selected to illustrate that small changes in initial proportions are predicted to lead to very different outcomes. For the full mapping of the space of initial conditions, see Fig. 3
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Background:
Processes driving ploidal diversity at the population level are virtually unknown. Their identification should use a combination of large-scale screening of ploidy levels in the field, pairwise crossing experiments and mathematical modelling linking these two types of data. We applied this approach to determine the drivers of frequenci...
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Citations
... This is a critical step because neoautopolyploids immediately face reduced fitness due to chromosomally unbalanced or even aborted gametophytes and/or gametes (see above), and density-dependent hybridization with the more common parental cytotype often resulting in nonviable progeny (minority-cytotype exclusion; Levin, 1975). Although P. rhodopea can, at least partially, mitigate the negative effect of the triploid block, neoautopolyploids produce so few seeds that their establishment and maintenance in a sympatric population would be highly problematic if they relied solely on sexual reproduction-an assumption supported by a simulation study of a mixedploidy Pilosella echioides (Chrtek et al., 2017). ...
... Indeed, previous extensive crossing experiments often found a certain fraction of such tetraploid hybrids, demonstrating that this pathway may act in addition to a triploid bridge (e.g. van Dijk and van Delden 1990; Burton and Husband 2001;Chrtek et al. 2017;Sutherland and Galloway 2017;Castro et al. 2020;Morgan et al. 2021). Although we did not encounter such a hybrid in our limited crossing experiment, the observation of a tetraploid seedling among the progeny of a diploid seed parent sampled in population HLI demonstrates that unreduced gametes of diploids may also be involved in tetraploid formation in the field. ...
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.
... However, in Salony et al. (2024), similar experimental crosses in M. guttatus revealed a strong barrier to triploid formation in both directions, resulting in nongerminable seeds. Further evidence for better survival of paternal excess hybrids comes from Pilosella echioides (Asteraceae): 44% viability in maternal excess compared with 66% in paternal excess (Chrtek et al., 2017). Importantly, the high viability is unlikely to be due to self-pollination as the species was shown to be self-incompatible in this study. ...
... However, this does not consistently follow a trend, as some taxa with nuclear endosperm deviate from this pattern. For instance, in rye (Secale cereale), the viability rates are 47.2% in paternal excess and 30% in maternal excess (Håkansson and Ellerström, 1950), and in P. echioides, the rates are 66% in paternal excess crosses and 44% in maternal excess (Chrtek et al., 2017). ...
... Similarly, reciprocal hybrids in Galeopsis and Oenothera are barely viable (Hákansson, 1952;von Wangenheim, 1962). However, in taxa such as Cyclamen and Pilosella (Takamura and Miyajima, 1996;Chrtek et al., 2017), reciprocal interploidy crosses exhibit relatively higher hybrid viability, despite these species sharing the common characteristics of having a permanent endosperm. On the other hand, in taxa with a transient endosperm, the variation also ranges from mostly viable seeds in crosses with higher maternal dosage, as observed in Arabidopsis and Brassica (Scott et al., 1998;Stoute et al., 2012), to the near absence of viable seeds in reciprocal crosses in Mimulus (Meeus et al., 2020;Salony et al., 2024). ...
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 triploid block across 11 angiosperm families. We particularly 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, likely 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 of 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.
... Models predicting success (i.e., individual establishment, followed by population persistence) of a neoautopolyploid have found that success is increased by reproductive assurance through selfing (Rodriguez 1996;Baack 2005;Rausch and Morgan 2005;Oswald and Nuismer 2011) or clonality (Chrtek et al. 2017;Van Drunen and Friedman 2022). In naturally occurring populations, autopolyploids have been observed to experience shifts in mating system, often to facultative reproductive systems with both asexual and sexual methods of reproduction (Barringer 2007;Husband et al. 2008). ...
The population dynamics of autopolyploids—organisms with more than two genome copies of a single species—and their diploid progenitors have been extensively studied. The acquisition of multiple genome copies is heavily influenced by stochasticity, which strongly suggests the efficacy of a probabilistic approach to examine the long-term dynamics of a population with multiple cytotypes. Yet our current understanding of the dynamics of autopolyploid populations has not incorporated stochastic population dynamics and coexistence theory. To investigate the factors contributing to the probability and stability of coexisting cytotypes, we designed a new population dynamics model that incorporates demographic and environmental stochasticities to simulate the formation, establishment, and persistence of diploids, triploids, and autotetraploids in the face of gene flow among cytotypes. We found that increased selfing rates and pronounced reproductive isolation promote coexistence of multiple cytotypes. In stressful environments and with strong competitive effects among cytotypes, these dynamics are more complex; our stochastic modeling approach reveals the resulting intricacies that give autotetraploids competitive advantage over their diploid progenitors. Our work is foundational for a better understanding of the dynamics of coexistence of multiple cytotypes.
... Species with widespread asexual reproduction often have a relatively high frequency of triploids (e.g. Karpavi cien_ e, 2017; Chung et al., 2015), indicating that the triploid disadvantages mainly affect sexual reproduction rather than vegetative growth (Chrtek et al., 2017). In clonal species, the sterility and low-seed viability of triploids have less impact on fitness because of a lower reliance on sexual reproduction (Barrett, 2015). ...
The relationship between polyploid formation, triploid fitness and plant reproduction has been studied for over a century, and uniparental reproduction has long been recognized to play a crucial role in polyploid establishment. Yet, we lack a synthesized framework of how polyploid establishment is expected to be influenced by different reproductive modes among angiosperms. Here, we provide new perspectives on how uniparental reproduction, pollination ecology, triploid fitness and assortative mating can impact minority cytotype exclusion (MCE) and, thereby, the likelihood of polyploid establishment. We review the current state of knowledge of the reproductive mechanisms that impact polyploid establishment and discuss often overlooked aspects of these processes, such as the influence of pollinator communities on rates of self‐pollination. We propose a framework for considering how variation in reproductive strategies and pollinator communities can impact the ability of a polyploid to overcome MCE. Finally, we propose links between patterns of variation in uniparental reproduction across plant communities and observed patterns in the distribution and abundance of polyploids.
... However, in Salony et al. (2024), similar experimental crosses in M. guttatus revealed a strong barrier to triploid formation in both directions, resulting in nongerminable seeds. Further evidence for better survival of paternal excess hybrids comes from Pilosella echioides (Asteraceae): 44% viability in maternal excess compared with 66% in paternal excess (Chrtek et al., 2017). Importantly, the high viability is unlikely to be due to self-pollination as the species was shown to be self-incompatible in this study. ...
... However, this does not consistently follow a trend, as some taxa with nuclear endosperm deviate from this pattern. For instance, in rye (Secale cereale), the viability rates are 47.2% in paternal excess and 30% in maternal excess (Håkansson and Ellerström, 1950), and in P. echioides, the rates are 66% in paternal excess crosses and 44% in maternal excess (Chrtek et al., 2017). ...
... Similarly, reciprocal hybrids in Galeopsis and Oenothera are barely viable (Hákansson, 1952;von Wangenheim, 1962). However, in taxa such as Cyclamen and Pilosella (Takamura and Miyajima, 1996;Chrtek et al., 2017), reciprocal interploidy crosses exhibit relatively higher hybrid viability, despite these species sharing the common characteristics of having a permanent endosperm. On the other hand, in taxa with a transient endosperm, the variation also ranges from mostly viable seeds in crosses with higher maternal dosage, as observed in Arabidopsis and Brassica (Scott et al., 1998;Stoute et al., 2012), to the near absence of viable seeds in reciprocal crosses in Mimulus (Meeus et al., 2020;Salony et al., 2024). ...
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 triploid block across angiosperms. We particularly assessed the impact of interploidy cross direction, types of endosperm development, endosperm persistence at seed maturity, and ploidy divergence. None of these factors had a significant impact on triploid seed viability, likely 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 of 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.
... Newly formed polyploid individuals, by necessity, emerge in an existing diploid parental population, creating a majority cytotype (the parent diploid) and a minority cytotype (the newly emergent polyploid; Levin, 1975). The new polyploid is exposed to minority cytotype exclusion (MCE; Levin, 1975), a frequency-dependent process whereby the minority cytotype is at a reproductive disadvantage through the compounded effects of high frequencies of interploid crosses (since initially only the majority cytotype is available for breeding; Chrtek et al., 2017). If successful intercytotype reproduction is possible, then higher-ploidy cytotypes may be produced by way of a triploid bridge (Burton and Husband, 2001;Yamauchi et al., 2004;Peckert and Chrtek, 2006). ...
... Therefore, other mechanisms may be important for the establishment of polyploids. Polyploids may achieve higher levels of fitness through increased potential for selffertilization and clonal reproduction (Levin, 1975;Rodríguez, 1996;Nakayama et al., 2002;Mable, 2004;Yamauchi et al., 2004;Rausch and Morgan, 2005;Hörandl and Hojsgaard, 2012;Hojsgaard et al., 2014;Hojsgaard and Hörandl, 2019;Husband, 2018, 2019;Spoelhof et al., 2020), potentially prolonged lifecycles/ iteroparity (Rodríguez, 1996), and perenniality (Gustafsson, 1948;Stebbins, 1950;Rodríguez, 1996;te Beest et al., 2012;Chrtek et al., 2017). Strategies that result in prolonged lifecycles or increased perenniality create the potential for an individual to persist long enough for a compatible mate to arise. ...
Premise
Polyploidy is a major factor in plant adaptation and speciation. Multiple mechanisms contribute to autopolyploid frequency within populations, but uncertainties remain regarding mechanisms that facilitate polyploid establishment and persistence. Here we aimed to document and predict cytotype distributions of Oxalis obliquifolia Steud. ex A. Rich. across Gauteng, South Africa, and test for evidence of possible mechanisms, including morphological, phenological, and reproductive traits, that may potentially facilitate polyploid persistence.
Methods
Over 320 O. obliquifolia plants from 25 sites were cytotyped using flow cytometry, and DNA ploidy was confirmed using meiotic chromosome squashes. Cytotypes were mapped and correlations with abiotic variables assessed using ordinations. To assess morphological and phenological associations with cytotype, we grew multiple cytotypes in a common garden, measured phenotypic traits and compared them using linear models and discriminant analyses. Intercytotype reproductive isolation was assessed using crossing experiments, and AMOVAs based on ITS DNA sequences tested for cytogeographic structure.
Results
Six cytotypes were identified, and most sites had multiple cytotypes. Abiotic variables were not predictive of cytotype distribution. A clear gigas effect was present. Differences in flower size and phenology suggested pollinator interactions could play a role in polyploid persistence. Intercytotype crosses produced seed at low frequency. DNA data suggested diploids and polyploids were largely reproductively isolated in situ, and polyploidization events were not frequent enough to explain high cytotype sympatry.
Conclusions
Diploids and polyploids are behaving as separate species, despite little observable niche differentiation and non‐zero potential intercytotype seed set. Tests on biotic interactions and intercytotype F1 fitness may provide insights into diploid and polyploid coexistence.
... For example, fitness advantages may arise for a recently derived, rare cytotype if it exhibits greater pathogen resistance (Oswald and Nuismer, 2007;Mehlferber et al., 2022), better adaptation to the local habitat (Li et al., 2004;Garmendia et al., 2018), or ploidy-specific pollinator differentiation, such that intraploidy competition is stronger than interploidy competition (Rodríguez, 1996;Fowler and Levin, 2016;López-Jurado et al., 2019). However, there are few empirical tests of such models (Husband, 2000;Chrtek et al., 2017), in part due to the challenges associated with conducting such experiments. ...
Premise
Theory predicts that mixed ploidy populations should be short‐lived due to strong fitness disadvantages for the rare ploidy. However, mixed ploidy populations are common, suggesting that the fitness costs for rare ploidies are counterbalanced by ecological benefits that emerge when rare. We investigated whether differences in ecological interactions with soil microbes help to maintain a tetraploid–hexaploid population of Larrea tridentata (creosote bush) in the Sonoran Desert, California, United States, where prior work documented ploidy‐specific root‐associated microbes.
Methods
We used a plant–soil feedback (PSF) experiment to test whether host‐specific soil microbes can alter the outcomes of intraploidy vs. interploidy competition. Host‐specific soil microbes can build up over time; thus, distance from a host plant can affect the fitness of nearby plants.
Results
Seedlings grown in soils from near plants of a different ploidy produced greater biomass relative to seedlings grown in soils from near plants of the same ploidy. Moreover, seedlings grown in soils from near plants of a different ploidy produced more biomass than those grown in soils that were farther from plants of a different ploidy. These results suggest that the ecological consequences of PSF may facilitate the persistence of mixed ploidy populations.
Conclusions
This is the first evidence, to our knowledge, that is consistent with plant–soil microbe feedback as a viable mechanism to maintain the coexistence of multiple ploidy levels in a single population.
... Alterations in reproductive strategies following WGM may counteract the disadvantages of a minority cytotype, e.g. by tolerating higher rates of autogamy [16] or by triggering/promoting asexual reproduction [17]. Asexuality can be achieved through the production of apomictically formed seeds, where meiosis and syngamy are bypassed [18] or through vegetative propagation [19][20][21]. Many apomicts are autopolyploids, particularly among grasses [22,23], and WGM is the primary cause of apomixis among these species, while hybridization seems to play a significant role in known allopolyploid apomicts [24,25]. ...
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 (rootsprouting), 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.
... Importantly, these patterns are scale-dependent; the coexistence of cytotypes is likely over larger spatial scales, while at shorter distances ploidy-uniform clusters prevailed (Trávníček et al. 2011a;Šingliarová et al. 2019). Non-random cytotype distribution over small spatial scales can be linked to strong cytotype exclusion, clonal reproduction (Chrtek et al. 2017;Duchoslav et al. 2020), different microhabitat preferences (Fowler and Levin 1984;Sonnleitner et al. 2010) or non-adaptive processes, like a founder event with subsequent seed dispersal limitation (Baack 2005;Mráz et al. 2012b). ...
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 reassessed the microspatial distribution of diploids and tetraploids and their affinities to varying vegetation-cover density in three mixed-ploidy populations in Central Europe. 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 co-existing 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.
