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Clonal population structure and genetic variation in sand-shinnery oak,Quercus havardii (Fagaceae)¹

^a Ecology Program, Department of Biological Sciences, Texas Tech University, Lubbock, Texas 79409–3131

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
We investigated clonal population structure and genetic variation in Quercus havardii (sand-shinnery oak), a deciduous rhizomatous shrub that dominates vegetation by forming uninterrupted expanses of ground cover over sandy deposits on the plains of western Texas, western Oklahoma, and eastern New Mexico. Isozyme electrophoresis (15 loci coding 11 enzymes) was used to recognize and map clones arrayed in a 2000-m transect (50-m sample intervals) and a 200 x 190 m grid (10-m sample intervals). Ninety-four clones were discovered, 38 in the transect and 56 in the grid, resulting in an estimated density of ~15 clones per hectare. Clones varied greatly in size (~100–7000 m), shape, and degree of fragmentation. The larger clones possessed massive interiors free of intergrowth by other clones, while the smaller clones varied in degree of intergrowth. The population maintained substantial levels of genetic variation (P = 60%, A = 2.5, H_exp = 0.289) comparable to values obtained for other Quercus spp. and for other long-lived perennials. The population was outcrossing as evidenced by conformance of most loci to Hardy-Weinberg expected genotype proportions, although exceptions indicated a limited degree of population substructuring. These data indicate that despite apparent reproduction primarily through vegetative means, Q. havardii possesses conventional attributes of a sexual population.

Key Words: allozyme • clone • Fagaceae • genetic variation • isozyme • population structure • Quercus

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Among the most unusual of biotic communities in North America is the sand-shinnery oak community occurring on sandy deposits in western Texas, eastern New Mexico, and southwestern Oklahoma (Fig. 1). The overwhelming dominant in this community is the plains-endemic Quercus havardii Rydb. (sand-shinnery oak), a clonal deciduous shrub of low stature, with sparsely branched aerial shoots rarely exceeding 1 m in height. It forms large patches through horizontal growth effected by subterranean rhizomes, which may achieve a diameter of >9 cm (Muller, 1951; Wiedman, 1960; Scifres, 1972; Pettit, 1979; Dhillion et al., 1994). In the eastern portion of the species' range these patches remain more or less discrete, but in the more western sand-shinnery oak community, the patches coalesce to form a continuous ground cover with stem densities ranging from 30 to 70 stems/m (Dhillion et al., 1994; Zhang, 1996). The resulting aspect of the community is a vast homogeneous "sea" of uniformly spaced Q. havardii stems similar in height and other attributes. This vegetation type is estimated to have originally covered an area of 2.3 million hectares, but present abundance has been substantially reduced through eradication, as Q. havardii is considered a pest by ranchers (Dhillion et al., 1994).

View larger version (41K): [in this window] [in a new window]   Fig. 1. The distribution of sand-shinnery oak and the location of our field site in Yoakum County, Texas. The sand-shinnery oak community per se is predominantly in the western continuous portions of the species' range.

	MATERIALS AND METHODS

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Study site and sampling strategy
This study was conducted at a permanent research site near Plains in Yoakum County, Texas (Fig. 1; Dhillion et al., 1994). The habitat consists of sand dunes dominated by Quercus havardii, which comprises >90% of the ground cover, interrupted in spots by disturbed sites and other plant species. Associated plant species included Artemisia filifolia, Yucca campestris, Schizachyrium scoparium, Andropogon hallii, Aristida purpurea, Eriogonum annuum, and Euphorbia fendleri (Dhillion et al., 1994; names of taxa based on Correll and Johnston, 1979).

As there was previously little more than anecdotal information on clone size for Quercus havardii (Muller, 1951), the most appropriate distance between sampling points was undetermined as this study commenced. To establish a first approximation of clone size, 40 samples were taken at 50-m intervals along a transect and electrophoresed (see below) to determine whether clones extended >50 m. As most samples in this transect possessed distinct genotypes and were therefore different genets (see Results), a finer sampling interval of 10 m was chosen. A grid measuring 200 x 190 m was established at the study site from which samples were obtained at 10-m intervals.

Electrophoresis of enzymes
Leaves were obtained for electrophoretic analysis from April through July 1993 and placed in sealable bags in an insulated container, and kept refrigerated until processing. Leaf tissue was homogenized within 3 d after harvest (longer delays resulted in significant loss of enzyme activity) in pH 7.5 "microbuffer" of Werth (1985) containing 5% polyvinylpyrrolidone (molecular mass 40 000 units) and 1% 2-mercaptoethanol. Homogenates were either immediately loaded into the starch gels (12% Sigma starch) or stored frozen at -85C for later electrophoresis. Electrophoresis and staining of enzymes followed standard procedures (Soltis et al., 1983; Werth, 1985; Wendel and Weeden, 1989), but employed the "zymecicle" methodology of Werth (1990). Leucine aminopeptidase (LAP) and esterase (EST) were resolved on the lithium hydroxide system (Werth, 1985); phosphoglucose isomerase (PGI), alcohol dehydrogenase (ADH), and triosephosphate isomerase (TPI) on buffer system 6 of Soltis et al. (1983); phosphoglucomutase (PGM) and 6-phosphogluconic dehydrogenase (6PGD) on the tris-citrate pH 8.0 buffer system of Selander et al. (1971); and aldolase (ALD), isocitrate dehydrogenase (IDH), malate dehydrogenase (MDH), 6PGD, and shikimate dehydrogenase (SKDH) on the morpholine-citrate buffer system (Werth, 1991).

Band interpretation and data analysis
Isozyme band patterns were interpreted using standard principles (Wendel and Weeden, 1989; Murphy et al., 1990). Alleles were designated by numbers representing the migration of the allozymes they encoded, with the lowest number assigned to the most anodal allozyme.

Genetic individuals (genets) were discriminated on the basis of their multilocus isozyme genotypes, and confidence levels for clone assignment estimated using the method of Parks and Werth (1993). Quantitative treatment of the data was carried out using BIOSYS-1 (Swofford and Selander, 1981), Statview Student for the Macintosh (1991), and NTSYS (Rohlf, 1988).

	RESULTS

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General
Fifteen loci coding 11 enzymes were consistently scorable and could be used for discrimination of genets. Of these 15 loci, 86.7% (13 loci-- Adh, Est, Idh, Lap, Mdh-1, Mdh-2, Pgi-2, Pgm-2, 6Pgd-1, 6Pgd-2, Skdh, Tpi-1, and Tpi-2) were polymorphic in the study area. The two nonvariable loci were Ald and Pgi-1. Three of the loci, Idh, Mdh-2, and 6Pgd-2, were not variable within the grid subpopulation, and one, Tpi-2, was not variable within the transect subpopulation.

In the initial transect, 38 of the 40 ramets sampled at 50-m intervals exhibited distinct genotypes and could thus be inferred to be different genets (Appendix). Two pairs of adjacent points, numbers 2/3 and 32/33 had identical genotypes, indicating the presence of single clones spanning greater than 50 m. In the two-dimensional grid, 56 distinct genotypes were observed among the 380 ramets sampled (Appendix; Fig. 2). The genotypes were numbered as encountered. In some cases the same genotype was inadvertently given two different numbers, in which case the higher number was omitted, resulting in ordinal values up to 62. Because the different sampling intervals and vastly different linear extent (2000 m vs. 200 m) of the grid and transect might influence their genetic makeup if genotypes were unevenly distributed across the population, most population genetic parameters were computed separately for these two subsamples. Allele frequencies for all loci were calculated separately for the grid and transect and then averaged to obtain population means (Table 1). For the grid subpopulation, in which closely spaced ramets resulted in repeated sampling of genets, allele frequencies were estimated both by tallying all genets (unadjusted) and by using the "round-robin" method, a subsampling routine that can avoid overestimation of frequencies for rare alleles, as described in Parks and Werth (1993). Both techniques resulted in nearly identical frequencies (Table 1), indicating that sufficient genetic variation was present to provide robust genet discrimination.

View larger version (201K): [in this window] [in a new window]   Fig. 2. Map depicting the identity of genotypes in our sampling grid (200 x 190 m). Each 10 x 10 m square was represented by a sample point in its center. Each pattern represents a different multilocus genotype, i.e., putative genet; numbers correspond to genet numbers in Appendix. Blank squares are regions devoid of Q. havardii ramets.

Clone size
Features of size and shape of Q. havardii clones in the grid were evaluated by construction of a map of genets (Fig. 2) and a histogram depicting the distribution in clone size (Fig. 3). Among the 56 clones of the grid, the majority were small (37 with only 1–4 sample points), and a few were large (five with 17 or more sample points). To rule out edge effects as a possible cause of this distribution, the clone size histogram was also plotted using only those clones that did not touch the edge of the grid, resulting in a similar distribution of clone sizes (Fig. 3). The 12 largest clones occupied >70% of the grid area, 40% being attributable to the three largest clones, clones 22, 26, and 32. The largest clone, number 22, was sampled at 70 points and thus occupied an estimated area of 7000 m (at 100 m per sample point).

View larger version (22K): [in this window] [in a new window]   Fig. 3. Clone size (number of ramets sampled) frequency distribution. The barred columns include all clones, whereas the open columns include only clones that do not come into contact with the edge of the sampling grid.

In evaluating the likelihood that each of these cases of separated ramet clusters represents clone fragmentation, it is necessary to consider that P_SE is the probability for second encounter of an independently formed ramet with one particular genotype. The collective probability that any one or more of the detected genotypes would be reencountered is much greater than P_SE because the number of "trials" (pairs of genets) is much greater. The probability of not reencountering a particular genotype is (1 - P_SE). The chance that none would be reencountered is the product of (1 - P_SE) for all genotypes in the grid subpopulation, which was computed as 0.329. Thus, although the chance of reencountering a particular genotype is low, the chance of reencountering one or more of the 56 genotypes is high, i.e., 0.671. Therefore, it is probable that at least one of the putatively fragmented clones may actually comprise a pair of different genets with identical genotypes, although it remains highly improbable that more than a few of the 15 cases of putative fragmentation are instead cases of distinct genet formation. It cannot be ascertained with certainty which groups of separated putative fragments with identical genotype actually comprise distinct genets. However, widely separated fragments, such as genotype 8, are especially suspect.

The number of fragments was unrelated to clone size (Fig. 4; Spearman rank correlation N = 24, r_s = 0.094, p = 0.66). This result apparently deviated from the random expectation, which is a positive relationship, since larger clones should have a higher probability of becoming fragmented.

View larger version (13K): [in this window] [in a new window]   Fig. 4. Graph of the number of clone fragments as a function of clone size (number of ramets sampled) for all clones that did not come into contact with the edge of the sampling grid.

Levels and patterns of genetic variability
Genetic variability was quantified for the grid, transect, and combined samples by computing three indices: mean expected heterozygosity (H_exp), proportion of loci polymorphic (P), and mean number of alleles per locus (A) (Table 2). Values of all three indices (H_exp = 0.289, P= 60%, and A = 2.50 for the combined sample) were higher than those reported for most other oaks that have been electrophoretically surveyed (Guttman and Weigt, 1989; Schnabel and Hamrick, 1990; Hamrick, Godt, and Sherman-Broyles, 1992; Berg and Hamrick, 1994) and were also high as compared to the mean values for flowering plants in general (H_exp = 0.113; P= 34.2%; A = 1.53) (Hamrick and Godt, 1989). These values were also high when compared to subgroups defined by life-history characters shared with Q. havardii, e.g., other dicots (H_exp = 0.096; P= 29.0%; A = 1.44), long-lived woody perennials (H_exp = 0.149; P = 50.0%; A = 1.79), temperate plants (H_exp = 0.109; P= 32.6%; A = 1.51), outcrossing wind-pollinated plants (H_exp = 0.148; P= 49.7%; A = 1.79), and other clonal plants (H_exp = 0.103; P= 29.4%; A = 1.47) (Hamrick and Godt, 1989).

	DISCUSSION

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Clonal populations often comprise an array of discrete patches that, depending on the growth strategy, may correspond to single genets (e.g., Daehler and Strong, 1994; Montalvo et al., 1997) or may each be composed of several genets (e.g., Parks and Werth, 1993; Berg and Hamrick, 1994). However, the Quercus havardii population addressed in this study comprises a single enormous patch, spread continuously over a large expanse of homogeneously suitable habitat. The use of isozymic markers has allowed for the first time a portion of this expanse to be viewed as genetically distinct individuals comprising a sexually interbreeding population. Despite rhizome growth that results in order-of-magnitude size variation among genets coupled with rarity of sexual recruitment (Muller, 1951; Wiedman, 1960; Pettit, 1979), this population appears to share features with populations of organisms with more determinate growth, i.e., large population size, an outcrossing breeding system in which mating approaches panmixia, and maintenance of a substantial level of genetic variation.

In this respect, Q. havardii parallels other species for which vegetative propagation does not substitute for sexual reproduction, but rather effects horizontal spread of sexually reproduced individuals. Such populations have been shown capable of maintaining significant genetic variation (Thomas and Dale, 1975; Ellstrand and Roose, 1987; Wolf, Haufler, and Sheffield, 1988; Wolf, Sheffield, and Haufler, 1991; Aspinwall and Christian, 1992; Berg and Hamrick, 1994; Lokker et al., 1994; Sipes and Wolf, 1997; Montalvo et al., 1997) despite possibly lowered effective population sizes in clonally reproducing species relative to species that reproduce only sexually. It is unlikely that population size constrains maintenance of genetic diversity in this species. Assuming that the density of ~15 genets per hectare in the grid is representative for populations of this species, the number of individuals across the species range (2.3 million hectares), much of which was contiguous up until the early 20th century, can be estimated as exceeding 30 million. Furthermore, the apparently low degree of genetic structure indicates that neighborhood sizes are very large, as indicated for other Quercus species (Berg and Hamrick, 1994; Montalvo et al., 1997; but see Sork, Huang, and Wiener, 1993).

Attributes of clonal architecture are highly variable among and sometimes within plant species (Ellstrand and Roose, 1987). Clone size may range from <1 m for some herbaceous species to >43 ha for a clone of Populus tremuloides Michaux (Kemperman and Barnes, 1976). Prior to the present study, the size range of Quercus havardii clones was unknown, although estimates of up to ~15 m had been made based on the sizes of discrete patches that occur in the eastern portion of the species range and of phenologically differentiated patches within the expansive communities (Muller, 1951). Here we have found that these previous estimates were conservative, as indicated by large clones such as number 22, which exceeded 150 m in maximum breadth and occupied ~7000 m.

Morphologies and growth strategies of clonal organisms vary across a broad spectrum from regularly shaped radiating circles of densely clumped ramets with minimal intergrowth (phalanx morphology) to irregularly shaped, meandering, and/or ramifying clones with more widespread ramets and a tendency for intergrowth and fragmentation (guerilla morphology) (Lovett-Doust, 1981; Silander, 1985). Quercus havardii clones, even the smaller ones, comprise numerous closely spaced ramets that occupy significant areas free of ramets from other clones (or other species) and tend not to be fragmented, thus possessing a fundamentally phalanx morphology. Phalanx morphology of Q. havardii is further suggested by anecdotal observation of its subterranean structure, usually revealed by exposure from wind erosion, rarely from purposeful excavations (J. C. Zak, Texas Tech University, personal communication). Such observations suggest a hierarchical system comprising groups of branches produced at regular intervals from a thick subterranean rhizome. However, to varying degrees individual clones also possess attributes associated with guerilla morphology. A meandering and branching form characterizes at least a portion of many of the clones, including the arms radiating from the larger ones, and some clones exhibit fragmentation. It remains uncertain, and a possible focus of future investigation, as to what kinds of spatial interactions occur between clones at a finer scale than addressed herein.

While the phenomenon of asexual proliferation through rhizome growth is readily observed in Quercus havardii, the nature of sexual reproduction and recruitment in this species is very poorly understood. Although large numbers of acorns are produced in ~3 out of every 10 yr (Muller, 1951; Pettit, 1979), Q. havardii seedlings rarely become established in the wild (Muller, 1951; Wiedman, 1960; Pettit, 1979), as virtually every available safe sight is occupied by existing genets, severely constraining the opportunity for seedling establishment. Moreover, disturbance by animals has been shown to facilitate establishment of herbaceous plant seedlings by opening sites in a deep layer of leaf-litter (Dhillion et al., 1994; Jeffery, 1998; Willig and McGinley, 1998). Perhaps disturbance may play a parallel role in recruitment of Q. havardii seedlings, but this remains to be observed directly.

Processes and histories of recruitment of long-lived perennials such as forest trees and other woody plants are difficult to evaluate because of the large time scales involved. Vegetative proliferation compounds the problem by blurring the distinction between individuals. The recognition of Q. havardii genets through isozyme fingerprints achieved in the present study narrows the universe of possibilities and clarifies the nature of questions that can be addressed in future studies. The large density of distinct genets (15 genets/ha) comprising an interbreeding sexual population with conventional attributes implicates an important and continuing, if episodic, role for sexual recruitment. The establishment of the population must have involved a complex dynamic that occurred during antiquity, the timing and progression of which can only be speculated, as the ages of the clones and the biotic community they so thoroughly dominate are unknown. The highly variable sizes and shapes of the Q. havardii clones, as they collectively occupy nearly the totality of a vast surface, must have largely been influenced by their competitive interactions as they came to abut. However, it remains unknown whether the spatial features of the genets revealed are long-enduring, having reached a stasis, are continually changing but in dynamic equilibrium, or are subject to drastic chaotic changes following episodic occurrence of environmental extremes.

	FOOTNOTES

 
¹ The authors thank Kathy Stamback, Jeff Jump, and especially Thao Le for assistance with isozyme electrophoresis; Arndt Laemmerzahl, and Michele Holland for assistance with field work; John Zak and Mike Willig for input into the study design; and Mr. Johnnie Fitzgerald for permission to conduct the study on his land. This study was conducted in partial completion of a Master's degree from Texas Tech University (SGM). Financial support was provided by the Office of Research Services at Texas Tech University in the form of a summer grant-in-aid to SGM and CRW.

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This Article Abstract Full Text (PDF) Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via ISI Web of Science (20) Citing Articles via Google Scholar Google Scholar Articles by Mayes, S. G. Articles by Werth, C. R. Search for Related Content PubMed Articles by Mayes, S. G. Articles by Werth, C. R. Agricola Articles by Mayes, S. G. Articles by Werth, C. R.