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a Department of Botany, University of Guelph, Guelph, Canada N1G 2W1; andDepartment of Botany, University of Washington, Seattle, Washington 98195–5325
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Key Words: Chamerion angustifolium • Epilobium • hybrid zone • intercytotype mating • mosaic • Onagraceae • polyploidy • triploids
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Contact zones, or geographic regions of overlap, between polyploids and their diploid progenitors provide an opportunity to observe the processes involved in the origin and divergence of polyploids. Like other hybrid zones, the distribution of chromosomal cytotypes within mixed zones can provide insight into the nature of interactions between parental genotypes (e.g., mating, competition), the genetic basis of their differences, and the mechanisms and strength of reproductive isolation that have evolved as a consequence (Harrison and Rand, 1989). In addition, the distribution of cytotypes may provide clues to the mechanisms maintaining the contact zone itself. Most theoretical models explain hybrid zones as a balance between dispersal by the parental taxa and selection against hybrid offspring. They differ, however, with respect to the role of selection acting on the parental types (Arnold, 1997). For example, contact zones characterized by a monotonic cline are called "tension zones," whose position is viewed as independent of the selective environment (Barton and Hewitt, 1985). Zones characterized by a patchy structure are called "mosaic zones" and are most likely maintained by an underlying environmental gradient (Harrison and Rand, 1989).
Chamerion angustifolium (formerly Epilobium, Onagraceae) is a perennial, herbaceous plant that exhibits variation in chromosome number throughout its geographical range. In North America, diploid (2n = 2x = 36) and tetraploid (2n = 4x = 72) plants have been found and are geographically separated with respect to latitude (Mosquin, 1966, 1967; Mosquin and Small, 1971), with the diploids occurring at higher latitudes. A contact zone between these cytotypes extends across North America near the southern limit of the boreal forest, and also extends north and south along the Rocky Mountains. Within the contact zone in the Rocky Mountains, diploids generally occur at higher altitudes than tetraploids (Flint, 1980). Still there are sites in the contact zone where both diploids and tetraploids occur in close proximity (zone of sympatry). However, the distribution of polyploidy in regions of sympatry and the potential for and degree of interaction between cytotypes are not known.
As part of a broader investigation into the evolutionary dynamics of polyploids, our objective in this study was to examine the diversity and distribution of cytotypes in a narrow contact zone between diploids and tetraploids in C. angustifolium. Specifically we addressed the following questions: (1) What are the frequencies of diploid and tetraploid plants? (2) Are diploids and tetraploids distributed along a monotonic gradient or in a series of monotypic patches? (3) Do triploids occur in locations with diploid-tetraploid mixtures? and (4) Do diploids and polyploids differ in morphology and reproductive capacity?
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Plants were sampled along the Beartooth Highway in Wyoming and Montana, between Red Lodge and Cooke City. This location was chosen because a broadscale survey of chromosomal variation conducted previously by Flint (1980) was available for the area and, therefore, preliminary information on the location of chromosome cytotypes was available. Leaf samples were taken at random from two diploid and three tetraploid reference sites (D2, D6, T2, T4, T26), previously identified by Flint (1980) as being fixed for diploids or tetraploids and from a putatively mixed zone (D23-mixed) in 1993 and 1994 (Fig. 1). We used the same population codes as Flint (1980) except for our D23-mixed population, which consists of Flint's D23, D22, T13, T8, and T9. The zone of sympatry, D23-mixed, occurs along an elevational gradient ranging from 2600 to 2780 m over a distance of 5 km (Fig. 1, Table 1). In the reference populations, leaves were sampled haphazardly throughout. Chamerion angustifolium spreads horizontally through the production of root buds, so a single genet may cover a large area. To maximize the number of genets sampled, all samples were taken from plants at least 2 m apart. In the D23-mixed site, leaves were sampled along transects (see insert, Fig. 1) placed in separate patches of Chamerion along the longest axis of each patch. Each transect varied in length depending on the size of the patch. Within each transect, plants were sampled approximately every 2 m. Twenty-seven transects were placed within the mixed zone, and from five to 16 plants (mean = 8.8) sampled from each. In total, 238 plants were sampled in the mixed zone and 135 (22–35 per population) in the reference populations. For each sample, a young leaf (>3 cm long) was removed, placed in a plastic bag, and put on ice until its ploidy could be determined. Leaves were returned to the laboratory within 36 h.
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For each sample, a 1 x 1 cm piece of fresh, young leaf was placed in a petri dish, on ice, and chopped using a clean razor blade in 1 mL of ice-cold buffer. The nuclei isolation buffer (pH 7), based on Michaelson et al. (1991), consisted of MgCl2 (4.3 g/L), NaCitrate (8.8 g/L), MOPS (4.2 g/L), and Triton X-100 (1 mL). The homogenate was then circulated in a pipette and filtered through a 50-µm mesh nylon screen. Finally, 400 µL of DAPI (4,6-diamino-2-phenylindole) stain were added and left at 4C for 20 min. Stained nuclei were passed through a PHYWE ICP-22 flow cytometer equipped with a HBO 100 high-pressure mercury lamp (UV). The fluorescence from each nucleus was measured and presented as a fluorescence histogram based on the 5000–10 000 nuclei examined per sample. The mean fluorescence for a leaf sample is proportional to the DNA content per nucleus for that individual. Chicken red blood cells (CRBC), stained in the same way, were run initially and after every fourth sample, as an external standard. To account for variation in machine parameters from one day to the next, estimates of DNA content were expressed as the proportion of the mean value for the CRBC standard run on the same day (hereafter referred to as relative fluorescence).
To examine the relationship between DNA content and ploidy, relative fluorescence was estimated for known diploids, triploids, and tetraploids that were generated and grown in the greenhouse. The three cytotypes were created by crossing four known diploid individuals from population D2 and four known tetraploid individuals from population T2 in all possible combinations (diallel design). Relative fluorescence was estimated for 21 progeny from the 2x x 2x crosses, 41 progeny from the 4x x 2x or 2x x 4x crosses, and 25 from the 4x x 4x crosses.
To classify each plant collected in the field according to ploidy, we used the distribution of relative fluorescence values for diploids, triploids, and tetraploids from the controlled crosses. In addition, diploid reference populations and a uniformly diploid transect (D23 Transect 6) sampled in the field were used to establish the expected range of fluorescence for diploids, triploids, and tetraploids from the field. We assumed that the range for tetraploids would span from two times the lowest value for diploids to two times the largest value for diploids. The expected fluorescence for triploids should range from the mean of the lowest diploid and tetraploid values to the mean of the highest values for diploid and tetraploids. Tetraploid reference populations were not used for determining the ploidy of samples because it was obvious from fluorescence values that they were not completely uniform. This second method of establishing expected ranges of relative fluorescence was used because the range of fluorescence values from the field did not correspond exactly to the range of fluorescence values from greenhouse-grown plants (mean relative fluorescence for diploids = 0.65, 0.63, and 0.49 for greenhouse, 1994 field, and 1993 field plants, respectively). This was not a problem in 1994, as the diploids, triploids, and tetraploids sampled were very close to greenhouse values and they appeared as three distinct modes of fluorescence. Data from 1993, however, were lower on average and of greater variance than those from 1994. The cause of differences in fluorescence values among years is unclear but may be a result of machine settings or environmental effects that could influence the degree of intercalation of the fluorescent dye (unpublished data). By comparing the fluorescence data from both years to the same diploid reference populations and by classifying plants as triploids only when their DNA content fell between the ranges for diploids and tetraploids (i.e., ambiguous relative fluorescence values were classified as either diploid or tetraploid), we feel our approach for determining ploidy was conservative.
While collecting leaf tissue in the mixed zone, we measured several other variables: leaf length, number of shoots, evidence of stems severed by herbivores, and reproductive status (vegetative, buds present, flowers produced). Leaf length was measured because Flint's (1980) results indicated that leaf length was the character best able to distinguish diploids from tetraploids. A mixed-model analysis of variance (ANOVA) with subpopulation (random effect: D22, T8–9, D23, T13), ploidy (fixed effect: diploid, triploid, and tetraploid) and subpopulation x ploidy interaction as the sources of variation was used to examine variation in leaf length and number of shoots. Contingency table analysis, using G and chi-square (when some cells = 0) tests were used to examine the dependence of reproduction on ploidy.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The frequencies of diploids, triploids, and tetraploids were spatially heterogeneous in the mixed zone (
= 147.1, df = 52, P < 0.001; Fig. 4). All of the transects that were fixed for a single cytotype occurred in the central to upper elevations of the mixed site (Table 1, Fig. 4). Neighboring transects were just as likely to be fixed for a different ploidy as for the same one. Transects with more than one ploidy were prevalent throughout the mixed zone, especially in the central to low elevation subpopulations, but they varied widely in cytotype frequencies (Fig. 4).
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On average, 23.4% of all plants showed some damage from herbivory. There were, however, no differences in the probability of herbivore damage among ploidies (G = 0.70, df = 2, P > 0.50). Significant differences did occur among ploidies in the proportion of plants that were vegetative rather than reproductive (i.e., had flower buds, flowers or fruit) (G = 11.9, df = 2, P < 0.005; Table 2). Sixty-five percent of diploids were reproducing at the time of the census, compared to 31% of triploids and 38% of tetraploids. This trend was apparent in each subpopulation, although it was marginally significant (0.05 > P < 0.10) in only two of four subpopulations (D22 and D23). At least 50% of all diploid individuals were reproductive in all subpopulations, whereas the proportion of triploids and tetraploids that were reproductive never reached 50% in any subpopulation. All the triploids and tetraploids that were classified as reproductive only had flower buds; none were observed with open flowers or fruit. Diploids were equally likely to have flower buds as triploids and tetraploids (G = 3.8, df = 2, P > 0.10), but were significantly more likely to have had open flowers ( = 15.9, df = 2, P < 0.001; Table 2). While the proportion of triploids and tetraploids flowering was zero, 12.5% of diploids had or were producing flowers. The frequency of flowering in diploids was highest (22%) in the high-elevation subpopulation, D22, moderate in the populations at intermediate elevation (percentage flowering: T8–9, 8.7%; D23, 16.7%), and lowest (0%) in the low-elevation T13.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The main finding in this study was that cytotype structure at a narrow diploid–tetraploid boundary was more complex than had been described at larger spatial scales (Mosquin, 1966; Flint, 1980). Mosquin (1966) and Flint (1980) reported the distributions of diploids and tetraploids as being parapatric with no evidence of mixing. The mixed zone sampled in this study cannot be characterized as two parapatric populations with no mixing, nor does it resemble a gradual, clinal transition from one cytotype to the other across the elevational gradient as has been described for many hybrid zones (Harrison and Rand, 1989). Rather, the cytotypes are intermixed in a mosaic-like pattern, where frequencies of diploids and tetraploids fluctuate widely from one transect to the next. A portion of this variation may be due to sampling error from small samples sizes in each transect. As a result, we may have underestimated the frequency of mixed patches within the contact zone. Also in contrast to previous studies, triploids were found, especially where diploids and tetraploids occurred in close proximity (i.e., on the same transect). It is important to note that triploid plants were identified from estimates of DNA content rather than from direct chromosome counts. Although the relationship between DNA content and ploidy was strong, and our interpretation of ambiguous DNA content values should provide a minimum estimate of triploids, further chromosome counts are necessary to verify the frequency of triploidy and the degree of aneuploidy among them.
The fact that diploids and tetraploids were geographically separated for the majority of their distributions is not a surprising result and has been described repeatedly for allo- and autopolyploid taxa in the last century (Manton, 1934; Clausen, Keck, and Hiesey, 1945; Stebbins and Zohary, 1959; Kay, 1969; Soltis, 1984; Rothera and Davy, 1986; Lumaret et al., 1987; Felber, 1988a; Van Dijk, Hartog, and Van Delden, 1992), although exceptions do occur (e.g., Nesom, 1983). Whether these distributional differences are the result of divergence in ecological tolerances between diploids and tetraploids or simply a historical product of colonization is not clear and is beyond the scope of this study. In contrast to our knowledge of broadscale distributions, much less information is available on the chromosomal structure and environmental correlates where the cytotypes are sympatric. In a detailed analysis of the local distribution of diploid and tetraploid cytotypes of Dactylis glomerata, Lumaret et al. (1987) found much variation in the local composition of populations. Diploids and tetraploids co-occurred, but their relative abundances differed in different microhabitats. Van Dijk, Hartog, and Van Delden (1992) found that cytotype frequencies in sympatric populations of Plantago media were highly heterogeneous, but no obvious correlation with the environment was apparent. These results are consistent with those for C. angustifolium in that diploids and tetraploids occur in close proximity. For C. angustifolium, the distribution of each cytotype may be only weakly associated with different microsites. Transects dominated by diploids are often located in low-lying drainage areas that are mesic and less exposed. However, most transects contained both cytotypes and may represent habitats that are marginal, yet tolerable, for both diploids and tetraploids. While there may be physical environmental variables that are associated with each cytotype, these associations are probably not strong, and it is difficult to ascertain which specific physical variables may be important in determining their distributions. Clearly, reciprocal transplant experiments are necessary to clarify the role of environment and ecological differentiation in the microdistribution of diploids and tetraploids in C. angustifolium.
Triploids were often present whenever diploid and tetraploid individuals of C. angustifolium occurred in the same transect. In contrast, triploids were rarely or never observed in the zones of sympatry in other autopolyploid complexes (Soltis, 1984; Lumaret et al., 1987; Wolf, Soltis, and Soltis, 1990; Van Dijk, Hartog, and Van Delden, 1992). The difference in results may be explained by differences in the viability of triploid seeds. For example, the absence of triploids in Plantago media corresponds with the low rate of triploids produced in controlled crosses (Van Dijk, Hartog, and Van Delden, 1992). In C. angustifolium, triploids are readily produced in diploid–tetraploid crosses and are also observed at low frequencies (7%) in the seed offspring of diploids and tetraploids from the mixed zone (B. Husband and D. Schemske, unpublished data). While reproductive triploids are present in C. angustifolium, they occur at lower frequencies than would be expected if mating were random between diploid and tetraploid cytotypes. Such a deficiency of triploid plants may be the result of asynchronous flowering, low mating success in between-cytotype pollinations, reduced survival of triploid seedlings, or nonrandom pollen transfer. Positive assortative mating is more likely than random mating if pollinators can discriminate among the cytotypes or if most of their flights are within patches of single cytotypes. Unfortunately, none of this information is available for polyploid species at a diploid–tetraploid contact zone.
Significant differences in morphology and reproduction among the cytotypes were observed in the mixed population. Only triploids were distinct with respect to leaf length, a morphological character used previously to discriminate between diploids and tetraploids (Flint, 1980). Clearly, other morphological characters need to be measured, but this result indicates that it would be extremely difficult to identify the cytotypes with certainty in the field, a pattern not uncommon for other autopolyploids at least in the zone of sympatry (Lumaret et al., 1987; Van Dijk, Hartog, and Van Delden, 1992). Patterns of reproduction were, however, much different among cytotypes. Diploids were significantly more likely to be reproductive (in bud or flower) than either triploids or tetraploids. Only diploids had successfully reached anthesis when we sampled at the end of the growing season. These differences in flowering propensity between the diploid and tetraploid cytotype may also limit opportunities for intercytotype mating in the contact zone (Felber, 1988b).
While the likelihood of flowering was highest for diploids, the proportion of diploid plants reaching anthesis dropped from 22 to 0% with decreasing elevation. In other words, diploids exhibited their highest potential for reproductive success at the elevations at which they are most common (high elevation). Tetraploids and triploids did not show a corresponding association with elevation. This is either because the entire mixed zone represents a marginal environment for polyploids or that the growing season at lower elevations was not complete, and that we did not sample late enough in the season to observe flowering in tetraploids and possibly triploids. Given that reproduction was scored in September, we think it is unlikely that the growing season continued beyond our sampling period. An in situ comparison of diploid and tetraploid Dactylis glomerata conducted by Lumaret et al. (1987) showed that cytotypes always had higher fitness in local environments where they were most common. Unfortunately, such comparisons are difficult to interpret because the location of each cytotype may be confounded with physical environment.
What factors may be involved in maintaining the distributions of cytotypes and the position of the contact zone between diploids and tetraploids in C. angustifolium? The classical view of a hybrid zone is of a monotonic cline representing a gradual or sudden replacement of one parental type with the other (Harrison and Rand, 1989). The spatial distribution of the parental taxa and the position of the contact area may be a result of their different ecological preferences along an environmental gradient (Endler, 1977) or it may be strictly an artifact of colonization history (Barton and Hewitt, 1985). The position of the contact zone is being maintained in one case by ecological sorting, while in the other, by selection against the rare parental type through selection against its hybrid offspring. Our results stand in contrast to the classical model in that the distribution of cytotypes is not clinal but rather a collection of patches that are heterogeneous in composition. Harrison and Rand (1989) describe this pattern as a mosaic hybrid zone. The distribution of cytotypes in C. angustifolium is consistent with a hybrid zone that is maintained by sorting along an environmental gradient. Patches are often composed of predominantly one cytotype, indicating slight differences in ecological amplitude. However, where both diploid and tetraploids co-occur, triploids also are present. This may occur if microsites that are suitable for the parental cytotypes are also favorable to triploids. This role of environmental heterogeneity in determining cytotype distributions is also supported by the fact that morphology and reproduction vary as a function of elevation within the mixed zone. If the contact zone was maintained by selection against triploids one would expect patches to consist of either diploids or tetraploids but this is not the case. Still, without further examination of the relative fitnesses of diploids, triploids, and tetraploids, we cannot completely exclude the possibility that the distribution of cytotypes is being maintained independently of the elevation gradient. Additional research on the relative fitness of triploids in the contact zone is necessary to understand their role in the maintenance of the hybrid zone and the dynamics of polyploid populations in Chamerion angustifolium.
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FOOTNOTES |
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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