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New Phytol. Author manuscript; available in PMC 2010 November 19.
Published in final edited form as:
PMCID: PMC2988484

Hybrid speciation in angiosperms: parental divergence drives ploidy


  • Hybridization and polyploidy are now hypothesized to have regularly stimulated speciation in angiosperms, but individual or combined involvement of these two processes seems to involve significant differences in pathways of formation, establishment and evolutionary consequences of resulting lineages. We evaluate here the classical cytological hypothesis that ploidy in hybrid speciation is governed by the extent of chromosomal rearrangements among parental species.
  • Within a phylogenetic framework, we calculate genetic divergence indices for 50 parental species pairs and use these indices as surrogates for the overall degree of genomic divergence (i.e. as proxy for assessments of dissimilarity of the parental chromosomes).
  • The results confirm that genomic differentiation between progenitor taxa influences the likelihood of diploid (homoploid) versus polyploid hybrid speciation because genetic divergence between parents of polyploids is found to be significantly greater than in the case of homoploid hybrid species.
  • We argue that this asymmetric relationship may be reinforced immediately after hybrid formation, during stabilization and establishment. Underlying mechanisms potentially producing this pattern are discussed.
Keywords: adaptation, allopolyploidy, homoploid hybrid, hybridization, parental divergence, polyploidy, speciation


At first glance hybridization might seem “a reversal in the process of evolutionary divergence” (Grant, 1981, p. 195), but in fact hybridization appears to regularly stimulate plant speciation: the combination of different genomes in hybrid lineages has extensive evolutionary and ecological implications, potentially facilitating evolutionary innovation and adaptive radiation (Anderson, 1949; Stebbins, 1950; Grant, 1981; Arnold, 1997; Barton, 2001; Rieseberg et al., 2003; Seehausen, 2004; Mallet, 2007; Paun et al., 2007).

Hybrid speciation refers to the mode of origin of a new species in which gene flow between species plays a major role. More than 25% of plant species seem to be involved in hybridization with other species (Mallet, 2005), but its frequency seems to vary considerably between groups, for example being more prevalent in rapidly radiating lineages (see Ellstrand et al., 1996). Closely related species are most likely to hybridize, but this phenomenon often persists for millions of years after initial diversification (Mallet, 2005). The rate of hybrid speciation is definitely much lower than the statistic of 25% due to many disadvantages that early generation hybrids need to overcome to achieve successful establishment (e.g., reduced fertility and viability, lack of reproductive and ecological isolation from the parents, lack of mates of the same type, hybrid dysgenesis and necrosis, etc.). An estimate from five regional floras indicated that c. 11% of species are putative hybrids (Ellstrand et al., 1996).

Homoploid hybrid speciation (“recombinational”, sensu Grant, 1981) appears to be facilitated by several factors, e.g., availability of a suitable ecological niche or an available fitness peak, and rapid chromosomal evolution (Rieseberg, 1997; Mallet, 2007). To be evolutionarily successful, even fertile and “stable” homoploid hybrids must be reproductively isolated from the parental species either by sorting genic or chromosomal sterility factors that already differentiate the parental species (Grant, 1981; Rieseberg, 2001; Wu, 2001) or by pre-zygotic barriers, such as spatial/temporal isolation and/or divergence into a new ecological niche (Rieseberg, 1997; Gross & Rieseberg, 2005). Indeed, hybrids may combine characteristics from both parents and/or exhibit transgressive traits that allow ecological distinctiveness (Andersson, 1949; Arnold, 1997; Rieseberg et al., 2003; Seehausen, 2004).

Homoploid hybrid speciation seems to proceed at a rapid tempo (Rieseberg et al., 1996; Rieseberg, 1997; Buerkle & Rieseberg, 2008), and diploid hybrid genomes are likely to be stabilized quickly, for example after 10-60 generations in the case of Helianthus anomalus (Ungerer et al., 1998). Buerkle and Rieseberg (2008) have recently shown, however, that in Helianthus recombination continues to shape genomic composition of homoploid hybrid species for hundreds of generations. Even at this scale, diploid hybrid speciation can still be considered one of the fastest modes of speciation.

Hybrid speciation may, however, happen much more suddenly when combined with polyploidy, which immediately provides a hybrid with a high degree of post-zygotic reproductive isolation from its progenitors: backcrossing to either parent will produce inviable or mostly sterile offspring of odd-numbered ploidy (triploids, pentaploids etc.: Stebbins, 1950, p. 308; Grant, 1981; Ramsey & Schemske, 1998). Allopolyploidy can be the product of gametic non-reduction (frequently via a “triploid bridge”; Ramsey & Schemske, 1998), and, more rarely, can also result from somatic chromosome doubling of a homoploid hybrid or polyspermy (Thompson & Lumaret, 1992; Ramsey & Schemske, 1998; Mallet, 2007). Of all these pathways, non-reduction during meiosis seems to be the most frequent route to polyploidy, as parents of spontaneous polyploids often produce a substantial number of unreduced gametes (see reviews by Thompson & Lumaret, 1992; Ramsey & Schemske, 1998).

Even if allopolyploidy can be viewed as abrupt or saltational speciation (Mallet, 2007), most neopolyploids will fail to become established because of meiotic abnormalities (Ramsey & Schemske, 2002) and/or their isolation, resulting in a frequency-dependent minority cytotype disadvantage (Husband, 2000). However, the latter may be overcome with the help of perenniality, asexual reproduction, assortative mating and loss of self-incompatibility barriers. Originating in sympatry (or parapatry) with progenitors, allopolyploids still require niche divergence to escape direct competition with parental taxa (Coyne & Orr, 2004). The co-joined genomes in polyploids usually have to face a complicated process of reorganization before full stabilization: chromosomal rearrangements within parental genomes, loss of low-copy DNA sequences, epigenetic effects on expression in duplicated genes and activation of transposable elements (reviews e.g., in Comai, 2005; Chen, 2007; Paun et al., 2007). Such genomic responses also have the potential to induce novel expression patterns, which together with permanent heterozygosity (potentially resulting in hybrid vigor) and gene redundancy, might result in significant shifts in morphology, breeding system and ecological tolerances, and, finally, in elevated evolutionary potential and major “jumps” in evolution (De Bodt & al., 2005; Comai, 2005; Otto, 2007; Paun et al., 2007).

Speciation via polyploidy is likely to be a major mode of sympatric speciation in plants. A model-based estimated frequency of polyploid (usually allopolyploid) speciation in angiosperms points to at least 2-4% of recent speciation events (Otto & Whitton, 2000). However, recent direct estimates indicate that 15 to 25% of angiosperm speciation events are accompanied by increase in ploidy (Wood & Rieseberg, 2005). Moreover, up to 70% of extant flowering plant species are currently polyploids (Otto & Whitton, 2000), and the rest have descended from polyploid ancestors and are paleopolyploids (NB. except probably Amborella; De Bodt et al., 2005; Cui et al., 2006). Meyers and Levin (2006) suggested that the abundance of polyploids may result from a simple ratcheting mechanism; they argued that in evolution chromosome number can double but not halve. However, genome size (as DNA amount and chromosome number) can decrease, for example as observed in Nicotiana sect. Suaveolentes where multiple chromosome fusions resulted in chromosome number reduction (Chase et al., 2003).

Because polyploidy and hybridization have been so central to plant evolution, it is important to identify processes responsible for origins of hybrid species and those that promote shifts in ploidy, changing the possible outcomes of hybrid speciation. The interest here is not simply limited to predicting results of hybrid evolution and of polyploid dynamics but is also of great importance for our understanding of evolutionary processes that result in isolation between species, including those that influence establishment of new taxa and maintain biodiversity.

A relevant hypothesis was proposed in the early 20th century: the level of (structural) differentiation between ancestor genomes influences ploidy of successful hybrids (e.g., Winge, 1917; Darlington, 1937; Stebbins, 1950). Winge (1917, as cited by Darlington, 1937), for example, considered that polyploid formation after somatic doubling of homoploid hybrids would be stimulated by the need for a partner with which chromosomes could pair. Therefore, higher chromosomal differentiation between parents would increase the chance of shifts in ploidy. Decades later, Grant (1981, p. 247-248 and 320) referring also to the initial formation of an allopolyploid, stated that pre-existing chromosomal rearrangements within parental genomes “upset the course of meiosis in the hybrid”, resulting in reduced pairing, and that the latter “sets [the stage] for [gamete] nonreduction and amphiploid formation”. Other authors extended this idea by referring more to the moment of polyploid establishment, rather than initiation. Darlington (1937, p.136), for example wrote: “the characteristic properties of hybrids depend not on the properties of the parents, but on the differences between these properties”. He considered that a “differential affinity” between parental chromosomes governs long-term successful pairing in structural hybrids and polyploids (pp. 160, 172 and 199): “The greater the [parental] dissimilarities, the more regularly do the identical chromosomes pair in the allotetraploid derived, and therefore the less frequent are the multivalents in the tetraploid”. In 1945 Clausen et al. (as cited by Buggs et al., 2008) reached the conclusion that the “success and constancy” of allopolyploids must be linked with the “degree of relationships” found between their parents. Even Stebbins (1950, p. 354) referred to the genetic relationships of the parental diploid species to each other as one of the factors promoting development of allopolyploidy in plants.

The potential cause-effect relationship between the level of chromosomal (genetic) divergence of the parents and ploidy of hybrids has recently been revisited by Chapman & Burke (2007) and Buggs et al. (2008), who, from different perspectives, reached partly contradictory conclusions. Based on 11 cases of homoploid hybrids (plus a misclassified polyploid Eupatorium) and 26 cases of allopolyploids, Chapman & Burke (2007) demonstrated that, in angiosperms, parental nuclear ribosomal ITS divergence is significantly greater for allopolyploids than for homoploid hybrids. However, the method employed disregarded the variable substitution rates expected across such unrelated cases even in the same molecular marker (a caveat discussed by the authors as well), and they included in the analysis hybrids formed by parents with different basic chromosome numbers (e.g., Arabidopsis suecica, Spiranthes diluvialis, Symphyotricum ascendens) or even different ploidies (Artemisia douglasiana, Primula scotica, Rubus maximus). Hybrid speciation starting from such parental pairs is particularly prone to result in allopolyploids and might follow special routes and rules (see Ramsey & Schemske, 1998). In contrast, Buggs and collaborators (2008) took a molecular phylogenetic approach to the issue, but relied on subjectively defined clades as a measure of genetic divergence. Moreover, the latter study considered any naturally occurring hybrid individual reported in the literature within eight selected plant genera and, therefore, focused on polyploid formation, not evolutionary success (effective speciation). Long-term success in meiosis is key to operation of the mechanism that governs ploidal shifts, which means that only taxa that appear to be valid species in their own right should be included in the calculations. Therefore, by including ephemeral homoploid hybrids, sterile triploids and neopolyploids, Buggs et al. did not directly evaluate the classical cytological hypothesis and failed to find convincing evidence showing that ploidal increase in established species is determined by the phylogenetic distance between progenitor species. However, their findings point to a restriction of homoploid formation to parental pairs less divergent than expectation if crossings were random between all species pairs in a genus.

In the light of this recent debate, we approach the potential relationship between ancestor divergence-descendant ploidy by uniting methodologically the two recent studies mentioned above. Like Chapman & Burke (2007) we use the extent of genetic divergence between parental pairs as a surrogate for chromosomal differentiation, but we attempt to standardize the method by taking into account the rate of evolution in the respective marker(s) and genus from a phylogenetic approach. We extend the sampling to more cases, but we include only diploid parental pairs with identical base chromosome numbers and only fertile, successful hybrids that have a long species history.

Material and Methods

Selection of taxa

This analysis is based on 50 case studies (Table 1) chosen from the literature following several rules: (i) the hybrid status for the respective species has been documented with some certainty by molecular means in addition to (at least) morphology; (ii) an extensive and representative molecular phylogenetic analysis for the genus including the parental taxa was already available; (iii) the parents are diploids and have the same chromosome number; and (iv) the hybrids are natural and stable, with proven evolutionary success (neopolyploids and unnamed suspected hybrids were excluded). Due to methodological constraints, we did not consider in our analysis intergeneric hybrids (e.g., allotetraploid Triticum turgidum), hybrids produced by more than two parents (e.g., homoploid hybrid Iris nelsonii) or hybrids from genera of uncertain delimitation (e.g., Tarasa and Brassica). The last exclusions were followed to try to minimize the influence of clerly artificial taxonomies.

Table 1
Details of hybrids included in this analysis. Taxonomy used follows the original papers. P-GDI: uncorrected P-derived parental genetic divergence index.

We classified the data into three categories: (1) homoploid hybrids (N = 16); (2) allopolyploids (N = 32); and (3) two cases of both diploid and polyploid hybrids formed by the same parental species (Table 1). We counted the parental pairs, so we considered just once the instances where more than one homoploid or polyploid hybrid was formed by the same parental pair. In this way, we were able to identify half as many homoploid hybrids as allopolyploid species. This pattern may result from a biological rarity of homoploid hybrid speciation versus allopolyploid speciation, but it also mirrors a more general problem, namely that detecting and rigorously documenting homoploid hybrid species is much more difficult than those with different ploidies (Rieseberg, 1997).

Molecular data and statistical analyses

Some DNA sequence matrices were obtained directly from authors of published analyses (see Acknowledgements); for the others, DNA sequences were collected from GenBank ( and re-aligned using Clustal W (; Chenna et al., 2003). Based only on ingroup taxa (species within genera), we calculated with PAUP* 4.0b10 (Swofford, 2003) all intrageneric pair-wise genetic distances, using both uncorrected p-distances (P) and Kimura’s (1980) two-parameter (K2P) distances. Uncorrected P is the observed number of changes between two sequences, with no correction for multiple changes. In contrast, the K2P model addresses this problem by considering equal base frequencies but different rates for transitions and transversions (Kimura, 1980).

Because species-level phylogenetic analyses use molecular markers exhibiting different substitution rates, we standardized our data among cases by calculating for each parental pair a genetic divergence index (GDI). For each instance, the genetic distance between parental pairs (Pd) was divided by the average genetic distance (Av) in the genus based on the same molecular markers. Under this definition, GDI is always positive; if GDI > 1.0, then Pd is higher than Av. When multiple sequences were available for a given taxon, an average of the genetic distance for all possible parental pairs was used in further analyses.

To check for potential bias in our analysis created by uneven sampling in phylogenetic trees, we performed a non-parametric, one-tailed Spearman rank order correlation of Av with the number of taxa included in each tree for both homoploid and allopolyploid species.

All statistical analyses were performed using SPSS 15.0 (SPSS, Chicago). As Pd, Av and GDI are not expected to be normally distributed, we treated our data as non-parametric.


The two genetic measures applied in this study, P and K2P, gave significantly congruent results (Spearman’s correlation coefficient based upon ranks Rho = 1, P < 0.0001, independently for Pd, Av and GDI). As expected, K2P values of Pd and Av were generally slightly higher then those calculated with P (Appendix 1). However, GDI values based on the two genetic distances were identical up to the second decimal, confirming the value of our standardizing approach. In the following tests, we generally focused on the P-derived GDI, due to simpler assumptions.

Nonparametric comparisons of GDI values (calculated overall, exclusively on nuclear data, or just with nuclear ribosomal ITS data) for homoploid versus polyploid hybrid species using the Mann-Whitney test indicated statistically significant asymmetric relationships (P < 0.0001, Table 2). Parents of polyploids are generally more divergent than the average intrageneric distance (i.e., GDI > 1), whereas for most homoploid hybrids GDI is less than 0.5 (Fig. 1). Additionally, in all cases of direct comparisons between homoploid and polyploid hybrids in the same genus (i.e., Achillea, Actinidia, Gossypium, Helianthus and Lithophragma; Table 1) parents of polyploids are more divergent.

Fig. 1
Box plots of the distribution of genetic divergence index (GDI) of parental pairs for homoploid and polyploid hybrids. The two groups have an asymmetric dispersion range, with the parents of allopolyploids being more divergent than those producing diploid ...
Table 2
Nonparametric comparisons of parental divergence indices for homoploid versus polyploid hybrid species using the Mann-Whitney test as calculated in SPSS. The indices are calculated using either the uncorrected-p (P) or Kimura’s (1980) two-parameter ...

A histogram (Fig. 2a) illustrating frequency distributions of classes of parental GDI for homoploid hybrid species and allopolyploids indicates that both categories have unimodal but distinct distributions. The relationships between frequency of occurrence and degree of chromosomal divergence of parental pairs for allopolyploids and homoploid hybrids (Fig. 2b) meet at a GDI ≈ 0.75, indicating an equal probability of a hybrid formation with and without a change in ploidy when Pd is ca. three quarters of Av.

Fig. 2
(a). Histogram illustrating the different frequency distribution of parental GDI classes for homoploid hybrid species (grey bars) and allopolyploids (open bars). Values on the x-axis show the limits of the GDI classes, with a 0.25 increment. (b). Hypothetical ...

The non-parametric, one-tailed Spearman rank order correlation of Av with the number of taxa included in each phylogenetic analysis was not significant (Spearman’s rho = 0.069, P = 0.322).


By comparing frequency distributions of parental genetic distance (used here as a surrogate for chromosomal differentiation) for homoploid and allopolyploid hybrid species, we demonstrate the relevance of progenitor divergence as a determinant of ploidy in resulting hybrid species: although the range of genetic divergence between the parents of homoploid hybrids is similar to those of allopolyploids, the actual values of divergence are significantly higher in the latter (Fig. 1).

Our standardized approach, integrating each parental pair within its generic context, has several advantages: (i) it makes our method independent of assumptions implied by specific genetic distances or defining clades (cf. Buggs et al., 2008), and (ii) it allows us to include molecular markers and more cases (cf. Chapman & Burke, 2007) and gives our analysis greater predictive power. The last derives from our suggestion that species pairs with a divergence smaller than three quarters of the average divergence between species within the genus (i.e., GDI ≤ 0.75) have chromosomes mostly displaying colinearity of genes. Most homoploid hybrids (75%) included here were formed between such parental pairs, but this category included just 12.5% of allopolyploids (Fig. 2a). Furthermore, if a parental pair has a divergence greater than three quarters of the average in a given genus, most of their corresponding chromosomes are likely to be sufficiently heterologous to act as homeologs, and hybridization is most likely to result in an increase in ploidy.

Two cases (in Paeonia and Stephanomeria; see Table 1) identified in the literature for which the same parental pair has successfully produced both homoploid and allopolyploid hybrid species substantiate our results. Their calculated divergence index (Table 1) is indeed close to the estimated value for which there should be an equal probability of hybrid formation with and without ploidy change (i.e., GDI ≈ 0.75, Fig. 2b). Our results parallel those of Chapman and Burke (2007): their analysis indicated that parents of allopolyploids are on average more than twice as divergent as parents of homoploid hybrids, a significant relationship that is also visible in GDI (Fig. 1).

Assumptions, limitations and alternatives

The general premise that genetic divergence provides the best available surrogate for differentiation of chromosome sets is often employed (e.g., Edmands, 2002). As early as 1937, Darlington (p. 197) hypothesized “a correlation between genetic differentiation of the chromosomes of the species and their structural differentiation”. Indeed, both genetic distance and magnitude of difference in genomic rearrangements between two species are expected to be proportional to the evolutionary time since common ancestry.

Calculating an average genetic distance within each genus adds a subjective component to our analyses. We cannot eliminate taxonomic inconsistencies created by differences in taxonomic practice among authors working on different taxa. We also start from the assumption that the modern taxa studied here are closely related to the actual progenitors of the hybrid species and that after hybridization genetic divergence between these species has remained largely unchanged. More appropriately, these taxa should be considered as closest living descendants of the donor species. However, most of the cases included here, both homoploid and polyploid hybrids, are likely to be relatively recent, as with time such cases become increasingly difficult to detect (Chase et al., 2003; Clarkson et al., 2004).

Underlying processes: allopolyploids

A theoretical model for polyploid speciation along a continuous variation of genomic divergence between diploid progenitors was developed by Sang and collaborators (2004). They treated the origin of a successful polyploid lineage as a function of (1) polyploid formation (production of polyploid individuals from diploid populations), further broken up into probability of unreduced gamete production and frequency of hybridization, and (2) successful establishment of polyploid populations. Such a model would imply that frequency of polyploid formation would have a negative exponential distribution on parental genomic divergence. The overall probability of successful polyploid speciation, however, would have a unimodal distribution on parental divergence (Sang et al., 2004), with established autopolyploids being much less frequent than allopolyploids, despite the fact that autopolyploids occur spontaneously in nature at relatively high rates (see Ramsey & Schemske, 1998).

The main route to allopolyploid speciation is represented by the fusion of an unreduced gamete with a haploid gamete resulting in a “triploid bridge” (Ramsey & Schemske, 1998; Husband, 2000), and after self-fertilization or backcrossing to diploids a new allotetraploid may originate. Alternatively, allopolyploid speciation can also result after fusion of two unreduced gametes, with better chances in dense hybrid zones, marginal or disturbed habitats and/or other limiting conditions (e.g., temperature variation; Thompson & Lumaret, 1992; Ramsey & Schemske, 1998). Such unreduced gametes are thought to be rare (Mallet, 2007) and will be unsuccessful and lost, especially if enough haploid gametes are produced. However, poor chromosome pairing in unbalanced diploid F1 hybrids leads to asynapsis at the first meiotic division, and such organisms form unreduced gametes with much greater frequency. Ramsey and Schemske (1998) reported that unreduced gametes are produced at rates ca. 50 times higher in hybrids than in non-hybrid lineages. As predicted by Grant (1981, see Introduction), it seems plausible that greater levels of parental divergence increase meiotic abnormalities at the homoploid level and, thus, the rate of non-reduction. For example, in Lilium, most gametes produced by intersectional hybrids are unreduced (van Tuyl et al., 1989). The same trend is expected in the case of allopolyploidy resulting from somatic chromosome doubling in meristematic tissues of a diploid hybrid or in a zygote/young embryo (e.g., Primula kewensis, Ramsey & Schemske, 1998). Such somatic doubling may be directly triggered by structural differences between parental homeologs (Winge, 1917, see introduction).

On the other hand, both somatic chromosome doubling and unreduced gametes require spontaneous occurrence of diploid hybrids that are at least partly fertile and self-compatible (Sang et al., 2004), thus limiting the possible maximal extent of parental divergence. Such a bounded distribution of parental divergence, between lower chances of gamete non-reduction or somatic doubling at minimal parental divergence and full diploid hybrid sterility at increased divergence, may result in apparently random occurrence of allopolyploidization events as suggested by Buggs et al. (2008). In addition, rare allopolyploid formation events via unreduced gametes produced directly in non-hybrid parents will not follow the rules presented above and may blur the trends concerning formation of allopolyploid individuals.

Independent of formation, a nascent allopolyploid must become established and expand its population/s in order to produce a new species. Establishment of the polyploid lineage will depend not only on stochastic events, such as the availability of appropriate environments, but also on its degree of viability, fertility, heterozygosity (hybrid vigour) and fitness. Darlington (1937, p. 196) hypothesized “a negative correlation between the fertility of diploids and that of the tetraploids to which they give rise. […] The greater the dissimilarities in the diploid, the more regularly do the identical chromosomes pair in the allotetraploid derived from it, and therefore the less frequent are the multivalents in the tetraploid”. A diploid hybrid with reduced chromosome-pairing will exhibit a high degree of sterility, which doubling overcomes. Fertility might increase with parental divergence, due to fewer meiotic abnormalities. Ramsey & Schemske (2002) provided evidence that the degree of allopolyploid fertility is positively correlated with frequency of bivalents, but not with other configurations. They also concluded that allopolyploids generated by semisterile diploid hybrids are generally much more fertile than their progenitors, an attribute partly reflecting genic incompatibilities independent of and in addition to meiotic behaviour. A significant increase in effective population size seems to be the consequence of selection on fertility acting on neopolyploids, which rapidly increases pollen viability and seed set. The picture here is more complex than at homoploid level, and it is still unclear how parental incompatibilities will behave at the polyploid level when they result in sterility/reduced fitness or break down. This is also due to a lack of study; allopolyploids do not facilitate gene flow between diverging parental taxa, and, hence, they are not considered in current research and debates regarding reproductive isolation and genetics of speciation (see for example Widmer et al., in press).

It is expected that heterozygosity (resulting in heterosis) generally provides increased fitness and adaptive potential, through enhancing the potential for spatial, temporal and functional variation in gene expression (Flagel & al., 2008). The proportion of homeologous loci that are stably heterozygous should be positively correlated with genomic divergence between progenitors. In addition, alterations of gene expression in allopolyploid genomes have the potential to trigger fitness differences in the parental environment, which will be available to selection. A few case studies have indicated that the extent of genomic alterations and changes in gene expression may depend on the degree of divergence between the parental diploid genomes. For example, Song et al. (1995) observed fewer rearrangements in the allopolyploid genome formed from closely related Brassica rapa and B. oleracea, but many more in the allopolyploid combining more divergent B. rapa and B. nigra. Another such example is Nicotiana where allopolyploids N. arentsii and N. rustica show only minimal genetic changes, but N. tabacum (resulted from widely divergent N. sylvestris and N. tomentosiformis) exhibits intergenomic translocations (Lim et al., 2004). Rapid genomic repatterning will also increase genetic variability available to new polyploid populations. Additionally, extensive changes in gene expression seem to be triggered by wide hybridization rather than polyploidy (Paun et al., 2007); recent studies show that genome duplication can, in fact, have widespread ameliorating effects on altered levels of gene expression arising from hybridization (as, e.g., in Senecio, Hegarty et al., 2006). In allopolyploid cotton, however, a significant proportion of expression novelty is likely triggered by polyploidy after long-term evolutionary processes on duplicated genes (Flagel et al., 2008). Finally, shifts in breeding system, like breakdown of self-incompatibility, seem to be initiated by polyploidization alone, whereas others, like apomixis, usually seem to be triggered by the effects of combining hybridization and polyploidy (see, e.g., Paun et al., 2006). In conclusion, the frequency distribution of allopolyploids along the continuum of ancestral genomic divergence (Fig. 2b) will have an optimum between low fertility, heterozygosity and fitness at minimal parental divergence (as compared to diploid progenitors and homoploid hybrids) and low probability of polyploid formation towards maximal divergence of progenitors (due to increased pre- and postzygotic barriers).

Auto- and allopolyploids

Buggs et al. (2008) argued that the low frequency of allopolyploids in lower parental divergence classes in the study of Chapman & Burke (2007) was due to exclusion of autopolyploids from analysis of the latter. Likewise, our study does not include any autopolyploids, but we definitely expect that parental divergence in this case should not span such a high interval (at least until GDI = 1, i.e. Pd = Av) to make the polyploid distribution fit a negative linear/exponential function (Fig. 2). The overall polyploid distribution would instead be bimodal, indicating the presence of different phenomena influencing the frequency of the two types of polyploids (see also Sang et al., 2004). We hypothesize that the adaptive valley between autopolyploid and allopolyploid frequency may have resulted from more or less equal combinations of bivalents and quadrivalents in meiosis. However, we regard inclusion of autopolyploids in analyses considering hybrid speciation as inappropriate because autopolyploid formation should correspond, at the diploid level, to frequent events of intraspecific processes, and these do not necessarily have a significant contribution to speciation.

Underlying processes: homoploid hybrids

The formation of homoploid hybrid individuals is partly shaped by stochastic events (e.g., shifts in distribution ranges) but is directly limited by the strength and nature of reproductive isolation between species pairs. Plant species are typically isolated by many pre- and postzygotic barriers and their complex interactions (Coyne & Orr, 2004). Recent studies have suggested that prezygotic isolation is usually much stronger than postzygotic isolation (Lowry et al., 2008; Widmer et al., in press; but see e.g., Cozzolino et al., 2004), due to factors such as distribution, immigrant inviability, phenological differences, pollinator specificity, mating system and pollen competition. Significant trends obvious in hybrid formation without a change in ploidy (see e.g., Buggs et al., 2008) represent, to a great degree, the entire speciation process in homoploid hybrids (this study). Studying hybrid formation, Buggs and colleagues (2008) reached the conclusion that parents of homoploid hybrids are less divergent than would be expected with random crossing. We found a similar, but more significant pattern: the probability of production of a diploid hybrid is highest if the parental divergence is less than or equal to (more or less) half the average in the genus and decreases as reproductive barriers (both pre- and postzygotic) become stronger between diploid parents with increased genomic divergence. With greater parental divergence, genic and/or chromosomal incompatibility will occur with greater probability. Examples of characterized genic incompatibilities include: genes involved in hybrid necrosis or weakness (Bomblies & Weigel, 2007) and cytonuclear incompatibility (Chase, 2007). Models have suggested that the level of incompatibility between species should increase with evolutionary time at least as rapidly as the square of the divergence time between the two species (snowballing effect; Orr, 1995). Therefore, the degree of fertility of a diploid hybrid decreases rapidly with increased genomic divergence. Classical models of chromosomal speciation have stated that after a particular level, meiotic mismatches of parental chromosomes or karyotypes will cause hybrid sterility and significant reduction in fitness (White, 1978; but see Lowry et al., 2008). In addition, chromosomal divergence may also increase the strength of genic incompatibilities by suppressing recombination and therefore maintaining the effects of linked isolation genes (Rieseberg, 2001).

The diploid form of hybrid speciation occurs mainly in sympatry or parapatry, and hence the greatest challenge of the nascent taxon is to achieve reproductive isolation. Isolation from progenitors often occurs as a by-poduct of the process that stabilizes the hybrid lineage and may be based on ecological factors (e.g., habitat divergence, Gross & Rieseberg, 2005), sorting pre-existing sterility factors and/or chromosomal rearrangements (Grant, 1981). All these pathways are potentially influenced by the extent of parental differentiation. Ecological divergence may be acquired by positive heterosis (hybrid vigour, Lippman & Zamir, 2007) and transgressive segregation (Gross & Rieseberg, 2005). Numerous experimental crosses have suggested that the optimal degree of genetic divergence for maximal expression of positive heterosis occurs within a range of divergence that is narrow enough for cytological irregularities not to be apparent (e.g., Moll et al., 1965; Cox & Murphy, 1990). Reproductive isolation can also be achieved by sorting pre-existing chromosomal rearrangements that differentiate the parental species, resulting in the formation of a novel recombinant genotype that is homozygous for these rearrangements (“recombinational” speciation, Grant 1981, p. 250). Stronger genetic isolation from progenitors is most likely when a barrier differentiating the parents is genetically and/or chromosomally extensive and complex (Rieseberg, 2000) However, the parental species must have genomes similar enough for pairing and recombination to occur.

There are at least two important implications of our results. First, there may be a fitness and fertility valley between homoploid hybrids and allopolyploids with increasing genomic divergence of progenitors (see also Darlington, 1937). A second adaptive valley may be represented by intermediates between typical auto- and allopolyploids, which will suffer the effects of mixed multivalent and bivalent formation in meiosis. Greater support for these hypotheses requires further experimental study.

Supplementary Material


Table S1. Details on the data included in the analyses and results for each individual hybrid case.


We thank D. Albach, R. Bateman, E. Conti, A. Davis, Y. Guo, G. Mansion, A. Mast, E.E. Schilling and R.E. Timme for providing aligned DNA sequence matrices; M. Winkler for her comments on appropriate statistical analysis; I. Leitch and A. Leitch for insightful discussions; and J. Wendel and one anonymous reviewer for useful criticisms. This research was funded by an Erwin Schrödinger fellowship (Austrian Science Fund, FWF; project J26406-B03) and an Intra-European Marie Curie fellowship (DactGene, MEIF-CT-2007-040494) to O.P.


  • Allan GJ, Clark C, Rieseberg LH. Distribution of parental DNA markers in Encelia virginensis (Asteraceae: Heliantheae), a diploid species of putative hybrid origin. Plant Systematics and Evolution. 1997;205:205–221.
  • Allen GA. Hybrid speciation in Erythronium (Liliaceae): a new allotetraploid species from Washington State. Systematic Botany. 2001;26:263–272.
  • Allen GA, Soltis DE, Soltis PS. Phylogeny and biogeography of Erythronium (Liliaceae) inferred from chloroplast matK and nuclear rDNA ITS sequences. Systematic Botany. 2003;28:512–523.
  • Andersson E. Introgressive Hybridization. Wiley; New York, USA: 1949.
  • Arnold M. Natural Hybridization and Evolution. Oxford University Press; Oxford, U.K.: 1997.
  • Barton NH. The role of hybridization in evolution. Molecular Ecology. 2001;10:551–568. [PubMed]
  • Bomblies K, Weigel D. Hybrid necrosis: autoimmunity as a common barrier to gene flow in plants. Nature Review in Genetics. 2007;8:382–393. [PubMed]
  • Bottini MCJ, De Bustos A, Sanso AM, Jouve N, Poggior L. Relationships in Patagonian species of Berberis (Berberidaceae) based on the characterization of rDNA internal transcribed spacer sequences. Botanical Journal of the Linnean Society. 2007;153:321–328.
  • Brochmann C, Borgen L, Stabbetorp OE. Multiple diploid hybrid speciation of the Canary Island endemic Argyranthemum sundingii (Asteraceae) Plant Systematics and Evolution. 2000;220:77–92.
  • Buerkle CA, Rieseberg LH. The rate of genome stabilization in homoploid hybrid species. Evolution. 2008;62:266–275. [PMC free article] [PubMed]
  • Buggs RJA, Soltis PS, Mavrodiev EV, Symonds VV, Soltis DE. Does phylogenetic distance between parental genomes govern the success of polyploids? Castanea. 2008;73:74–93.
  • Chapman MA, Burke JM. Genetic divergence and hybrid speciation. Evolution. 2007;61:1773–1780. [PubMed]
  • Chase CD. Cytoplasmic male sterility: a window to the world of plant mitochondrial–nuclear interactions. Trends in Genetics. 2007;23:81–90. [PubMed]
  • Chase MW, Knapp S, Cox AV, Clarkson JJ, Butsko Y, Joseph J, Savolainen V, Parokonny AS. Molecular systematics, GISH and the origin of hybrid taxa in Nicotiana (Solanaceae) Annals of Botany. 2003;92:107–127. [PMC free article] [PubMed]
  • Chat J, Jáuregui B, Petit RJ, Nadot S. Reticulate evolution in kiwifruit (Actinidia, Actinidiaceae) identified by comparing their maternal and paternal phylogenies. American Journal of Botany. 2004;91:736–747. [PubMed]
  • Chen ZJ. Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annual Review in Plant Biology. 2007;58:377–406. [PMC free article] [PubMed]
  • Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Research. 2003;31:3497–3500. [PMC free article] [PubMed]
  • Clarkson JJ, Knapp S, Garcia VF, Olmstead RG, Leitch AR, Chase MW. Phylogenetic relationships in Nicotiana (Solanaceae) inferred from multiple plastid DNA regions. Molecular Phylogenetics and Evolution. 2004;33:75–90. [PubMed]
  • Clarkson JJ, Lim KY, Kovarik A, Chase MW, Knapp S, Leitch AR. Long-term genome diploidization in allopolyploid Nicotiana section Repandae (Solanaceae) New Phytologist. 2005;168:241–252. [PubMed]
  • Clausen J, Keck DD, Hiesey WM. Experimental studies on the nature of species. II Plant evolution through amphiploidy and autopolyploidy, with examples from the Madiinae. Carnegie Institution of Washington Publications: 1945;564:1–174.
  • Comai L. The advantages and disadvantages of being polyploid. Nature Review in Genetics. 2005;6:836–846. [PubMed]
  • Cozzolino S, D’Emerico S, Widmer A. Evidence for reproductive isolate selection in Mediterranean orchids: karyotype differences compensate for the lack of pollinator specificity. Proceedings of the Royal Society of London B. 2004;271:S259–S262. [PMC free article] [PubMed]
  • Cox TS, Murphy JP. The effect of parental divergence on F2 heterosis in winter wheat crosses. Theoretical Applied Genetics. 1990;79:241–250. [PubMed]
  • Coyne JA, Orr HA. Speciation. Sinauer Associates; Sunderland, Massachusetts: 2004. Polyploidy and hybrid speciation; pp. 321–351.
  • Cronn RC, Wendel JF. Cryptic trysts, genomic mergers and plant speciation. New Phytologist. 2004;161:133–142.
  • Cui L, Wall PK, Leebens-Mack JH, Lindsay BG, Soltis DE, Doyle JJ, Soltis PS, Carlson JE, Arumuganathan K, Barakat A, Albert VA, Ma H, dePamphilis CW. Widespread genome duplications throughout the history of flowering plants. Genome Research. 2006;16:738–749. [PubMed]
  • Darlington CD. Recent Advances in Cytology. Ed. 2 Blakiston; Philadelphia: 1937.
  • De Bodt S, Maere S, van de Peer Y. Genome duplication and the origin of angiosperms. Trends in Ecology and Evolution. 2005;20:591–597. [PubMed]
  • Edmands S. Does parental divergence predict reproductive compatibility? Trends in Ecology and Evolution. 2002;17:520–527.
  • Ellstrand NC, Whitkus R, Rieseberg LH. Distribution of spontaneous plant hybrids. Proceedings of the National Academy of Sciences, USA. 1996;93:5090–5093. [PubMed]
  • Fehlberg SD, Ranker TA. Phylogeny and biogeography of Encelia (Asteraceae) in the Sonoran and Peninsular deserts based on multiple DNA sequences. Systematic Botany. 2007;32:692–699.
  • Fjellheim S, Jørgensen MH, Kjos M, Borgen L. A molecular study of hybridization and homoploid hybrid speciation in Argyranthemum (Asteraceae) on Tenerife, the Canary Islands. Botanical Journal of the Linnean Society. In press.
  • Ford VS, Gottlieb LD. Single mutations silence PgiC2 genes in two very recent allotetraploid species of Clarkia. Evolution. 2002;56:699–707. [PubMed]
  • Ge S, Sang T, Lu B-R, Hong D-Y. Phylogeny of rice genomes with emphasis on origins of allotetraploid species. Proceedings of the National Academy of Sciences USA. 1999;96:14400–14405. [PubMed]
  • Grant V. Plant Speciation. Ed. 2 Columbia University Press; New York: 1981.
  • Gross BL, Rieseberg LH. The ecological genetics of homoploid hybrid speciation. Journal of Heredity. 2005;96:241–252. [PMC free article] [PubMed]
  • Guggisberg A, Bretagnolle F, Mansion G. Allopolyploid origin of the Mediterranean endemic, Centaurium bianoris (Gentianaceae), inferred by molecular markers. Systematic Botany. 2006;31:368–379.
  • Guo Y-P, Ehrendorfer F, Samuel R. Phylogeny and systematics of Achillea (Asteraceae-Anthemideae) inferred from nrITS and plastid trnL-F DNA sequences. Taxon. 2004;53:657–672.
  • Guo Y-P, Saukel J, Mittermayr R, Ehrendorfer F. AFLP analyses demonstrate genetic divergence, hybridization, and multiple polyploidization in the evolution of Achillea (Asteraceae-Anthemideae) New Phytologist. 2005;166:273–290. [PubMed]
  • Guo Y-P, Vogl C, van Loo M, Ehrendorfer F. Hybrid origin and differentiation of two tetraploid Achillea species in East Asia: molecular, morphological and ecogeographical evidence. Molecular Ecology. 2006;15:133–144. [PubMed]
  • Hedrén M. Systematics of the Dactylorhiza euxina/incarnata/maculata polyploidy complex (Orchidaceae) in Turkey: evidence from allozyme data. Plant Systematics and Evolution. 2001;229:23–44.
  • Hegarty MJ, Barker GL, Wilson ID, Abbott RJ, Edwards KJ, Hiscock SJ. Transcriptome shock after interspecific hybridization in Senecio is ameliorated by genome duplication. Current Biology. 2006;16:1652–1659. [PubMed]
  • Howarth DG, Baum DA. Genealogical evidence of homoploid hybrid speciation in an adaptive radiation of Scaevola (Goodeniaceae) in the Hawaiian islands. Evolution. 2005;59:948–961. [PubMed]
  • Howarth DG, Gustafsson MFG, Baum DA, Motley TJ. Phylogenetics of the genus Scaevola (Goodeniaceae): implications for dispersal patterns across the pacific basin and colonization of the Hawaiian islands. American Journal of Botany. 2003;90:915–923. [PubMed]
  • Hughes CE, Govindarajulu R, Robertson A, Filer DL, Harris SA, Bailey CD. Serendipitous backyard hybridization and the origin of crops. Proceedings of the National Academy of Sciences USA. 2007;104:14389–14394. [PubMed]
  • Husband BC. Constraints on polyploid evolution: a test of the minority cytotype exclusion principle. Proceedings of the Royal Society of London B. 2000;267:217–223. [PMC free article] [PubMed]
  • Jung E, Tate PL, Horn R, Kochert G, Moore K, Abbott AG. The phylogenetic relationship of possible progenitors of the cultivated peanut. Journal of Heredity. 2003;94:334–340. [PubMed]
  • Kim Y-D, Kim S-H, Landrum LR. Taxonomic and phytogeographic implications from ITS phylogeny in Berberis (Berberidaceae) Journal of Plant Research. 2004;117:175–182. [PubMed]
  • Kimura M. A simple method for estimating evolutionary rate of base substitution through comparative studies of nucleotide sequences. Journal of Molecular Evolution. 1980;16:111–120. [PubMed]
  • Koch M, Al-Shehbaz I-A. Molecular data indicate complex intra- and intercontinental differentiation of American Draba (Brassicaceae) Annals of the Missouri Botanical Garden. 2002;89:88–109.
  • Kuzoff RK, Soltis DE, Hufford L, Soltis PS. Phylogenetic relationships within Lithophragma (Saxifragaceae): hybridization, allopolyploidy, and ovary diversification. Systematic Botany. 1999;24:598–615.
  • Lee J, Baldwin BG, Gottlieb LD. Phylogeny of Stephanomeria and related genera (Compositae–Lactuceae) based on analysis of 18S-26S nuclear rDNA ITS and ETS sequences. American Journal of Botany. 2002;89:160–168. [PubMed]
  • Levin RA, Wagner WL, Hoch PC, Hahn WJ, Rodriguez A, Baum DA, Katinas L, Zimmer EA, Sytsma KJ. Paraphyly in tribe Onagreae: insights into phylogenetic relationships of Onagraceae based on nuclear and chloroplast sequence data. Systematic Botany. 2004;29:147–164.
  • Li J, Huang H, Sang T. Molecular phylogeny and infrageneric classification of Actinidia (Actinidiaceae) Systematic Botany. 2002;27:408–415.
  • Lim KY, Matyasek R, Kovarik A, Leitch AR. Genome evolution in allotetraploid Nicotiana. Biological Journal of the Linnean Society. 2004;82:599–606.
  • Lippman ZB, Zamir D. Heterosis: revisiting the magic. Trends in Genetics. 2007;23:60–66. [PubMed]
  • Liu Q, Brubaker CL, Green AG, Marshall DR, Sharp PJ, Singh SP. Evolution of the FAD2-1 fatty acid desaturase 5′ UTR intron and the molecular systematics of Gossypium (Malvaceae) American Journal of Botany. 2001;88:92–102. [PubMed]
  • Lowry DB, Modliszewski JL, Wright KM, Wu CA, Willis JH. The strength and genetic basis of reproductive isolating barriers in flowering plants. Philosophical Transactions of the Royal Society of London B. 2008;363:3009–3021. [PMC free article] [PubMed]
  • Maki M, Murata J. Allozyme analysis of the hybrid origin of Arisaema ehimense (Araceae) Heredity. 2001;86:87–93. [PubMed]
  • Mallet J. Hybridization as an invasion of the genome. Trends in Ecology and Evolution. 2005;20:229–237. [PubMed]
  • Mallet J. Hybrid speciation. Nature. 2007;446:279–283. [PubMed]
  • Mansion G, Zeltner L, Bretagnolle F. Phylogenetic patterns and polyploid evolution within the Mediterranean genus Centaurium (Gentianaceae - Chironieae) Taxon. 2005;54:931–950.
  • Maurin O, Davis AP, Chester M, Mvungi EF, Jaufeerally-Fakim Y, Fay MF. Towards a phylogeny for Coffea (Rubiaceae): identifying well-supported lineages based on nuclear and plastid DNA sequences. Annals of Botany. 2007;100:1565–1583. [PMC free article] [PubMed]
  • Mavrodiev EV, Tancig M, Sherwood AM, Gitzendanner MA, Rocca J, Soltis PS, Soltis DE. Phylogeny of Tragopogon L. (Asteraceae) based on internal and external transcribed spacer sequence data. International Journal of Plant Sciences. 2005;166:117–133.
  • Meyers LA, Levin DA. On the abundance of polyploidy in flowering plants. Evolution. 2006;60:1198–11206. [PubMed]
  • Moll RH, Lonnquist JH, Fortuno J Wlez, Johnson EC. The relationship of heterosis and genetic divergence in maize. Genetics. 1965;52:139–144. [PubMed]
  • Orr HA. The population genetics of speciation: the evolution of hybrid incompatibilities. Genetics. 1995;139:1805–1813. [PubMed]
  • Otto SP. The evolutionary consequences of polyploidy. Cell. 2007;131:452–462. [PubMed]
  • Otto SP, Whitton J. Polyploid incidence and evolution. Annual Review in Genetics. 2000;34:401–437. [PubMed]
  • Pan J, Zhang D, Sang T. Molecular phylogenetic evidence for the origin of a diploid hybrid of Paeonia (Paeoniaceae) American Journal of Botany. 2007;94:400–408. [PubMed]
  • Paun O, Fay MF, Soltis DE, Chase MW. Genetic and epigenetic alterations after hybridization and genome doubling. Taxon. 2007;56:649–656. [PMC free article] [PubMed]
  • Paun O, Stuessy TF, Hörandl E. The role of hybridization, polyploidization and glaciation in the origin and evolution of the apomictic Ranunculus cassubicus complex. New Phytologist. 2006;171:223–236. [PubMed]
  • Pillon Y, Fay MF, Shipunov AB, Chase MW. Species diversity versus phylogenetic diversity: a practical study in the taxonomically difficult genus Dactylorhiza (Orchidaceae) Biological Conservation. 2006;129:4–13.
  • Pillon Y, Fay MF, Hedrén M, Bateman RM, Devey DS, Shipunov AB, van der Bank M, Chase MW. Evolution and temporal diversification of western European polyploid species complexes in Dactylorhiza (Orchidaceae) Taxon. 2007;56:1185–1208.
  • Ramsey J, Schemske DW. Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annual Review of Ecology and Systematics. 1998;29:467–501.
  • Ramsey J, Schemske DW. Neopolyploidy in flowering plants. Annual Review of Ecology and Systematics. 2002;33:589–639.
  • Renner SS, Zhang L-B, Murata J. A chloroplast phylogeny of Arisaema (Araceae) illustrates tertiary floristic links between Asia, North America, and East Africa. American Journal of Botany. 2004;91:881–888. [PubMed]
  • Rieseberg LH. Hybrid origins of plant species. Annual Review of Ecology and Systematics. 1997;28:359–389.
  • Rieseberg LH. Crossing relationships among ancient and experimental sunflower hybrid lineages. Evolution. 2000;54:859–865. [PubMed]
  • Rieseberg LH. Chromosomal rearrangements and speciation. Trends in Ecology and Evolution. 2001;16:351–358. [PubMed]
  • Rieseberg LH, Raymond O, Rosenthal DM, Lai Z, Livingstone K, Nakazato T, Durphy JL, Schwarzbach AE, Donovan LA, Lexer C. Major ecological transitions in wild sunflowers facilitated by hybridization. Science. 2003;301:1211–1216. [PubMed]
  • Rieseberg LH, Sinervo B, Linder CR, Ungerer M, Arias DM. Role of gene interactions in hybrid speciation: evidence from ancient and experimental hybrids. Science. 1996;272:741–745. [PubMed]
  • Sang T, Crawford DJ, Stuessy TF. Chloroplast DNA phylogeny, reticulate evolution, and biogeography of Paeonia (Paeoniaceae) American Journal of Botany. 1997;84:1120–1136. [PubMed]
  • Sang T, Pan J, Zhang D, Ferguson D, Wang C, Paun K-Y, Hong D-Y. Origins of polyploids: an example from peonies (Paeonia) and a model for angiosperms. Biological Journal of the Linnean Society. 2004;82:561–571.
  • Schilling EE, Linder CR, Noyes RD, Rieseberg LH. Phylogenetic relationships in Helianthus (Asteraceae) based on nuclear ribosomal DNA internal transcribed spacer region sequence data. Systematic Botany. 1998;23:177–187.
  • Seehausen O. Hybridization and adaptive radiation. Trends in Ecology aqnd Evolution. 2004;19:198–207. [PubMed]
  • Seelanan T, Schnabel A, Wendel JF. Congruence and consensus in the cotton tribe (Malvaceae) Systematic Botany. 1997;22:259–290.
  • Seelanan T, Brubaker CL, Stewart J, Craven LA, Wendel JF. Molecular systematics of Australian Gossypium section Grandicalyx (Malvaceae) Systematic Botany. 1999;24:183–208.
  • Senchina DS, Alvarez I, Cronn RC, Liu B, Rong J, Noyes RD, Paterson AH, Wing RA, Wilkins TA, Wendel JF. Rate variation among nuclear genes and the age of polyploidy in Gossypium. Molecular Biology and Evolution. 2003;20:633–643. [PubMed]
  • Soltis DE, Soltis PS, Schemske DW, Hancock JF, Thompson JN, Husband BC, Judd WS. Autopolyploidy in angiosperms: have we grossly underestimated the number of species? Taxon. 2007;56:13–30.
  • Song K, Lu P, Tang K, Osborn CT. Rapid genome change in synthetic polyploids of Brassica and its implications for polyploid evolution. Proceedings of the National Academy of Sciences USA. 1995;92:7719–7723. [PubMed]
  • Stebbins GL. Variation and Evolution in Plants. Columbia University Press; New York and London: 1950.
  • Sun K, Chen X, Ma R, Li C, Wang Q, Ge S. Molecular phylogenetics of Hippophae L. (Elaeagnaceae) based on the internal transcribed spacer (ITS) sequences of nrDNA. Plant Systematics and Evolution. 2002;235:121–134.
  • Swofford DL. PAUP*: Phylogenetic Analysis Using Parsimony (* and other methods) Version 4.0b10 Sinauer Associates; Sunderland, Massachusetts: 2003.
  • Thompson JD, Lumaret R. The evolutionary dynamics of polyploid plants: origins, establishment and persistence. Trends in Ecology and Evolution. 1992;7:302–307. [PubMed]
  • Timme RE, Simpson BB, Linder CR. High-resolution phylogeny for Helianthus (Asteraceae) using the 18S-26S ribosomal DNA external transcribed spacer. American Journal of Botany. 2007;94:1837–1852. [PubMed]
  • Ungerer MC, Baird SJE, Pan J, Rieseberg LH. Rapid hybrid speciation in wild sunflowers. Proceedings of the National Academy of Sciences USA. 1998;95:11757–11762. [PubMed]
  • van Tuyl JM, De Vries JN, Bino RJ, Kwakkenbos TAM. Identification of 2n-pollen producing interspecific hybrids of Lilium using flow-cytometry. Cytologia. 1989;54:737–745.
  • Vander Stappen J, Lopez S Gama, Davila P, Volckaert G. Molecular evidence for the hybrid origin of a new endemic species of Stylosanthes Sw. (Fabaceae) from the Mexican Yucatán Peninsula. Botanical Journal of the Linnean Society. 2002;140:1–13.
  • Wang A, Schluetz F, Liu J. Molecular evidence for double maternal origins of the diploid hybrid Hippophae goniocarpa (Elaeagnaceae) Botanical Journal of the Linnean Society. 2008;156:111–118.
  • Weiss-Schneeweiss H, Schneeweiss GM, Stuessy TF, Mabuchi T, Park J-M, Jang C-G, Sun B-Y. Chromosomal stasis in diploids contrasts with genome restructuring in auto- and allopolyploid taxa of Hepatica (Ranunculaceae) New Phytologist. 2007;174:669–682. [PubMed]
  • Wendel JF, Cronn RC. Polyploidy and the evolutionary history of cotton. Advances in Agronomy. 2003;78:139–186.
  • White MJD. Modes of Speciation. W.H. Freeman & Co.; San Francisco, CA: 1978.
  • Widmer A, Baltisberger M. Molecular evidence for allopolyploid speciation and a single origin of the narrow endemic Draba ladina (Brassicaceae) American Journal of Botany. 1999;86:1282–1289. [PubMed]
  • Widmer A, Lexer C, Cozzolino S. Evolution of reproductive isolation in plants. Heredity. In press. doi: 10.1038/hdy.2008.69. [PubMed]
  • Winge Ø . The chromosomes. Their numbers and general importance. Comptesrendus des travaux de la laboratoire Carlsberg. 1917;13:131–275.
  • Wolfe A, Randle CP. Relationships within and among species of the holoparasitic genus Hyobanche (Orobanchaceae) inferred from ISSR banding patterns and nucleotide sequences. Systematic Botany. 2001;26:120–130.
  • Wolfe AD, Randle CP, Datwyler SL, Morawetz JL, Arguedas N, Diaz J. Phylogeny, taxonomic affinities, and biogeography of Penstemon (Plantaginaceae) based on ITS and cpDNA sequence data. American Journal of Botany. 2006;93:1699–1713. [PubMed]
  • Wolfe AD, Xiang Q-Y, Kephart SK. Diploid hybrid speciation in Penstemon (Scrophulariaceae) Proceedings of the National Academy of Sciences USA. 1998;95:5112–5115. [PubMed]
  • Wood TE, Rieseberg LH. The Frequency of Polyploid Speciation in Land Plants: A Phylogenetic Approach. Abstract 476. Botany 2005: Learning From Plants; Scientific meeting; Austin, Texas. August 13 - 17, 2005.2005.
  • Wu C-I. The genic view of the process of speciation. Journal of Evolutionary Biology. 2001;14:851–865.