Origins of genotypic variation in North American dandelions inferred from ribosomal DNA and chloroplast DNA restriction enzyme analysis.
Key words. - Chloroplast DNA, clonal variation, hybridization, ribosomal DNA, Taraxacum.
Agamic complexes, resulting from the combination of agamospermy and hybridization, characteristically have intricate genetic relationships between the original parental species and the derived apomictic forms (Grant, 1981). Often the identity of the parental species and the direction of hybridization remains obscure. A familiar example of an evolutionary successful and geographically widespread agamic complex is the genus Taraxacum (Asteraceae), the dandelions. Asexual dandelions reproduce by nonpseudogamous gametophytic parthenogenesis (Gustafsson, 1946) and are presumably allopolyploids (Richards, 1986). The morphological, ecological, and geographic integrity of asexual Taraxacum polyploids has led to the description of nearly 2,000 microspecies comprising 90% agamospecies and 10% diploid species in 26 sections (Richards, 1973).
West central Asia is the putative origin of the genus Taraxacum, and members of the genus migrated to northern and other temperate regions (van Soest, 1958a; Richards, 1973). The genus is geographically widespread, although individual taxa may have restricted distributions. In particular, sexual diploids tend to have localized distributions and are usually found in mixed populations with triploids in Europe (Jenniskens, 1984; den Nijs and Sterk, 1984a, 1984b; den Nijs and van der Hulst, 1988) and Asia (Morita, 1976, 1980). Sexual species are rare in northern Europe, and outside of Europe and Asia native sexual species have been found in Greenland (T. pumilum), South America, and the Sierra Nevada Mountains of California (Richards, 1986). In contrast, although many asexual polyploids have successfully colonized North America, surveys of the weedy Taraxacum flora (notably sections Ruderalia and Erythrosperma) have not revealed diploid specimens (van Soest, 1958b; Lyman and Ellstrand, 1984; den Nijs et al., 1990).
Dandelions putatively colonized the Americas post-Pleistocene via Beringia (Chaney and Mason, 1936; Richards, 1973), and dandelions were also presumably introduced into the United States by European settlers (Solbrig, 1971). Therefore, the North American Taraxacum flora comprises native and more recently introduced microspecies (Haglund, 1943; van Soest, 1958a, 1958b; Richards, 1973; Doll, 1977). The common weedy dandelion in North America is a triploid apomict and is broadly classified as T. officinale Wiggers, or T. laevigatum (Willd.) DC, the red seeded dandelion (Taylor, 1987). Although others consider these "species" to be an aggregate of distinct agamospecies that are more equivalent in rank to sections of Taraxacum (Richards, 1985), the broad classification of weedy North American dandelions is used here. Taraxacum officinale and T. laevigatum are widespread in North America and show considerable clonal diversity based on allozymes (Lyman and Ellstrand, 1984). Solbrig and Simpson (1974, 1977) have demonstrated variation in habitat distribution and competitive ability among different T. officinale biotypes, and Taylor (1987) showed that there is no clear morphological, ecological, or biochemical differentiation between T. officinale and T. laevigatum, except for red achene coloration. In contrast to the allozyme studies that document extensive clonal diversity, the objective of this study is to identify the mechanisms that generate the clonal diversity, using direct DNA analysis.
Nuclear and cytoplasmic DNA markers are powerful tools to study the evolution of species involving hybridization and polyploidy. Biparentally inherited nuclear DNA in sexual species identifies the parental hybridizing species, and uniparentally inherited cytoplasmic DNA can be used to infer the direction of hybridization events and to identify clonal lineages. For example, nuclear and chloroplast DNA (cpDNA) have been used to document the reticulate evolution of Gossypium (Wendel et al., 1991) and interspecific gene flow and introgression in Iris (Arnold et al., 1991), Quercus (Whittemore and Schaal, 1991), and Helianthus (Rieseberg et al., 1990). Similarly, joint analysis of mitochondrial DNA and nuclear encoded allozymes have been used to determine the hybrid origin of unisexual Ambystoma (Kraus and Miyamoto, 1990) and to show the polyphyletic origin of obligate parthenogenesis in Daphnia pulex (Crease et al., 1989). In addition, cpDNA has been used to identify the species contributing the cytoplasmic genome in hybridization events (Palmer et al., 1983; Wyatt et al., 1988; Furnier et al., 1990) and to infer multiple origins of allopolyploids (Erickson et al., 1983; Soltis and Soltis, 1989; Doyle et al., 1990) and autopolyploids (Soltis et al., 1989; Wolf et al., 1990).
The goal of this study is to assess the relative contribution of two potential sources of genotypic variation, 1) the accumulation of mutations within clonal lineages and 2) multiple origins of asexual polyploids via hybridization. Restriction enzyme analysis of nuclear ribosomal DNA (rDNA) and cpDNA and combined analysis of rDNA and cpDNA identifying clonal genotypes is used to distinguish the sources of genotypic variation in North American asexual dandelions. Ribosomal DNA and cpDNA characters that are unique to asexual genotypes indicate the accumulation of mutations within clonal lineages and are evidence of independent evolution of asexual genotypes. Alternatively, an array of asexual polyploid genotypes that share the same polymorphic rDNA and cpDNA characters in various combinations are evidence of the multiple formation of the asexual forms.
Materials and Methods
Collections. - Dandellons were obtained mostly from regions in North America and Europe to survey rDNA and cpDNA in natural populations and in numerous microspecies within the genus. This sampling scheme allows the identification of polymorphism in the genus, which facilitates the differentiation of hybrid and mutational origins of genotypic variation and allows for interpretation of rDNA and cpDNA variation in a taxonomic context.
Plants or achenes of 318 dandelions were collected from various locations in North America (including a sample from Jamaica, the West Indies) and of 52 dandelions from natural populations in mostly northern regions of Europe (Table 1). These plants were broadly classified as either T. officinale, or T. laevigatum if the plant had red achenes. Using more restrictive criteria, Dr. A. J. Richards kindly identified 40 of these dandelions to specific Taraxacum agamospecies (Table 2). Additionally, 70 plants or achenes of 46 agamospecies and 6 diploid sexual species were obtained and are of European or Asian origin (Appendix). The achenes were germinated and the plants were greenhouse grown. Vouchers (listed in King, 1989) were deposited at MO.
TABLE 1. The dandelions collected from various regions in North America and Europe. The location, number of plants, and designation are listed. Representative specimens (listed in King, 1989) are deposited at MO. Location N Designation North America St. Louis, MO 57 MO 1-57 Fairbanks, AK 12 AK 1-12 Denali Park, AK 10 AK 13-22 Brooks Range, AK 4 AK 23-26 Silver Springs, MD 3 MD 1-3 Centreville, MD 14 MD 4-17 San Francisco, CA 11 CA 1-11 Louisville, KY 18 KY 1-18 Big Bend Ranger Station, CA 13 CA 12-25 Santa Barbara, CA 11 CA 26-36 Claremont, CA 10 CA 37-46 Sparks, NV 22 NV 1-22 Albuquerque, NM (1986) 10 NM 1-10 Oneida, WI 17 WI 1-17 Manchester, MA 16 MA 1-16 Ixtaccihuatl, Mexico 3 MX 1-3 Chicago, IL 14 IL 1-14 New Hampton, NH 11 NH 1-11 Pine Creek, CO 5 CO 1-5 Baca Grande, CO 3 CO 6-8 Rocky Mtn National Park, CO 7 CO 9-14 Washington, DC 5 DC 1-5 Grayson, KY 4 KY 19-22 Verona, VA 6 VA 1-6 Dowington, PA 3 PA 1-2 Beaner Falls, PA 3 PA 3-5 Central, KS 2 KS 1-2 Albuquerque, NM (1988) 12 NM 11-22 Philadelphia, PA 2 PA 6-7 New York, NY 3 NY 1-3 West Indies Jamaica 7 JM 1-7 Europe Eketorp, Sweden 11 SW 1-11 Holltorp, Sweden 10 SW 12-21 Drosstorp, Sweden 5 SW 22-26 Glasgow, Scotland 10 SW 1-10 Southern England 2 EN 1-2 Tonquedec, France 8 FR 1-8 St. Moritz, Switzerland 6 SZ 1-6
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Cloning Taraxacum Ribosomal DNA. - Ribosomal DNA clones were screened from a Taraxacum lambda library. Soybean rDNA clones pgmrl and pXBr1 (courtesy of E. Zimmer) were used to identify Taraxacum rDNA clones with 3.6, 0.9, and 5.2 kb inserts. The clones were screened, purified, and subcloned into pUC19, and plasmid DNA was prepared using standard procedures (Maniatis et al., 1982). The subclones pTEE3 (3.6 kb insert), pTEE5 (5.2 kb insert), pTEE9 (0.9 kb insert), and pXBr1 were used to map restriction enzyme sites relative to a conserved XbaI site in the 18S gene (Eckenrode et al., 1985).
Nuclear Ribosomal DNA and Chloroplast DNA Analysis. - Total cellular DNA was extracted from liquid nitrogen powdered leaf tissue by the CTAB method of Murray and Thompson (1980) as modified by King (1989). Ribosomal DNA was surveyed with 15 hexanucleotide recognition sequence restriction endonucleases (see Fig. 1) and cpDNA was surveyed with 6 of these enzymes. Taraxacum rDNA was surveyed with Taraxacum probes, cpDNA was surveyed with Petunia chloroplast clones (provided by J. Palmer) representing 21.0, 15.3, 9.2, and 9.0 kb of the large single copy region and a 7.6 kb segment of the inverted repeat. The location of the clones on the cpDNA genome, referred to as P3, P6, P8, P10, and P12, respectively, are shown in Sytsma and Gottlieb (1986). Conditions for electrophoresis and hybridization are detailed in King (1989). Probes were labeled for hybridization with [[alpha-.sup.32]P] dCTP by the random primer method (Feinberg and Vogelstein, 1983). The filters were washed and autoradiography was done as described by Learn and Schaal (1987).
Sixty-five rDNA cleavage sites were mapped; 17 sites were present in all plants, and 48 sites were polymorphic among the plants surveyed (Fig. 1). In addition, the mapping showed variation in restriction sites and rDNA repeat lengths within single plants, although the variation was not partitioned within or between the rDNA arrays in an individual. Two of the restriction sites were unique to asexual plants: an SspI site in AK 15 (Alaska) and an XbaI site in three plants of the same genotype from Jamaica (Fig. 1). Among the taxa surveyed, total repeat length ranged from about 8.6 kb in T. montanum sect. Spuria to about 11.0 kb in an agamosperm in sect. Spectabilia. The repeat lengths did not fall into discrete size classes among plants, but discrete size classes could be resolved within individuals. Most plants commonly had two repeat lengths of approximately 9.0 and 9.2 kb and up to four repeat lengths were detected within a single plant. Length polymorphisms in eight specific regions of the intergenic spacer ranging in size from approximately 100 to 1,000 bp were identified.
The rDNA genotype of each plant was determined by scoring for the presence or absence of the 48 polymorphic sites and 8 polymorphic lengths; 142 rDNA genotypes were discriminated. Six of the genotypes occurred in both red and nonred achene plants, so additional scoring for red achene coloration yielded a total of 148 rDNA clones. The relative frequency of a single clone ranged from 0. 2% (N = 1) to 26% (N = 115) and 102 of the 148 (69%) rDNA clones were unique (Fig. 2a).
The rDNA genotype of each plant was also characterized using the restriction sites only as a more conservative indication of the evolutionary relationships among the rDNA. Length variants were excluded because similar length variants in the intergenic spacer region may arise through independent events that cannot be distinguished due to the nature of the events that gencrate length variation and the low resolving power of agarose gel electrophoresis. Based on polymorphic restriction sites only, 96 rDNA genotypes were characterized.
Chloroplast DNA restriction site and fragment length polymorphisms were determined from restriction fragment profiles. Of 64 restriction fragments, 11 restriction site, 2 putative site, and 11 length polymorphisms were scored (Table 3). The putative sites were scored as site polymorphisms because fragment length variation was not detected with other enzymes in this region, and one of the two restriction fragments that would characterize the presence of the site was not visualized with P3 or adjacent probes. Length variation, determined if fragment sizes varied with several enzymes and a single probe, showed approximately 100-400 bp differences.
The 24 cpDNA polymorphisms discriminated 83 cpDNA haplotypes among 439 plants surveyed. The relative frequency of a single haplotype ranged from 0.2% (N = 1) to 29.0% (N = 129), and 48 of the 83 (58%) haplotypes were unique (Fig. 2b). Seven cpDNA polymorphisms were unique to haplotypes and were found in four polyploids and two diploid species (Table 3).
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The cpDNA haplotypes were also characterized based on the site polymorphisms only, as a more conservative estimate of the evolutionary events that gave rise to cpDNA haplotype diversity. Length variants were again excluded because similar length variants may arise from independent events in cpDNA (e.g., Palmer et al., 1985). The 13 polymorphic sites discriminated 26 cpDNA haplotypes.
Combined Analysis of Ribosomal DNA
and Chloroplast DNA
A total of 232 clones out of 440 dandelions surveyed (427 asexual plants and 13 sexual plants) were discriminated by the combination of rDNA and cpDNA polymorphic restriction sites and lengths, and the presence or absence of red achene coloration. Only nine of these clones based on this combined analysis were shared between North American and Eurasian dandelions surveyed. The relative frequency of a single clone ranged from 0.2% (N = 1) to 10.5% (N = 46) (Fig. 2c), and 79.7% (N = 185) of the clones were unique. The numbers of rDNA clones, cpDNA haplotypes, and combined rDNA-cpDNA-achene coloration clones in the North American, European and microspecies are summarized in Table 4.
Table 4. a summary of Taraxacum rDNA, cpDNA and combined rDNA-cpDNA (genotypes) characterized by restriction enzymes and red achenes in North American, European, and microspe cies dandelions. The percent of genotypes per plant sampled is in parenthesis. Collection N rDNA cpDNA Genotypes North America 318 82 (25.8%) 54 (17.0%) 145 (45.6%) Europe 52 30 (57.7%) 14 (26.9%) 37 (71.2%) Microspecies 70 56 (80.0%) 34 (48.6%) 62 (88.6%) Total
A matrix of the associations between the rDNA genotypes and the cpDNA haplotypes that were based on restriction sites only is shown in Table 5. This matrix shows that a single rDNA genotype is associated with several of the cpDNA haplotypes, and the opposite pattern, that a single cpDNA haplotype is associated with several rDNA genotypes. The figure also shows the number of plants in the survey that had a particular rDNA-cpDNA combination.
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A sample of rDNA genotype and cpDNA haplotype combinations are presented in Tables 6 and 7 to show some of the relationships observed between rDNA and cpDNA and the morphologically described asexual taxa, or agamospecies. Two distinct patterns are observed: one pattern shows genotypic diversity within agamospecies (Table 6), and conversely, the other observation is several different microspecies (the asexual and sexual taxa) share a single rDNA-cpDNA genotype (Table 7).
TABLE 6. Examples of rDNA and cpDNA variation within agamospecies. The genotype designation is rDNA based on site and length polymorphisms, rDNA based on sites polymorphisms, cpDNA haplotypes based on site and length polymorphisms, and cpDNA based on site polymorphisms. Section Apmospecies Location Genotype Ruderalia T. cordatum IL, USA 14 11 9 13 IL, VA, USA 13 11 47 13 Sweden MO, USA 28 69 47 13 NM, USA 133 74 13 21 Sweden 13 11 41 11 Celtica T. nordstedtii England 94 51 89 25 England 102 55 89 25 Czechoslovakia 115 67 89 25 Czechoslovakia 115 67 42 25
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Hybrid Origin of
The genotype analysis combining rDNA and cpDNA support multiple hybrid formation of asexual polyploids and subsequent introduction as the most likely means of generating genotypic variation in North American weedy dandelions. This is based on the complex pattems of rDNA-cpDNA associations that can most simply be explained by multiple hybridization events and the lack of weedy sexual dandelions in North America that could be involved in the formation of new asexual genotypes.
Two patterns of rDNA-cpDNA association were observed: a single rDNA genotype associated with several cpDNA haplotypes, and a single cpDNA haplotype associated with several rDNA genotypes. The production of different rDNA-cpDNA patterns of association in the asexual polyploids through hybridization can be illustrated by two models. The models are based on the rDNA of an asexual polyploid that shows the rDNA of both parents (even though the separate rDNA contribution from each parent is not identified) and the uniparental inheritance of cpDNA that is assumed to be maternal, as it is in most angiosperms.
Model 1. - The same rDNA genotype would be associated with different cpDNA haplotypes if asexual offspring were produced from crosses between two species with different cpDNA and in which both species had the opportunity to be the maternal parent. The asexual polyploid offspring would then have the same rDNA genotype (the sum of the rDNA from both species), but would have cpDNA depending on which species was the maternal parent.
The accumulation of mutations within a cpDNA lineage that maintained a single rDNA genotype could also produce this pattern. The three characters unique to cpDNA haplotypes in the asexual dandelions (in North America) are consistent with this process. Similarly, the cpDNA variation may be due to regions of the molecule that are more susceptible to recurring mutational events. Avise et al. (1987) cite several studies of mitochondrial DNA that indicate particular restriction sites "blink" on and off during evolution. Because gain and loss of restriction sites are influenced by nucleotide changes at several positions, independent events could lead to the same apparent character state. Thus, the distribution of some restriction sites among the different Taraxacum cpDNA haplotypes, which contribute to cpDNA haplotype diversity, may be due to the repeated loss and gain of particular sites. Even though these alternate processes may contribute to cpDNA haplotype diversity, the large number of genotypes are characterized by different combinations of the various cpPDNA and rDNA and show that most of the genotypic diversity is due to hybridization, and not mutation.
Model 2. - Several rDNA genotypes would be associated with a single cpDNA haplotype if a single species with a distinct cpDNA haplotype was the maternal parent in all cases of hybridization. In this case, if the hybridizing species show rDNA polymorphism, multiple hybridization events could produce different rDNA genotypes among the asexual plants. These asexual genotypes would be expected to have some shared rDNA polymorphisms among them. The rDNA polymorphisms in the asexual polyploids would be the sum of the variation contributed by the hybridizing species, yet would have the same cpDNA because they are descended from the same maternal lineage. Note that it is not necessary to be able to distinguish the rDNA from each parent to infer this process, although being able to so would aid identification of the species producing the asexual plants.
The accumulation of mutations in rDNA within cpDNA lineages explains some observations in this study and is perhaps expected because cpDNA is uniparentally inherited, does not recombine, and tends to evolve at a slower rate than nuclear genes (Wolfe et al., 1987). Therefore, cpDNA is not likely to accumulate mutations at a higher rate than rDNA within a clonal lineage. The two unique rDNA polymorphisms in North America genotypes are consistent with the accumulation of mutations in rDNA, although given the relatively small sample of taxa surveyed, the maintenance of ancestral polymorphisms cannot be ruled out. In a separate study (King and Schaal, 1990), an analysis of restriction enzyme variation in rDNA, cpDNA, and alcohol dehydrogenase- 1 (Adh- 1) between seed parent plants and asexually reproduced offspring showed that changes in rDNA and Adh- 1 occur within asexual lineages of Taraxacum and indicates that mutation within asexual lineages is an important source of genotypic variation in asexual dandelions.
How much non-Mendelian processes contribute to the rDNA genotypic diversity observed in the present study is difficult to evaluate because of the complex structure of rDNA and mutational processes that are characteristic of repeated gene families. Homogenization of the rDNA multigene family by mechanisms of concerted evolution (Arnheim, 1983) may reduce rDNA variation within a cpDNA lineage over time. Crease and Lynch (1991) have shown that obligate clonal lineages of Daphnia lose rDNA repeat-type variability over time, and in triploid parthenogenetic lizards it appears that biased gene conversion can homogenize rDNA arrays effectively "hiding" the source of one parental rDNA (Hillis et al., 1991). Another homogenizing mechanism, unequal chromatid exchange, is proposed to occur between rDNA repeats in wheat (Dvorak and Appels, 1986). These mechanisms may contribute to the homogenization of rDNA in Taraxacum to a particular repeat type within asexual lineages that have different cpDNA haplotypes. This would explain the relatively low number of unique mutations detected in rDNA and explain why certain repeat types are common and widespread. Without ruling out the importance of mechanisms homogenizing rDNA repeats and mutational processes generating variation, the characterization of all but two rDNA genotypes by different combinations of the polymorphic rDNA characters shows that hybridization has been the major mechanism generating rDNA genotypic diversity, as well as the combined rDNA-cpDNA genotypic variation.
The rDNA-cpDNA associations shown in Table 5 illustrate that the two models of hybridization are the most simple ways to explain the observed genotypic diversity in asexual dandelions, with mutational processes contributing to genotypic diversity in asexual dandelions to a much lesser extent. The evidence of multiple independent origins of asexual polyploids is shown by the rDNA-cpDNA combinations, over half of which are unique in the asexual plants (222 unique clones/427 asexual plants when both restriction sites and lengths are scored), even though the individual rDNA and cpDNA genotypes may be frequently represented. For example, Table 5 shows that the most common rDNA genotype (11) is associated with nine different cpDNA haplotypes. The most common cpDNA haplotype (13) is associated with 46 different RDNA genotypes, of which 20 are also found in combination with other cpDNA haplotypes.
North American Dandelions
Although dandelions colonized the Americas post-Pleistocene, the lack of genetic differentiation between weedy dandelions in North America and Europe indicates a recent origin and introduction of members of the aggregate species T. officinale sect. Ruderalia, and T. laevigatum sect. Erythrosperma into North America.
Hybridization and production of polyploids resulting from crosses between sexual diploids and asexual polyploids are thought to occur among dandelions in sections Ruderalia and Erythrosperma, presumably through occasional reductional meiosis of the pollen or egg in the polyploids (den Nijs and van der Hulst, 1988; Morita et al., 1990). In North America, clonal genotypes are unlikely to be produced from sexual reproduction between facultative agamosperms and sexual diploids because weedy diploids are absent, or have not been detected. It is more plausible that clonal genotypes are introduced from regions where asexual and sexual dandelions cooccur, as in various regions of Europe (den Nijs and Sterk, 1984a, 1984b; Jenniskens, 1984; den Nijs and van der Hulst, 1988; den Nijs et al., 1990) and Eastern Asia (Morita, 1980). Sexual reproduction between ploidy levels has been demonstrated by experimental hybridizations between diploids and triploids, in both directions, which produce both sexual and asexual offspring (Richards, 1970; Muller, 1972; Jenniskens, 1984; Morita et al., 1990). Also, aneuploids from asexual polyploids may show sexuality (Sorensen, 1958). The sexual diploids from France and T. limburgense, sect. Ruderalia, have rDNA (22) and cpDNA (13 and 4, respectively) genotypes based on polymorphic sites that are present in high frequency in the asexual dandelions surveyed (Table 5) and this genetic similarity between asexual and sexual dandelions is consistent with the recent discussions about gene flow between ploidy levels in natural populations (den Nijs and van der Hulst, 1988; den Nijs et al., 1990; Morita et al., 1990).
Based on morphology several North American dandelions are identified as native European agamospecies (Table 2). In contrast to the morphological similarity among the North American weedy dandelions and European agamospecies, only 9 of 222 clones (characterized by rDNA and cpDNA polymorphic sites and lengths and red achenes) among the 427 asexual plants surveyed are present in both North America and Europe (a complete listing of all clones based on these characters is in King, 1989 and is available upon request). Specific combinations of rDNA genotypes and cpDNA haplotypes in the asexual plants are not shared between the North American and European plants collected from natural locations, but all of the individual rDNA genotypes and cpDNA haplotypes in the plants from northern Europe are represented in the weedy asexual North American dandelions. Again, this pattern is most simply explained by multiple origins of asexual polyploids from a group of plants with the represented rDNA polymorphisms and cpDNA haplotypes.
North American dandelions with red achenes do not form a natural group based on either rDNA or cpDNA, so lack of differentiation between North American aggregate species T. officinale and T. laevigatum in rDNA and cpDNA is consistent with Taylor's (1987) observations based on morphology and phenolic compounds and suggests they are not separate evolutionary lineages.
Twenty-one plants surveyed were known to be either tetraploid, pentaploid, or hexaploid. Of these plants, four were collected in the United States, CA31 2n = 48, and AK23-26 2n = 32; the rest are microspecies (see Appendix). Even though most of the tetraploids, pentaploids, and hexaploids have unique rDNA genotypes, they have cpDNA haplotypes 21, 24, and 13 (Table 5), which are among the most frequently represented cpDNA. This shows that diploids, triploids and 4x-6x ploidy levels all share the same maternal lineages.
In other studies, morphology and allozymes have been used to document clonal variation, but they alone cannot unambiguously determine the origins of variation. The unique contribution of this study is the use of rDNA and cpDNA restriction enzyme analysis to identify the origins of genotypic variation in asexual dandelions. Ribosomal DNA, a representative nuclear gene, and cpDNA both offer distinct historical information in addition to the level of clonal variation revealed by the rDNA and cpDNA polymorphisms. From the distribution of characters and associations of rDNA and cpDNA, this study suggests that the polyploids are closely related and unambiguously shows multiple origins of asexual polyploids and agamospecies.
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|Author:||King, Lynn Mertens|
|Date:||Feb 1, 1993|
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