Research Article

Major Ecological Transitions in Wild Sunflowers Facilitated by Hybridization

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Science  29 Aug 2003:
Vol. 301, Issue 5637, pp. 1211-1216
DOI: 10.1126/science.1086949


Hybridization is frequent in many organismal groups, but its role in adaptation is poorly understood. In sunflowers, species found in the most extreme habitats are ancient hybrids, and new gene combinations generated by hybridization are speculated to have contributed to ecological divergence. This possibility was tested through phenotypic and genomic comparisons of ancient and synthetic hybrids. Most trait differences in ancient hybrids could be recreated by complementary gene action in synthetic hybrids and were favored by selection. The same combinations of parental chromosomal segments required to generate extreme phenotypes in synthetic hybrids also occurred in ancient hybrids. Thus, hybridization facilitated ecological divergence in sunflowers.

The role of hybridization in evolution has been debated for more than a century. Two highly polarized viewpoints have emerged. At one extreme, hybridization is considered to be a potent evolutionary force that creates opportunities for adaptive evolution and speciation (1, 2). In this view, the increased genetic variation and new gene combinations resulting from hybridization promote the development and acquisition of novel adaptations. The contrasting position accords little evolutionary importance to hybridization (aside from allopolyploidy), viewing it as a primarily local phenomenon with only transient effects—a kind of “evolutionary noise” (35). Unfortunately, definitive support for either viewpoint is lacking. Although footprints of past hybridization are often detected by molecular phylogenetic studies (6), their presence does not indicate that the hybridization was adaptive. Likewise, the documentation of fit hybrids in contemporary hybrid zones (2) is not proof of an adaptive role for hybridization, because fit hybrid genotypes may be transitory as a result of recombination (7).

One means by which fit hybrid genotypes may become established is through diploid hybrid speciation (8, 9). In this process, a reproductive barrier arises in a new hybrid lineage, which protects it from gene flow with its parental species or other hybrid genotypes. Models of diploid hybrid speciation suggest that reproductive isolation may arise through rapid chromosomal repatterning, ecological divergence, and/or spatial separation (8, 10). Ecological divergence may be of particular importance to the process, because computer simulations indicate that hybrid speciation is unlikely in the absence of niche separation (10, 11), and all documented examples of diploid hybrid species are divergent ecologically from their parental species (12, 13). Indeed, hybrid species often occur in habitats more extreme than those of any congener (14). Evidence that hybridization has played a key role in adaptation to these novel or extreme habitats would support the hypothesis that hybridization can be an important creative force in evolution.

Here, we ask whether hybridization has facilitated major ecological transitions in annual sunflowers of the genus Helianthus, a group that is ideal for addressing this question. Molecular phylogenetic evidence indicates that three of the 11 species in this group (H. anomalus, H. deserticola, and H. paradoxus) are stabilized diploid hybrid derivatives of two widespread species, H. annuus and H. petiolaris (14). The hybrid species appear to have been derived independently from the parental species and are found in the most extreme habitats of any Helianthus species: H. anomalus occurs on sand dunes in Utah and northern Arizona, USA; H. deserticola inhabits dry, sandy soils on the desert floor in Nevada, Utah, and Arizona; and H. paradoxus is restricted to a handful of brackish salt marshes in west Texas and New Mexico. In contrast, the two parental species are broadly distributed throughout the central and western United States and occur in less extreme environments. Helianthus annuus inhabits mesic, clay-based soils that are wet in the spring but may dry out later in the summer. Helianthus petiolaris occurs in sandier soils with less vegetation cover. Finally, microsatellite divergence of the three hybrid species from their parents suggests that they originated between 60,000 and 200,000 years before the present (1517). Thus, they arose recently enough to make partial experimental replication feasible (18, 19), yet are ancient enough to exclude anthropogenic influences in their origin.

We have used several approaches to study the role of hybridization in ecological adaptation and speciation in this group, including detailed phenotypic comparisons of synthetic and natural sunflower hybrids, selection experiments in natural sites, quantitative trait locus (QTL) analyses of synthetic hybrids, and comparisons of genomic composition between the synthetic and ancient hybrids. We ask the following questions: (i) Can the extreme traits displayed by the ancient hybrid species be experimentally generated by hybridizing the parental species? (ii) Are these phenotypes favored in the natural habitats of the hybrid species? (iii) What is the genetic basis of the extreme trait values? (iv) Do genetic correlations facilitate or impede ecological divergence? (v) Can the genomic composition of the ancient hybrid species be predicted from the QTL analysis of synthetic hybrids? That is, do the ancient hybrid species have the predicted combination of parental chromosomal segments for producing their extreme phenotypes?

Can trait differences in ancient hybrids be recreated in synthetic hybrids? We first asked whether traits that differentiate the ancient hybrid species from their parents (20) could be recreated by hybridizing contemporary populations of the parental species. This question was addressed by propagating 20 individuals of each of the five species plus 400 BC2 hybrids of H. annuus × H. petiolaris in the University of Georgia greenhouses (21). All plants that survived to maturity were measured for 22 morphological, 6 life history, and 12 physiological traits (Table 1) (table S1).

Table 1.

Comparisons of morphological, life history, and physiological traits among H. annuus and H. petiolaris and their three hybrid derivative species: H. anomalus, H. deserticola, and H. paradoxus. Only traits that map to linkage groups 1 and 10 are shown (see table S1 for comparisons of all 40 traits). Traits that significantly differ between the two parental species, H. annuus and H. petiolaris, are indicated with an asterisk. For the ancient hybrid species, traits that significantly exceed both parental trait values are referred to as “extreme.” Those that are significantly different but intermediate between the parental species are referred to as “intermediate.” Traits that do not differ significantly from one or both parental species are designated ANN-like, PET-like, or ANN/PET-like. Trait abbreviations and units of measure are as follows: DISKDIA, disk diameter (mm); LFAREA, leaf area (cm2); LFSHAP, leaf shape (length/width ratio); LFWDTH, leaf width (mm); LIGLGTH, ligule length (mm); LIGNUM, number of ligules or ray flowers; PHYLGTH, phyllary length (mm); PHYNUM, phyllary number; RTLG96, root length after 96 hours (mm); SEEDW, initial seed weight (mg); STEMDIA, stem diameter at 2 cm above the ground (mm); BUDDAY, days until budding; FLBIO, flower biomass (g); FLODAY, days until first floret; RGR, relative growth rate (cm/day); B, leaf boron concentration (ppm); Ca, leaf calcium concentration (ppm); K, leaf potassium concentration (ppm); Mg, leaf magnesium concentration (ppm); Mn, leaf manganese concentration (ppm); SLA, specific leaf area (cm2/g). Means ± SD are shown for the two parental species.

Trait H. annuus (ANN) H. petiolaris (PET) H. anomalus (ANO) H. deserticola (DES) H. paradoxus (PAR)
Morphological traits
DISKDIA* 27.48 ± 5.14 16.24 ± 2.40 13.19 12.04 15.24
Extreme Extreme PET-like
LFAREA* 63.30 ± 36.79 24.97 ± 9.48 19.25 20.21 92.18
Extreme Extreme Extreme
LFSHAP* 1.71 ± 0.27 2.35 ± 0.58 4.47 3.63 2.79
Extreme Extreme PET-like
LFWDTH* 75.9 ± 2.4 42.1 ± 10.9 27.4 28.4 70.8
Extreme Extreme ANN-like
LIGLGTH* 34.7 ± 6.0 28.28 ± 4.30 29.65 25.68 26.25
PET-like PET-like PET-like
LIGNUM* 18.32 ± 3.06 11.59 ± 2.15 10.63 10.25 14.70
Extreme Extreme Intermediate
PHYLGTH* 21.3 ± 3.9 13.0 ± 2.2 23.6 15.1 11.7
Extreme PET-like PET-like
PHYNUM* 27.00 ± 4.61 18.82 ± 2.40 17.19 16.88 18.60
PET-like Extreme PET-like
RTLG96 13.2 ± 6.0 6.4 ± 3.9 13.2 8.6 12.2
ANN-like PET-like ANN-like
SEEDW 5.64 ± 0.37 1.71 ± 0.32 7.39 3.11 4.24
Extreme Intermediate Intermediate
STEMDIA 14.54 ± 1.63 7.55 ± 1.16 6.02 7.74 11.15
Extreme PET-like Intermediate
Life history traits
BUDDAY* 37.85 ± 11.11 34.35 ± 6.91 45.31 29.50 100.06
Extreme Extreme Extreme
FLBIO* 55.7 ± 10.4 10.0 ± 4.8 6.0 4.8 11.8
PET-like PET-like PET-like
FLODAY* 59.35 ± 13.94 48.71 ± 7.24 60.19 42.50 106.00
ANN-like Extreme Extreme
RGR 2.56 ± 0.40 2.37 ± 0.50 2.36 2.34 1.19
PET-like PET-like Extreme
Physiological traits
B* 66.04 ± 19.18 66.54 ± 16.93 61.86 32.10 39.81
ANN/PET-like Extreme Extreme
Ca 16,927.34 ± 7064.30 19,685.13 ± 7358.02 13,436.70 16,843.16 22,338.20
ANN/PET-like ANN/PET-like ANN/PET-like
K* 49,226.90 ± 6831.37 61,708.53 ± 5885.27 44,451.29 49,298.71 38,310.09
Extreme ANN-like Extreme
Mg* 3283.18 ± 582.83 4212.85 ± 542.28 3455.07 4271.48 5698.12
Intermediate PET-like Extreme
Mn 196.69 ± 32.79 216.42 ± 61.76 215.35 189.62 354.12
ANN/PET-like ANN/PET-like Extreme
SLA* 207.88 ± 50.55 320.17 ± 72.87 240.53 268.67 241.85
Intermediate Intermediate Intermediate

When compared to the parental species, H. anomalus differed significantly for 20 of the 40 traits (Table 1) (table S1). Of these 20 traits, 13 significantly exceeded the parental trait values and seven were intermediate. For H. deserticola, 11 traits were extreme relative to the parental species and three were intermediate. Helianthus paradoxus was the most divergent of the three hybrid species, with 15 extreme and eight intermediate traits.

Intermediate trait values are most easily accounted for in hybrid species because hybrids combine alleles from both parental species. Indeed, the full range of intermediate values were recovered for all traits in the synthetic BC2 hybrids (table S1). However, extreme phenotypic values are frequently reported in segregating hybrids as well, a phenomenon referred to as transgressive segregation. A recent survey of 171 studies of segregating hybrids revealed that 536 (43.6%) of 1229 traits examined were transgressive (22). An even higher proportion of extreme traits was observed in the present study. Twenty-five (62.5%) or 27 (67.5%) of the 40 traits assayed in the BC2 hybrids were transgressive, depending on whether the observed number of extreme phenotypes was compared to expectations for two versus three standard deviations, respectively (table S1). These are very high percentages for wild, outcrossing species (22).

There was not a perfect match, however, between the extreme traits observed in the three ancient hybrid species and the presence or direction of transgression in the BC2 population. In some instances, the lack of significant transgression appears to be a statistical artifact of high levels of phenotypic variation in one of the parental species, but for other traits the range of phenotypic variation in the BC2 is truly narrow. Thus, a more relevant measure of the possible contribution of hybridization to phenotypic divergence is the proportion of extreme traits that are within the range of variation found in the BC2 population. For H. anomalus, 11 of 13 (84.6%) extreme traits were within the range of the BC2 population and thus could be accounted for by hybridization (table S1). All 11 extreme traits (100%) in H. deserticola were within the range of phenotypic variation observed in the BC2, and 10 of 15 (66.7%) extreme traits in H. paradoxus could be accounted for by hybridization (table S1). Traits beyond the range of the BC2 population might be transgressive in a reciprocal backcross population. Alternatively, they may have arisen through mutational divergence rather than hybridization. Either way, it is clear that the majority of extreme traits observed in the ancient hybrid species could have been generated through hybridization.

Are the extreme phenotypes adaptive? Although the three ancient hybrid species are phenotypically divergent with respect to their parental species, the trait differences do not necessarily represent adaptations to the habitats in which they occur. They could, for example, have diverged through drift or as a by-product of adaptive developmental changes (23). There are two kinds of evidence, however, that suggest that many of the trait differences are adaptive.

First, the three hybrid species have suites of traits that are commonly observed in unrelated taxa found in the same habitats. For example, H. anomalus, like other sand dune endemics, has large seeds, rapid root growth, and succulent leaves (Table 1) (table S1). Large seeds reduce the probability of burial by moving sand, rapid root growth helps tap into water reserves, and succulent leaves reduce water loss in arid environments (24). Helianthus deserticola has many classic features of a desert annual, including rapid flowering, small narrow leaves, and reduced boron uptake (Table 1) (table S1). Rapid flowering ensures reproduction after heavy seasonal rain, the small narrow leaves decrease water loss and avoid fatal overheating (25), and reduced boron uptake may increase boron toxicity tolerance in low-rainfall regions. Like many other salt-loving species (halophytes), H. paradoxus reduces the toxic effects of sodium and other mineral ions through active exclusion (26), internal sequestration, and increased leaf succulence (27).

Second, we have conducted a series of experiments in parallel to those reported here, in which BC2, parental, and hybrid species individuals were transplanted into the habitat of each of the ancient hybrid species. The results from these experiments have been fully analyzed only for the H. paradoxus habitat (26), but they are illustrative of preliminary findings from the H. anomalus and H. deserticola sites. As predicted, leaf succulence and mineral ion uptake are under strong directional selection in the H. paradoxus habitat, and the strength of selection for QTLs underlying these traits (the selection coefficient, s, ranges from 0.08 to 0.13) is strong enough to account for the origin of H. paradoxus in parapatry with its parental species (26). Also, QTLs from both parental species were significantly positively selected in the H. paradoxus habitat, as required for models of diploid hybrid speciation (10).

What is the mode of gene action responsible for transgression? To determine how extreme phenotypes are generated through hybridization, we genotyped 384 BC2 plants of H. annuus × H. petiolaris for 96 molecular markers known to cover most of the sunflower genome (21). The genomic location, percentage of variance explained (PVE), and additive effects of QTLs underlying the 40 traits scored in the previous experiment were estimated with composite interval mapping (21). In addition, all pairs of marker loci were tested for interaction effects or epistasis (21).

We detected 185 QTLs for the 40 traits (Fig. 1) (fig. S1 and table S2). QTL effects were modest in magnitude, ranging from 4 to 17% PVE. However, it is the directionality of QTL effects that is most relevant to the issue of transgressive segregation. More than 39% of QTL effects were in the opposite direction of species differences, and 34 of the 40 traits analyzed had at least one opposing QTL (fig. S1 and table S2). That is, for these QTLs, the H. annuus allele produced a more H. petiolaris-like phenotype, and vice versa.

Fig. 1.

QTL positions and correlations among QTLs on selected linkage groups for morphological, life history, and physiological traits (Table 1) differentiating H. annuus and H. petiolaris. Marker names are listed to the left of each linkage group, and QTL positions, 1-lod support intervals, and magnitudes are indicated by vertical bars to the immediate right of each linkage group. The plus or minus symbol above each QTL indicates the direction of effect of the H. annuus allele. The three groups of colored bars farther to the right of each linkage group show the direction of effect of each QTL with respect to the three ancient hybrid species (ANO, H. anomalus; DES, H. deserticola; PAR, H. paradoxus). Blue bars indicate that the H. annuus QTL allele is in the direction of the ancient hybrid species; yellow bars indicate that the H. petiolaris QTL allele is in the direction of the ancient hybrid. Gray bars indicate that the hybrid species is intermediate for the trait or cannot be differentiated from either parental species. Overlapping bars that are mostly the same color (excluding the gray bars) indicate that genetic correlations are favorable for producing the multitrait phenotype of the corresponding ancient hybrid species.

The presence of QTLs with opposing effects provides a simple explanation for transgressive segregation: Segregating hybrids can combine plus alleles or minus alleles from both parents, thereby generating extreme phenotypes (Table 2). This “complementary gene action” model accounts for most of the transgressive phenotypes observed in the H. annuus × H. petiolaris BC2 population (table S2). All but five of the transgressive traits had complementary QTLs. Of the five traits that lacked opposing QTLs, three had a single detected QTL, and thus the complementary gene model could not be tested. For the two remaining traits (LIGNUM and SLA), putative antagonistic QTLs were detected that barely fell beneath the significance threshold. On the other hand, some traits had complementary QTLs but did not display significant phenotypic transgression. This could be due to the limited sample size of the BC2 population or to high phenotypic variance in the parental species.

Table 2.

Hypothetical example of transgressive segregation due to the complementary action of genes with additive effects.

QTLs Phenotypic values
Species A (AA genotype) Species B (BB genotype) Transgressive F2 Transgressive F2
1 +1 −1 +1 (AA) −1 (BB)
2 +1 −1 +1 (AA) −1 (BB)
3 +1 −1 +1 (AA) −1 (BB)
4 −1 +1 +1 (BB) −1 (AA)
5 −1 +1 +1 (BB) −1 (AA)
Total +1 −1 +5 −5

Although most transgressive phenotypes can be accounted for by complementary genes, epistatic interactions appear to contribute as well. Significant epistasis was observed for 18 traits, 14 of which showed significant transgression (tables S1 and S3). These observations are broadly consistent with evidence from studies of cultivated plants, in which complementary gene action is the primary cause of transgressive segregation, with less frequent contributions from epistasis and overdominance (22, 28).

Do genetic correlations facilitate or impede ecological divergence? The phenotypic comparisons and QTL experiments described above indicate that most trait differences in the ancient hybrid species can be recovered by hybridizing their parental species. To generate the complex, multitrait phenotype of a hybrid species, however, it is necessary to combine all trait differences into a single individual. This will only be possible if closely linked or pleiotropic QTLs have effects that are in the same direction with respect to the hybrid species phenotype. Thus, for each of the hybrid species, we asked whether correlations among closely linked or pleiotropic QTLs were suitable for producing their phenotype (21). This was accomplished by testing whether the positions [i.e., 1-lod (logarithm of the odds ratio for linkage = 1) support intervals] of QTLs with effects in the same direction with respect to a given hybrid species phenotype overlapped more frequently than would be expected by chance (Fig. 1) (fig. S1). Congruence in the direction of QTL effects was measured with the φ coefficient of association, a standard measure of association that can vary from -1 to 1 (29).

Overlapping QTLs most often had effects in the same direction with respect to the phenotypes of the ancient hybrid species (Fig. 1) (fig. S1). The φ coefficient of association was 0.32 (N = 256, P < 0.001) for H. paradoxus, 0.47 (N = 256, P < 0.001) for H. anomalus, and 0.53 (N = 256, P < 0.001) for H. deserticola. Note that these are conservative estimates of congruence levels, because the 1-lod support intervals for some QTLs were large (Fig. 1) (fig. S1 and table S2). Incongruence of QTL directions for QTLs within 2 cM of each other are infrequent; only 4, 5, and 10 such instances of incongruence were observed for H. anomalus, H. deserticola, and H. paradoxus, respectively.

These results indicate that genetic correlations likely facilitated the origin of the three ancient hybrid species and the acquisition of their multitrait phenotypes, particularly for H. anomalus and H. deserticola. It is noteworthy that both species carry multiple chloroplast DNA haplotypes from their parental species (15, 16), which suggests that they may be multiply derived in nature. In contrast, less frequent positive genetic correlations make it difficult to recreate the multitrait phenotype of H. paradoxus, and this species appears to have a single origin (17).

Can the genomic composition of the ancient hybrid species be predicted from QTL analyses of synthetic hybrids? The experiments described above show that hybridization could have facilitated ecological divergence, but do not prove that it actually did so. An alternative hypothesis, for example, is that the ecological differences that characterize the three ancient hybrid species arose through mutational divergence and were incidental to hybrid origin. To determine whether hybridization actually did facilitate ecological divergence, we compared the genomic composition of the three ancient hybrid species with predictions from the QTL analyses of the BC2 population of H. annuus × H. petiolaris.

To estimate genomic composition, we generated high-resolution genetic linkage maps, based primarily on microsatellite and amplified fragment length polymorphism (AFLP) markers (21), for each of the three ancient hybrid species. Seventeen linkage groups were recovered for each of the three hybrid species, which corresponds to their haploid chromosome number (Fig. 2) (fig. S2). For H. anomalus, the present study added 318 markers to the previously published 701-marker map (30), bringing the total number of markers mapped to 1019. The 1019 markers spanned 1908.3 cM, with an average spacing between markers of 1.90 cM. The linkage maps for H. deserticola and H. paradoxus reported here comprise 672 and 771 markers, respectively. Map lengths and average marker spacing are 1229 cM and 1.88 cM, respectively, for H. deserticola, and 1420.5 cM and 1.88 cM, respectively, for H. paradoxus.

Fig. 2.

Comparison of the genomic composition of the ancient hybrid species with predictions from the QTL analyses (Fig. 1) (fig. S1) for five collinear chromosomes (see fig. S2 for the remaining 12 chromosomes). Linkage groups are designated by number according to the standard nomenclature for sunflower (21). Letter(s) in parentheses after linkage group designations for H. anomalus enable comparisons with previous genetic mapping studies of this species (18, 30). Positions of molecular markers used in the QTL analyses are shown to the left of each linkage group, and the distribution of species-specific parental markers (table S4) is shown in the center of each linkage group, with markers derived from H. annnus in blue and those from H. petiolaris in yellow. Bars to the right of each linkage group indicate the parentage of chromosomal segments, as predicted from the QTL analyses.

The most likely parental species origin of each mapped marker was then determined by surveying five natural populations each of H. annuus and H. petiolaris (21). In all, 427, 290, and 325 of the markers mapped in H. anomalus, H. deserticola, and H. paradoxus, respectively, could be assigned to one or the other parental species and thus were informative with respect to genomic composition (table S4).

We then used the φ coefficient of association (21) to compare the genomic distribution of parental species markers in each of the ancient hybrids with predictions from the BC2 QTL data. Species-specific parental markers mapped in each of the hybrid species either matched or did not match the identity of the predicted parental species donor for that genomic region (Fig. 2) (fig. S2).

Congruence between predicted and actual genomic composition was high (Fig. 2) (fig. S2), with φ coefficient values of 0.56 (N = 150, P < 0.001) for H. paradoxus, 0.58 (N = 193, P < 0.001) for H. anomalus, and 0.65 (N = 94, P < 0.001) for H. deserticola. Because of limited map resolution for species-specific markers, we cannot determine the actual lengths of parental chromosomal segments. Possibly they are very large, as previously suggested for H. anomalus (30). If this were the case, it would suggest that hybrid speciation occurred rapidly, resulting in the fixation of large parental chromosomal segments that have remained largely intact since their initial establishment. Alternatively, the hybrid species' genomes may be considerably more fine-grained than shown here, and the clustering of markers derived from the same parental species may result from the preponderance of genetic material from that parent in a given genomic region (and not from the presence of a fully intact chromosomal segment). Either way, the ancient hybrid species appear to have the predicted combination of parental genetic material for producing their extreme phenotypes.

Previously (18), it was shown that three synthetic hybrid lineages of H. annuus × H. petiolaris converged onto a combination of chromosomal blocks that was similar to that found in H. anomalus, although some differences remained. The present data set accounts for aspects of the H. anomalus genotype that could not be explained by fertility selection alone. For many genomic regions, however, there was concordance between the predicted genomic composition from fertility selection and the QTL analysis of phenotypic differences, implying that genes causing hybrid inviability or sterility may overlap with those responsible for phenotypic differences.

Conclusions. Our results corroborate the view that hybridization can play an important creative role in adaptive evolution, and suggest a simple genetic mechanism (complementary gene action) by which this may occur. Whether these conclusions can be extrapolated to taxa other than Helianthus is less clear. Hybridization is frequent in many organismal groups (2), particularly plants (31), fish (32), and birds (33), and transgressive segregation appears to be the rule rather than the exception in interspecific crosses (22). Thus, an important and widespread role for hybridization in adaptive evolution is plausible. For hybridization to contribute to adaptation, however, fit hybrid genotypes must escape from “the mass of unfit recombinants” in a hybrid population [(7), although see (34)]. Mechanisms by which this may occur include asexual reproduction, selfing, diploid hybrid speciation (discussed herein), and the introgression of advantageous alleles (7). Unfortunately, little is known about the frequency of the latter two mechanisms, which are most applicable to sexual, outcrossing species.

Our results also suggest a largely unexplored mechanism for large and rapid adaptive transitions, such as the colonization of discrete and divergent ecological niches. Entry into discrete niches is theoretically difficult, because it may require simultaneous changes at multiple traits and/or genes. Hybridization offers a means by which this difficulty may be overcome because, unlike mutation, it provides genetic variation at hundreds or thousands of genes in a single generation. Moreover, new allelic variation introduced by hybridization has already been tested by selection in the genetic background of one of the parental species and thus is less likely to be deleterious.

Evolutionary biologists have struggled to link results from experimental microevolutionary studies of contemporary populations directly to evolutionary changes occurring in the distant past (34). Our results bridge this gap by showing that large morphological and ecological differences in three ancient hybrid sunflower species can be recreated through contemporary hybridization, and that these ancient hybrid species have the predicted combination of parental chromosomal blocks for producing their phenotypes. Hence, hybridization did indeed facilitate major ecological transitions in wild sunflowers.

Supporting Online Material

Materials and Methods

Figs. S1 and S2

Tables S1 to S4


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