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Population Biology |
Division of Biological Sciences, 105 Tucker Hall, University of Missouri, Columbia, Missouri 65211-0074 USA
Received for publication August 7, 2003. Accepted for publication January 8, 2004.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Asteraceae • exotic species • genetic assimilation • hybridization • Taraxacum
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Arnold, 1997
). The resulting hybrid zones can be stable due to habitat-specific hybrid superiority (bounded hybrid superiority; Moore, 1977
) or a balance between selection against hybrids and parental dispersal (dispersal/selection balance; Key, 1968
; Barton and Hewitt, 1985
). Alternatively, hybrid zones can be transient, and parental populations enter into a race with two possible finish lines: separation or fusion (Howard, 1993
). If hybrids are sterile or of low fitness, the reinforcement of stronger prezygotic reproductive barriers between congeners should be favored by natural selection (Dobzhansky, 1940
). Although still controversial, "reinforcement" of species boundaries can theoretically reduce hybridization and eventually dissolve the hybrid zone (Howard, 1993
; Cain et al., 1999
). Alternatively, production of fertile hybrids represents an initial step in the merging of two populations to form a hybrid swarm. If one or a few hybrid genotypes are competitively superior, this swarm may give rise to a novel "species" (evolutionary novelty; Arnold, 1997
). However, hybrids may backcross with one or both parental species resulting in introgressive hybridization (Anderson, 1949
; Rieseberg and Wendel, 1993
). Numerical superiority (the minority principle), a fitness advantage, or unidirectional reproductive barriers favoring one species over the other can lead to asymmetrical introgression (genetic assimilation) resulting in one species genetically "swamping out" the other (Levin, 1975
; Ellstrand and Elam, 1993
; Rhymer and Simberloff, 1996
). Hybrid zones have traditionally been associated with local disturbance events (Stebbins, 1950
). One such man- made "disturbance" is the introduction of non-indigenous species (Vitousek et al., 1997
). It follows that exotic plant species may offer unique opportunities to examine the beginning stages of hybrid zones, which often otherwise lack an historical context and can easily go unnoticed because they are transient.
If fertile hybrids are formed and backcross with parental species, native populations may be directly threatened by introgression (Ellstrand and Elam, 1993
). Interspecific gene flow can result in the formation of native–exotic hybrid swarms and the loss of "pure" native populations (Rhymer and Simberloff, 1996
). Ultimately if introgression is asymmetrical, favoring the exotic species, genetic assimilation can result in the extinction of the native species (Levin et al., 1996
; Huxel, 1999
; Wolf et al., 2001
). Here I examine several factors influencing interspecific hybridization and hybrid zone formation between native and exotic congeners. First, for heterospecific pollen transfer to occur, native and exotic species must exhibit sympatry and overlap in flowering phenology. Next, one or both of the interacting species must reproduce sexually and receive heterospecific pollination to produce fertile hybrid offspring. Third, pollen limitation of plants receiving mixed or heterospecific pollen loads also may enhance the rate of hybridization by relaxing pre-zygotic reproductive barriers, which often limit overall hybridization rates (e.g., pollen competition; Carney et al., 1994
, 1996
).
The genus Taraxacum, dandelions, is a useful system for the study of hybrid zones because of its past evolutionary history as well as interactions between extant native and exotic species. Although various breeding systems occur in Taraxacum, most species in the genus are obligate agamosperms, producing seed asexually and endosperm autonomously (Richards, 1986
; Asker and Jerling, 1992
). Agamospermous dandelions are typically triploid (3x = 24) but higher ploidy levels are also apomictic. The diploid (2n = 16) Taraxacum species that have been surveyed reproduce sexually, and this reproductive mode is commonly coupled with self-incompatibility (Richards, 1973
, 1986
). True hybrids are produced in both diploid–diploid and triploid–diploid crosses (Richards, 1970
; Morita et al., 1990a
; Tas and van Dijk, 1999
), although crossing apomictic triploid Taraxacum species with sexual diploid species can also produce high percentages of self-fertilized seed via the mentor effect (Morita et al., 1990a
; Tas and van Dijk, 1999
). Richards (1973)
theorized that the genus Taraxacum evolved in the Himalayan region, where primitive sexual species are common. After the last glacial period, northern advanced apomicts (possibly sections Arctica and Borealia) met advancing hybrid swarms that formed from sexual species meeting in the tailings of receding glaciers. Hybridization between apomictics and sexuals led to the vast array of current apomictic lineages. Here I investigate an analogous situation, where anthropogenic introduction, rather than glacial retreat, provides the basis for interspecific contact.
Taraxacum ceratophorum (Asteraceae), the alpine dandelion, is a circumboreal species found throughout the North American Rocky Mountains (Scott, 1995
). Fossils of T. ceratophorum, estimated to be 100 000 yr old, have been discovered in Alaska, indicating a native range in North America (Chaney and Mason, 1936
; Richards, 1973
). The range of this indigenous dandelion overlaps with Taraxacum officinale, an exotic species introduced early during European settlement of North America (Josselyn, 1672
; Solbrig, 1971
; Mack, 2003
). Both species are perennial herbs and from a radial rosette of leaves produce solitary heads composed of yellow ligulate florets. Although inflorescence diameter and height overlap (Cronquist et al., 1994
; Brock, 2003
), T. ceratophorum and T. officinale are distinguishable by the position of bracts in the outer involucre whorl (appressed and reflexed, respectively) and the tips of bracts in the inner involucre whorl (corniculate and not corniculate, respectively; Cronquist et al., 1994
). North American populations of T. officinale are composed of triploid apomictic individuals (King, 1993
; Lyman and Ellstrand, 1998
). Both tetraploid (4x = 32) and diploid chromosome counts have been reported for T. ceratophorum (Scott, 1995
).
Species status in Taraxacum varies along a spectrum from the predominantly European "microspecies" concept to the North American "macrospecies" concept (Hughes and Richards, 1989
). In its extreme form, different genets of asexual dandelions could be described as different microspecies, while the more conservative approach combines variants under broader species boundaries. Due to the lack of microspecies descriptions in North America, I follow the current species designations (Harrington, 1954
; Cronquist et al., 1994
; Scott, 1995
; for sections see Kirschner and Stepanek, 1987
); Taraxacum ceratophorum Ledeb. (section Borealia) and T. officinale Weber (section Ruderalia).
The goal of this study was to examine the initial biotic conditions required for genetic assimilation of native plant populations by exotic congeners. I address the following specific questions: (1) Do T. ceratophorum and T. officinale occur in sympatry in the Colorado Rocky Mountains? (2) To what extent do their flowering phenologies and insect visitors overlap? (3) Do populations of T. ceratophorum reproduce sexually? (4) If so, are they pollen limited? (5) Does heterospecific pollination result in fruit set in T. ceratophorum? (6) If so, what proportion of germinating seeds are hybrids?
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The assumption that diploid populations are sexual was also tested directly in a T. ceratophorum population on Pennsylvania Mountain (see Experimental analysis of the T. ceratophorum breeding system: Test for sexual reproduction).
To conduct chromosome counts, I sampled mature infructescences from four randomly chosen T. ceratophorum plants along a 50-m transect in each population. Seeds from each plant were germinated and the seedlings grown for 3 mo in the greenhouse at University of Missouri-Columbia, at which time the smaller branch roots were pruned to induce new root growth. Five days later, young roots from each plant were removed and placed separately into moist microcentrifuge tubes. After piercing the lid, tubes were placed in an air-sealed iron chamber and subjected to N2O gas (1013 kPa) for 1 h at room temperature (Kato, 1999
). Root tips were fixed in 90% acetic acid (5 min) and then washed in dH2O (5 min). Following Kato (1997)
, root tips were enzymatically macerated for 50 min at 37°C, and meristematic tips were removed. I spread the root cells on microscope slides, which were then place in a humidity chamber for 15 min. Chromosomes were stained with 2.5% acetic orcein and visualized with a light microscope at 1000x magnification.
Experimental analysis of hybridization potential between T. ceratophorum and T. officinale
Study site
Experiments took place on Pennsylvania Mountain (Park County, Colorado, USA, 39°15' N, 106°07' W) in the Mosquito Range of the central Rocky Mountains. At this site, T. ceratophorum grows from the tree line (
3505 m) upwards into the open alpine tundra. Taraxacum officinale is found within the same elevation range, where it often (though not exclusively) grows along road cuts, trails, and in areas of natural disturbance. I studied two spatially distinct subpopulations of each species. For T. officinale, I examined a subpopulation (To1) at the lower edge of the transition zone between timberline (krummholz) and alpine communities and a subpopulation (To2) at the upper edge of the zone. These subpopulations were separated by 780 m. The two subpopulations of T. ceratophorum (Tc1 and Tc2) were both at the upper limit of the krummholz and were separated by 310 m. The upper T. officinale subpopulation was separated by about 250 m from each of the T. ceratophorum subpopulations.
Flowering phenology and insect visitation
In June 1999, I randomly located 10 0.25-m2 quadrats along a 50-m transect within each of the four subpopulations, subject to the constraint that each quadrat contained at least two dandelions with flower buds. The initial flowering date was missed at the lower elevation subpopulation (To1). As a result, censusing started during initial flowering at higher elevations and continued until flowering was complete in all subpopulations. Plots were censused every fourth day, and the number of inflorescences with open florets in each was recorded. Flowering phenology was surveyed again in the summer of 2000, using the same permanently marked quadrats. In 1999, the density of flowering plants per quadrat in Tc1 and Tc2 subpopulations averaged 13.2 ± 1.68 plants/m2 (mean ± 95% confidence limits [CL]) and 10.8 ± 1.2 plants/m2, respectively. For quadrats in To1 and To2 subpopulations, flowering plants averaged 12.4 ± 1.84 plants/m2 and 14.4 ± 3.56 plants/m2, respectively. In 2000, the average density of reproductive plants per quadrat decreased for both T. ceratophorum subpopulations (Tc1, 7.2 ± 2.8 plants/m2; Tc2, 8.8 ± 2.28 plants/m2) and T. officinale subpopulations (To1, 11.6 ± 1.4 plants/m2; To2, 10.8 ± 3.32 plants/ m2). Inflorescence counts were averaged for the 10 plots within each subpopulation and normalized by dividing daily means by the peak flowering density. During peak flowering of 1999 (20 July–1 August), insects were collected daily (0800–1400 hours) from inflorescences of T. ceratophorum and T. officinale to examine the overlap in insect visitor taxa between species.
Experimental analysis of the T. ceratophorum breeding system
Test for sexual reproduction
In each of the two T. ceratophorum subpopulations, 16 spatial blocks were arranged haphazardly within a 200-m2 plot. Individual blocks were established by selecting four dandelions within 2 m of one another. Two dandelions per block were randomly assigned to treatments intended to elucidate the breeding system of T. ceratophorum. To prevent insect visitation, both plants were individually surrounded by fine mesh (1-mm2 bridal veil) that was held away from the inflorescence by a supporting frame (14 cm height x 11.5 cm diameter). I performed a conspecific hand pollination on florets of the first plant, while florets of the remaining plant were not pollinated. For conspecific pollination, I cross-pollinated inflorescences daily by gently brushing four florets from a pollen donor across the stigmatic lobes of recipient florets. Taraxacum florets are protandrous; the style emerges through a ring of five dehiscing anthers picking up pollen, which is then presented to visiting insects. As each floret matures, the stigma lobes reflex, allowing for self-pollination (Richards, 1970
). The absence of fruit production in the unpollinated individual would indicate self-incompatibility. Alternatively, fruit set in both treatments would indicate either self-compatibility or apomixis. To distinguish between these reproductive modes I conducted a genetic analysis of progeny produced from the hand pollination treatment (described below).
Seeds of agamospermous dandelions are (barring mutation and somatic recombination) genetically identical to the maternal parent (Richards, 1996
). In the hand pollination treatment, I performed crosses between and among different genotypes at the polymorphic isozyme locus malate dehydrogenase (MDH) to produce F1 progeny with expected Mendelian segregation ratios. Crosses were performed between the following homozygote and heterozygote genotypes using Fast (F) and Slow (S) allele designations; FF x SS, FS x SS, FS x FS. Sexual reproduction would be confirmed in FF x SS crosses by the production of all FS offspring and in FS x SS crosses by the production of FS and SS offspring in a 1 : 1 ratio. Sexual reproduction (but not necessarily outcrossing) would be confirmed in FS x FS crosses by a 1 : 2 : 1 progeny ratio of FF : FS : SS genotypes.
To genotype parents, I took leaf tissue from each pollen recipient and from randomly sampled pollen donors at least 15 m away. Before anthesis tissue from each parent plant was placed in a plastic bag on ice for transport to the laboratory. Plants were screened at the MDH locus, so that donors could be assigned to specific crosses designed to yield progeny genotype frequencies for tests of expected Mendelian segregation ratios. Leaf tissue from donor and recipient plants was ground in an extraction buffer consisting of 0.1 mol/ L Tris (pH 7.0), 0.132 mol/L ascorbic acid, 0.001 mol/L MgCl2, 0.01 mol/L KCl, 0.001 mol/L EDTA, and 0.1% (v/v) 2-mercaptoethanol (Hughes and Richards, 1985
). Following recipes established by Hughes and Richards (1985)
, Dowex chloride (mass equivalent to sample tissue) was added to each extraction to reduce the protease activity of latex. Using filter paper wicks, proteins were loaded onto horizontal starch (11%) gels. I used a histidine- citrate (pH 5.7) buffer system and then stained gels for resolution at the MDH locus (protocols in Wendel and Weeden, 1989
).
Fruits generated by these and other pollination treatments (described below) were bagged with lightweight cloth to prevent loss of the seed and collected in September when mature. The percentage of fruits containing seeds (percent seed set) was assayed by distinguishing fertilized T. ceratophorum achenes (straw to dark brown colored) from the flat white to yellow empty fruits (Richards, 1970
). To determine whether progeny genotypes conformed to predicted Mendelian ratios at the polymorphic MDH locus, seeds from five randomly chosen families in each subpopulation were planted in trays of peat growing medium (Pro-Mix BX Professional General Purpose Growing Medium; Premier Horticulture, Red Hill, Pennsylvania, USA) in the greenhouse at the University of Missouri-Columbia. Leaf tissue from at least 16 individuals in each progeny array (mean N = 19) was screened at the MDH locus.
Test for pollen limitation on seed set rates
To test for pollen limitation, inflorescences of two additional randomly selected T. ceratophorum plants in each of the 16 blocks per subpopulation were left open to natural pollinators. One individual was assigned at random to receive additional pollen, while the other plant was not manipulated (control). Again, four florets from a randomly selected T. ceratophorum donor were brushed across the stigmas of each plant daily in the pollen addition treatment. Seed set in the control treatment, when compared with that of plants receiving conspecific hand pollination, also provided a measure of hand pollination efficiency.
Test for interspecific compatibility, seed viability, and parentage
In 2001, I crossed T. officinale pollen donors onto recipient T. ceratophorum plants to test for interspecific cross-compatibility. In the T. ceratophorum Tc1 population I caged 18 randomly selected plants to receive heterospecific pollination (cages described in: Experimental analysis of the T. ceratophorum breeding system: Test for sexual reproduction). A day prior to use as pollen donors, T. officinale inflorescences from the To1 population were individually placed in florist "aquapics" and then housed at the field site in a mesh-covered insect exclusion box. Due to low fertility in the 1999 conspecific hand pollinations (Results: Test for pollen limitation on seed set rates), I performed interspecific crosses in 2001 by daily brushing the receptive stigmas of each T. ceratophorum inflorescence with a fresh randomly selected T. officinale inflorescence. Each donor inflorescence was used only once to prevent pollen contamination between crosses. Mature seeds were collected in August and percent seed set determined. To estimate seed viability and provide cotyledon tissue for paternity analysis, I planted the seeds in the greenhouse at the University of Missouri-Columbia in trays of Pro-Mix peat medium and monitored germination over 30 d. Due to variation in fruit set and damage by Hemipteran seed predators, only a subset of seeds produced by each of the 18 crosses was included in the germination trial (mean N = 10, range 4–13).
Seedlings were screened at the species-specific microsatellite locus, MSTA 64 (described below), to determine if they were true hybrids or alternatively, if they matched T. ceratophorum genotypes. Individuals with T. ceratophorum genotypes presumably represent selfed seedlings from a breakdown in self- incompatibility (the mentor effect) and not outcrossed individuals since caging effectively prevents seed set (Results: Test for sexual reproduction). For each seedling, cotyledon tissue was removed and DNA was extracted using the method of Wang et al. (1993)
. I followed protocols for polymerase chain reaction (PCR) and product resolution on acrylamide gels developed while identifying the species-specific marker (below); however I increased the amount of template DNA to 2 µL in each PCR reaction.
MSTA 64 was identified as a species-specific microsatellite marker by sampling T. ceratophorum and T. officinale leaf tissue from three populations in Park County, Colorado, USA (Weston Pass, Pennsylvania Mountain, and Bross Mountain), and two populations in Summit County, Colorado, USA (Hoosier Pass and Boreas Pass). Within each population I found patches composed entirely of T. ceratophorum or T. officinale. From each of the species- specific patches, I randomly sampled leaf tissue of five individuals along a 50-m transect. Tissue was placed on ice in damp plastic bags and was later flash frozen in liquid nitrogen.
I extracted DNA from each sample using a protocol developed by Paterson et al. (1993)
and modified for use in a microcentrifuge tube. Sample tissue (0.04 g) was placed in a 1.5-mL microcentrifuge tube and ground in liquid nitrogen. Protocols described by Paterson et al. (1993)
were followed thereafter but 700 µL of lysis buffer, 700 µL of chloroform-isoamyl alcohol (24 : 1), and 1 mL of 70% ethanol were substituted for original volumes in the protocol. The DNA pellet was resuspended in 50 µL of TE buffer (pH 8.0) for storage and diluted 1 : 8 with dH2O for use in PCR reactions. Primers for the locus MSTA 64, developed by Falque et al. (1998)
, were screened for species-specific products. The PCR reactions contained 1x buffer, 2.5 µmol/ L MgCl2, 200 nmol/L of each primer (A/B), 200 µmol/L of each dNTP, 0.625 units of Taq, and 1 µL of template DNA. Reactions were run on a Hybaid thermocycler (Thermo Electron Corporation) with the following program: 1 cycle of 94°C (5 min), followed by 40 cycles of 94°C (30 s), 52°C (45 s), and 72°C (1 min), and a final elongation step at 72°C (5 min). The PCR products were separated on 8% polyacrylamide gels using 1x TBE buffer and then resolved with ethidium bromide stain. Using this microsatellite marker, T. ceratophorum and T. officinale samples from all five populations could be taxonomically resolved based on species-specific banding patterns.
Data analysis
I used Hurlbert's Index to quantify the degree of overlap in flowering phenology of the four subpopulations (Ludwig and Reynolds, 1988
). Hurlbert's index is:
 | (1) |
0.25) was subsequently dropped from the model. Data were angular transformed prior to analysis to fit assumptions of ANOVA. As plants that were caged from insects and left unpollinated set no seed, this treatment was not included in the ANOVA. Planned comparisons were performed to test for significant differences between treatments. Categorical analysis of variance (Catmod procedure, SAS version 6.12) was used to test if maternal plants of T. ceratophorum varied in their likelihood of producing hybrid or selfed seed (the binomial response variable) when pollinated by T. officinale donors. |
RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Test for pollen limitation on seed set rates
Pollen addition significantly affected seed set in T. ceratophorum (F2, 72 = 12.50, P 
0.0001) (Fig. 3). Variation in seed set among subpopulations and in the effect of pollen addition among subpopulations (site by treatment interaction) were not significant (P = 0.22). Planned comparisons revealed that plants receiving only conspecific hand pollination were not as fertile (46.2 ± 10.6%) as plants open to insect visitation (70.1 ± 8.4%) (control) (t = 3.12, P = 0.0026). The reduced seed set of hand-pollinated flowers is likely due to the low number of donor florets (four) used. Pollen addition increased seed production by 17.8% compared to that of open controls (82.6 ± 6.8% vs. 70.1 ± 8.4%, t = 1.97, P = 0.0527), indicating pollen limitation of seed set (Fig. 3).
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2 = 18.31, df = 17, P = 0.37). |
DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Ecological conditions for the initial stages of genetic assimilation are met in populations of Taraxacum ceratophorum and T. officinale. Both spatial and phenological overlaps in flowering occur in this system. Taraxacum officinale co-occurs with T. ceratophorum at all sites surveyed in this study. Flowering phenology during 2 yr at Pennsylvania Mountain also showed considerable interspecific overlap. These findings indicate that spatial and temporal barriers will not limit heterospecific pollen transfer between T. officinale and T. ceratophorum. Furthermore, insect visitors to inflorescences of T. ceratophorum and T. officinale overlapped extensively and observations in mixed arrays of T. ceratophorum and T. officinale inflorescences indicated that insects (primarily dipterans) indiscriminately visit both Taraxacum species (Brock, 2003
). Taraxacum ceratophorum and T. officinale produce morphologically similar florets (e.g., color and stylar pollen presentation) and inflorescences (e.g., height and diameter) and conform to the generalist pollination syndrome exhibited in the Asteraceae (Torres and Galetto, 2002
) and genus Taraxacum (Mosquin, 1971
). These factors favor the incidence of heterospecific pollen transfer.
Three lines of evidence demonstrate that T. ceratophorum reproduces sexually. Allele segregation at the MDH locus in progeny of known crosses conformed to predicted Mendelian ratios under outcrossing. The absence of seed production in the pollinator exclusion treatment also supports a sexual breeding system with self-incompatibility. Third, all populations surveyed in this study contained only diploid individuals (2n = 16). Although sexual reproduction has occasionally been demonstrated in higher ploidy levels (Kirschner et al., 1994
; Lyman and Ellstrand, 1998
), all diploid Taraxacum species that have been tested are reported as sexual (Richards, 1973
). Sexual dandelions are thought to be infrequent outside of Europe and Asia (Richards, 1973
, 1986
). However, other sexual dandelion species have been reported in North America (e.g., T. californicum and T. pumilum) (Richards, 1986
; Lyman and Ellstrand, 1998
).
Heterospecific pollination of T. ceratophorum with pollen from T. officinale resulted in moderate levels (37.3%) of seed production in 2001. Other reports of diploid–triploid interspecific crosses, in which entire capitula were used as pollen donors, yielded similar levels of seed set (mean 18–28%) (Richards, 1970
; Morita et al., 1990a
; Tas and van Dijk, 1999
). The moderate to low seed production from interspecific diploid– triploid crosses is most likely due to inviability or reduced performance of aneuploid pollen at the prezygotic and/or postzygotic level (Richards, 1973
, 1986
; Tas and van Dijk, 1999
).
Under greenhouse conditions, seed germination was high (68.1%) for seeds resulting from interspecific crosses. However, only 33% of seedlings were of hybrid origin, with the remaining seedlings derived from self-fertilization by the maternal T. ceratophorum plant. It should be noted that this is not a direct measurement of the interspecific hybridization rate, since seeds failing to germinate may be a nonrandom sample of the total. Maternal families did not vary significantly in the production of hybrid seed, suggesting that all of the maternal genotypes sampled are equally at risk of interspecific mating. Other studies on Taraxacum have also demonstrated high seed germination rates following hybridization (Richards, 1970
; Morita et al., 1990a
; Tas and van Dijk, 1999
) and a mentor effect in triploid–diploid crosses (Morita et al., 1990a
; Tas and van Dijk, 1999
). However the proportion of true hybrids in the F1 generation is much higher in this study than in studies of other sexual taxa (12.5% and 11%, Morita et al., 1990b
; Tas and Van Dijk, 1999, respectively). It is possible that my hand pollination technique transferred more heterospecific pollen to T. ceratophorum, resulting in increases in both seed set and the proportion of hybrids in the F1 generation. Alternatively, euploid T. officinale pollen grains may have higher tube growth rates in T. ceratophorum styles, competing against conspecific pollen more effectively than in other diploid–triploid species crosses in Taraxacum.
Together these results indicate that sexual populations of the native T. ceratophorum may face the threat of genetic assimilation by the non-indigenous T. officinale. Several factors make this scenario possible. First, the breeding systems in this case allow for extreme asymmetrical introgression. Hybrids will only be formed in sexual T. ceratophorum and possible sexual hybrids, resulting in unidirectional interspecific gene flow. Second, T. ceratophorum exhibited pollen limitation of seed set in 1999, although the reduction in fertility is likely to vary among years. Because pollen competition is often cited as a barrier to hybridization (Arnold et al., 1993
; Carney and Arnold, 1997
; Wang and Cruzan, 1998
), pollen-limited populations should experience reduced native–exotic competition for ovules favoring paternity of heterospecific donors. Third, although the mean hybridization rate with hand pollination was relatively low, breeding systems in hybrids can, depending upon their ploidy level, range from sexual to the more frequent apomictic (Richards, 1970
; Morita et al., 1990a
, b
). Any apomictic hybrid individuals that become established could represent sources for large numbers of genetically identical hybrid offspring, inflating the future contribution of current hybridization to the gene pool.
On the other hand, the likelihood of genetic assimilation depends not only on early stages in the hybrid life cycle, but also on the establishment of fertile hybrid plants. Crosses between other diploid–triploid Taraxacum species have shown that, relative to sexual diploids, both sexual and apomictic F1 hybrids exhibit reductions in seed set (Tas and van Dijk, 1999
; van Dijk et al., 1999
). Yet despite reduced fertility, greenhouse-raised hybrids from sexual–apomictic crosses are commonly reported as vigorous (Richards, 1970
; Morita et al., 1990b
) and a recent study found that 82% (N = 225) of plants with morphological characteristics of T. officinale sampled in Japan were hybrids between T. officinale and sexual Japanese dandelions (primarily T. platycarpum) (Shibaike et al., 2002
and references therein). Although these other studies suggest that Taraxacum hybrids are vigorous and fertile, these later stages in the life cycle of interspecific hybrids between T. ceratophorum and T. officinale must be investigated.
The net production of hybrid seed by T. ceratophorum would be higher if not for the mentor effect, which mitigates hybridization through self-fertilization. Although the mentor effect should theoretically reduce the rate of extinction due to hybridization (Wolf et al., 2001
), self-fertilization in an otherwise obligately outcrossing species, like T. ceratophorum, results in inbreeding depression for the maternal plant (Daehler, 1999
; Stephenson et al., 2000
). As a result, T. officinale may not only be directly altering T. ceratophorum offspring through hybridization, but might also indirectly alter the genetic and demographic viability of native congeners by promoting inbreeding depression.
In simulating extinction due to hybridization, Wolf et al. (2001)
and Huxel (1999)
indicate that factors contributing to the asymmetry of the species relationship can lead to rapid loss of the native species. In Taraxacum, asymmetrical hybridization, reduced prezygotic reproductive barriers, and potentially vigorous fertile hybrids may encourage the loss of the native gene pool. Similar genetic threats may face Taraxacum californicum, a federally endangered native species. Despite its uncommon aneuploid number of chromosomes (2n = 31), this species also appears to be sexual and in frequent sympatry with T. officinale (Lyman and Ellstrand, 1998
). Threats of hybridization with T. officinale are compounded by small population sizes of endemic species, which also contributes to an asymmetrical advantage for the exotic T. officinale. Taken together, these results illustrate that when exotics expand their range, native congeners face not only threats to demographic parameters but genetic threats as well.
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FOOTNOTES |
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1 The author thanks C. Galen, B. Rothermel, A. Dona, L. Dudley, D. Figueroa-Castro, and two anonymous reviewers for comments on the manuscript; E. Baack, D. Giblin, M. Doyle, and A. Carroll for assistance with field work; the University of Colorado at Colorado Springs for providing access to the field sites on Pennsylvania Mountain; and T. Holtsford, S. Mathews, J. Birchler, A. Kato, C. Dillman, and J. Johnson for advice and assistance in the laboratory. This research was supported by the University of Missouri RIF Fellowship and TWA Scholarship to M. Brock and NSF grant DEB-0087412 to C. Galen.
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Carney S. E. M. L. Arnold 1997 Differences in pollen-tube growth rate and reproductive isolation between Louisiana irises. Journal of Heredity 88: 545-549
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