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2Utah State University, Biology Department, 5305 Old Main Hill, Logan, Utah 84322-5305 USA; 3U.S. Fish and Wildlife Service, Nevada State Office, 4600 Kietzke Lane, C-125, Reno, Nevada 89502 USA; and 5USDA-ARS Bee Biology and Systematics Laboratory, Utah State University, 5310 Old Main Hill, Logan, Utah 84322-5310 USA
Received for publication March 2, 2000. Accepted for publication June 15, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: allozyme • endemic • gene flow • isozyme • rare
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Schemske et al., 1994
), successful management of many rare plant populations is greatly improved by genetic data (Ellstrand and Elam, 1993
; Hamrick and Godt, 1996
). A rare plant conservation plan based only on genetic or demographic generalizations is inferior to one informed by a genetic profile. For example, it is generally thought that gene flow into disjunct populations is much lower than that into central populations and that this difference leads to lower genetic variability in disjuncts. Current population size is also taken to be positively related to genetic variability. It follows, therefore, that the conservation value of large, central populations exceeds that of small, disjunct ones. However, policies based strictly on such generalizations, without the benefit of genetic data, would be wrong for species like the swamp pink, Helonias bullata, in which some disjunct populations are more genetically diverse than central populations and in which population size does not correlate positively with genetic variability (Hamrick and Godt, 1996
). As seen in that example and so many others, there are too many exceptions in nature for us to rely entirely on generalizations when making conservation plans.
Here we examine genetic structure of the single population of a narrow endemic plant, Eriogonum ovalifolium Nutt. var. williamsiae Reveal (Steamboat buckwheat), listed as endangered by the U.S. Fish and Wildlife Service on 8 July 1986 (51 Federal Register 24669). The sole population occurs on federal and private land in the Steamboat Hills, in southern Washoe County, Nevada, where it is roughly divided into three subpopulations on 
100–150 ha of sinter, a substrate derived from hot spring deposits. This perennial taxon was described in 1981 as being restricted to the Steamboat Springs area, with the note that it had been collected routinely since 1884 (Reveal, 1981
), apparently only in that area.
Genetic information for this taxon is especially desirable because of the mixed land ownership and the likelihood that habitat loss and plant mortality will continue. For example, some of the population occurs on the right-of-way of a U.S. interstate highway that is due for expansion. The largest part of the population is on private land leased for geothermal resource development. Past power plant construction has already resulted in the attempted transplantation of 17 000 ramets (at a survival rate of 25%; T. Knight, personal communication, The Nature Conservancy, Las Vegas). Construction, and the attendant need for mitigation, is expected to continue (U.S. Fish and Wildlife Service, 1995
).
Such anthropogenic threats make imperative a genetic evaluation of this rare taxon. Knowledge of the genetic diversity patterns and structure of the population, including information on clone size and frequency, will better enable us to make power plant siting recommendations and offer guidance about preferred transplantation sites. Clonal spread is suggested by the extensive systems of underground rhizomes seen in individual plants and by the observation that small rosettes are usually found close to large ones (U.S. Fish and Wildlife Service, 1995
). Large clone size would increase the likelihood of genetic drift and inbreeding in a self-compatible taxon by decreasing effective population size (Ellstrand and Elam, 1993
). Although it is possible to confirm that this taxon reproduces vegetatively by excavating plants, and to use resultant estimates of genet size to adjust population size, interramet connections often deteriorate and are difficult to find. It is less destructive and more accurate to use genetic techniques to estimate clone size.
Finally, genetic evidence for the distinctness of this rare taxon should be examined. Eriogonum ovalifolium has seven varieties within Nevada: caelestinum Reveal, depressum Blank, eximium (Tidestrom) J. T. Howell, nivale (Canby in Cov.) M. E. Jones, ovalifolium, purpureum (Nelson) Durand, and williamsiae (Reveal, 1978,
1981,
1985
), and the morphological distinctions among them are not always clear. Evaluation of the systematic relationships of var. williamsiae with respect to the rest of the varieties is needed.
We used analysis of allozyme variation to address the following questions: (1) How genetically variable is var. williamsiae? (2) Are genotype frequencies consistent with random mating or inbreeding? (3) Is the single population of var. williamsiae structured genetically? (4) Is the taxon clonal and, if so, what is the size of clones in the population? (5) How genetically distinct is E. o. var. williamsiae from other varieties of E. ovalifolium?
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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10-m intervals from a single 400-m transect in subpopulation 3.
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25–1800 cm).
We sampled 30–32 plants of each of five additional varieties of E. ovalifolium (Table 1) from ten other sites. The five varieties were chosen because of their proximity to var. williamsiae. We did not sample E. o. var. depressum, which occurs only in Elko and White Pine counties in eastern Nevada. Morphologically, var. williamsiae is most similar to var. eximium; they are distinguishable by the color of their tomentum (white in var. williamsiae, brown in var. eximium), and by their leaves: the leaves of var. eximium are larger with distinctly brown edges. These brown edges are not as conspicuous in var. williamsiae and are not found in all leaves (Reveal, 1985
). Plants sampled from these additional populations were at least 1 m apart. All samples were stored at 4°C until analyzed. Voucher specimens were deposited at UTC.
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). Starch gels (12%) were run at 20 mA for 10–12 h. The buffer systems used, enzymes and loci examined, and number of alleles observed are shown in Table 2. Initially we screened 15 enzymes of which 8 were reliable and therefore retained. Sigma starch (S-4501, Sigma Chemical Company, St. Louis, Missouri, USA) was used for all gels, and staining procedures followed Soltis et al. (1983)
. The loci were numbered sequentially with the fastest migrating locus labeled as "1" and the fastest allele for each locus as "A." Bands were interpreted based on known cellular compartmentization and enzyme substructuring (Weeden and Wendel, 1989
).
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) and Biosys-1 (Swofford and Selander, 1981
). Genetic variability within E. o. var. williamsiae was described by calculating the following statistics for each population: percentage of polymorphic loci (P), mean number of alleles per locus (A), observed heterozygosity (Hobs), and expected Hardy-Weinberg heterozygosity (Hexp). Any locus with more than one allele was considered polymorphic.
The observed genotype frequencies for E. o. var. williamsiae were compared to those expected under the Hardy-Weinberg model using chi-square tests and Levene's (1949)
correction for small sample size. For loci with more than two alleles, all alleles except the most common were pooled for the analysis. Loci with P values > 0.05 were considered to be in Hardy-Weinberg proportions.
Genetic substructuring of E. o. var. williamsiae was examined using Wright's F statistics (Wright, 1965
), including the inbreeding coefficient (FIS), the fixation index (FST), and the overall inbreeding coefficient (FIT). FIS describes the relative reduction of heterozygosity due to nonrandom mating within subpopulations, and FST describes differentiation among subpopulations as a function of variance in allele frequency (Hartl and Clark, 1997
). These F statistics can thus be used to describe the levels of substructuring and inbreeding within a population.
An estimate of the extent of clonal spread was made by determining the multilocus genotypes within the three clusters of samples (A, B, and C). The probability of sampling each given multilocus genotype (pgen) was calculated as the Hardy-Weinberg frequency multiplied across loci, following Parks and Werth (1993)
and Montalvo et al. (1997)
:
). Chi-square statistics for gametic disequilibrium were calculated as the squared estimates divided by the sampling variances, under the hypothesis that the true value of the disequilibrium was zero. Locus pairs with values below the alpha level of 0.05 were considered to be in gametic disequilibrium. Since allele frequencies are used in calculating pgen, we also assumed that clones were not resampled for those individuals used to determine allele frequencies. The possibility of resampling clones was minimized by always sampling ramets that were at least 10 m apart. The clustered sampling was intended to estimate clone frequency and size and so was not included in the calculations of allele frequencies. To address how distinct E. o. var. williamsiae was from other varieties of E. ovalifolium, a phenogram of genetic distances among populations was generated using a UPGMA (unweighted pair group method using arithmetic averages) cluster analysis of Nei's genetic identity coefficients.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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as the overall average percentage of polymorphic loci within populations (34.2%). The mean number of alleles per locus (A) and expected heterozygosity (Hexp) for var. williamsiae were also higher than the average values given by Hamrick and Godt (1989)
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for endemic to widespread species (also shown in Table 3). The values calculated for var. williamsiae, while higher than this entire range, were closer to the values given for widespread species. This was unexpected because var. williamsiae is a narrow endemic taxon.
Genotype proportions and exchange of genes within the population
The chi-square test for deviation from Hardy-Weinberg genotype proportions gave P values that were all >0.05, except for 6pgd-1 in subpopulation 1, which was 0.038. This one significant P value was the result of a deficiency in heterozygotes, which could be caused by inbreeding. However, inbreeding should affect all loci instead of just one locus in one subpopulation. There are several other possible causes, including a violation of some other Hardy-Weinberg principle or sampling error. Because we chose a 0.05 alpha level, we expect (if the hypothesis were true) these calculations of P values to cause an erroneous rejection of a true null hypothesis in 5% of the cases, on average. We ran this test 21 times and thus would expect to observe a P value <0.05, on average, once, which we did. Since all other P values were much greater than 0.05 (
= 0.53, SD = 0.25), our data are consistent with the assumption of Hardy-Weinberg proportions. The chi-square test is not very sensitive to small deviations from the expected genotype frequencies, and we did not test for alternatives to the null hypothesis of Hardy-Weinberg proportions. Thus, we can only state that these loci do not deviate enough to be detected by our test (Hartl and Clark, 1997
).
Genetic structure of E. o. var. williamsiae
The F statistics also gave no evidence of inbreeding (Table 4). In fact, five of the seven FIS and FIT values were negative, indicating a slight excess of heterozygotes. All FIS and FIT values, negative or positive, remained small. The FST values were also close to zero, indicating little genetic substructuring in the single population of E. o. var. williamsiae. The deviation of FIS and FST from zero was tested by the chi-square test, and the chi-square values were summed for an overall test. The results showed that none of these values varied significantly from zero.
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Upon examining the multilocus genotypes of the samples in clusters A, B, and C (Table 5), two groups of possible clones were found (Fig. 1) based on the very low probability of their identical genotypes arising independently (pgen). One was in cluster A and consisted of six samples of genotype 3 with a pgen of 0.01. The other was in cluster C and consisted of two samples of genotype 21 with a pgen of 7.44 x 10-5. Since both pgen values were far below our 
of 0.05, we considered each group of identical samples to be a clone. The farthest distance between any two sampled ramets with the same genotype was 67 cm. This occurred between the two samples of genotype 21, in cluster C. The largest distance within the other clone (in cluster A) was 62 cm.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), all three estimates of genetic variation (A, Hexp, and especially P) were high compared even to the average for widespread species (Hamrick and Godt, 1989
). If the rest of the genome of var. williamsiae is as variable as the small portion we studied, then it is unusually diverse for a narrow endemic taxon. There are multiple possible sources for high genetic variation, two of which include either hybridization with other closely related taxa (Godt and Hamrick, 1996
; Colosi and Schaal, 1997
) or recent speciation via hybridization of two or more widespread taxa (Wolfe and Elisens, 1993
; Rieseberg and Van Fossen, 1995
; Godt and Hamrick, 1996
; Smith and Pham, 1996
). The gynodioecious breeding system of E. o. var. williamsiae, which will be discussed below, could also be involved in the maintainance of high variation because it promotes outcrossing. Genetic variation in E. o. var. williamsiae appears to be spread evenly throughout the 100–150 ha population. Neither inbreeding nor population substructuring was evident at the scale at which we sampled. Genetic identities among the three purported subpopulations were very high (I = 1.00), and FST values were very low.
The absence of inbreeding is somewhat surprising because Steamboat buckwheat has several attributes that would seem to promote selfing. Plants produce numerous flowers simultaneously and are clonal, though clones are not large (see below). Bisexual flowers are self-compatible, but not autogamous, thus necessitating pollen vectors. Flowers are visited by a diverse group of smallish insects including bees, wasps, flies, and butterflies (V. J. Tepedino, W. R. Bowlin, and J. K. Archibald, unpublished data) whose different foraging behaviors may affect the relative levels of inbreeding and outbreeding. Wasps, and especially flies and butterflies, which are not central-place foragers (Orians and Pearson, 1979
; Geer et al., 1995
), are likely to disperse pollen widely because they visit flowers only for nectar and visit relatively few flowers per genet (see discussion in Proctor, Yeo, and Lack, 1996
). In contrast, the small halictid bee visitors that collect pollen as well as nectar undoubtedly visit more flowers per genet and more frequently effect geitonogamous pollinations. The absence of inbreeding suggests that selection has been against inbred individuals or that the shorter average flight distances of bees are more than compensated by the outbreeding brought about by the longer flights of other flower visitors.
We confirmed that Steamboat buckwheat reproduces vegetatively, but clones appear to be small (<70 cm in extent). Because we sampled relatively few ramets at this scale, we cannot judge the frequency of clonal growth. Answering this would require a more intensive sampling scheme at the scale of 0–100 cm. Regardless, our results show that clones of var. williamsiae are probably not so large that they greatly reduce the effective population size, as would occur if the population was composed of a few very large clones (e.g., Aspinwall and Christian, 1992
).
As expected, E. ovalifolium var. williamsiae appears to be genetically similar to the other varieties of E. ovalifolium we examined, though similarities were not higher than those commonly encountered between varieties of one species (Crawford, 1983
). The closest genetic identity was between endangered var. williamsiae and widespread var. ovalifolium. Indeed, var. ovalifolium population A was more similar to var. williamsiae than to var. ovalifolium populations B and C (Fig. 2), prompting the question of whether these two varieties should be treated as distinct taxa. High genetic identity is an inviting but insufficient reason to merge two varieties. First, genetic identities between varieties often approach or equal values among populations within the same variety (Crawford, 1983
). Second, the genetic identity that we calculated was based on a relatively small sample of allozyme loci within the entire genome. These two varieties might possess fixed differences at other loci, perhaps even at loci whose products have more ecological significance than the ones we studied. Third, morphologically, these two varieties are quite different. In general, var. ovalifolium is larger than all other varieties studied here; its leaves, scapes, involucres, and flowers are generally longer than those of var. williamsiae (Reveal, 1985
). The corolla of var. ovalifolium is yellow, that of var. williamsiae is white or cream, turning pink with age.
Though it is premature to merge var. ovalifolium with var. williamsiae at present, a more detailed genetic and ecological analysis is warranted (Rieseberg, 1997
). Reciprocal transplants or common garden experiments should be done to determine whether the morphological differences between varieties are genetic or are environmental effects of growing on different substrates. A survey should be conducted to determine the distribution and morphological characteristics of all other varieties of E. ovalifolium in the Steamboat Springs region and its immediate surroundings. Also, breeding experiments to test the interfertility of these varieties could be conducted. Although varieties are generally expected to be interfertile, if a test revealed cross-incompatibility, it would provide evidence that the varieties are indeed distinct.
One alternative explanation for the genetic similarity between endemic var. williamsiae and widespread var. ovalifolium is that the latter has hybridized with another variety to create the former, perhaps by cytoplasmic introgression. Examples of such phenomena are becoming widely recognized (Rieseberg and Soltis, 1991
; Rieseberg, 1995
). A likely participant in such a scheme is the geographically restricted var. eximium, which var. williamsiae most closely resembles morphologically.
Our reasons for proposing an hybridization hypothesis are fourfold. First, while examining the breeding system in the year subsequent to our genetic sampling, we discovered that E. o. var. williamsiae is gynodioecious (V. J. Tepedino, W. R. Bowlin, and J. K. Archibald, unpublished data). This finding contrasts with previous descriptions (Reveal, 1981, 1985
; Williams, 1982
; Kartesz, 1987
; U.S. Fish and Wildlife Service, 1995
), which imply that the flowers are all bisexual (only Hickman [1993
] noted that flowers are sometimes unisexual). The female genets produce flowers whose stamens bear anthers that are either small, poorly developed, and knoblike, or larger but flattened; neither type produces pollen. The flowers of hermaphrodite plants produce normal, plump, polleniferous anthers capable of siring seeds (V. J. Tepedino, W. R. Bowlin, and J. K. Archibald, unpublished data). We take this as an important datum because cytoplasmic male sterility (CMS) and gynodioecy were unknown in Eriogonum until recently (several subspecies of E. umbellatum have now been found to be gynodieocious; K. Steiner, personal communication, California Academy of Sciences) and are rare in the Polygonaceae (Kaul [1988
] records few published examples), but male sterility, particularly CMS, is a common condition in hybrids (Grant, 1975
). However, it is possible that gynodioecy is more prevalent in this species or genus than it currently appears. More work needs to be done on the breeding systems of other varieties and species in the genus before it can be determined if gynodioecy evolved independently in E. o. var. williamsiae. If it was independently derived in this group, its appearance could be due to hybridization, with the female plants then being maintained by selection (Richards, 1997
).
Second, as with many hybrids (Ellstrand and Elam, 1993
), production of viable seed by Steamboat buckwheat is very low (U.S. Fish and Wildlife Service, 1995
). Some of the poor seed production is due to high seed predation by larvae of the lycaenid butterfly genus Euphilotes (W. R. Bowlin, personal communication, Utah State University). However, flower heads collected in each of 3 yr by The Nature Conservancy for storage by the Berry Botanical Garden have produced <1% viable seeds, strongly suggesting other genetic incompatibility factors as well, such as those associated with hybridization (Rieseberg, 1997
).
Third, like many hybrids (Rieseberg, 1997
), Steamboat buckwheat is confined to a novel habitat that differs greatly from that of its hypothesized parents. Steamboat buckwheat occurs only on substrate derived from hot springs activity that supports few other plant species (U.S. Fish and Wildlife Service, 1995
). In Washoe County, its hypothesized parents, vars. ovalifolium and eximium, are found on dry sand or gravel and granitic sand, respectively (Hickman, 1993
). Such ecological premating barriers aid in isolating nascent taxa and in reducing the incidence of introgression (Rieseberg, 1997
).
Fourth, as noted above, one explanation for the high genetic variability we found in Steamboat buckwheat is recent origin through hybridization and/or hybrid dysgenesis (Barton and Hewitt, 1985
; Rieseberg, 1997
). It is common for hybrids, particularly recent ones, to display high levels of genetic variability (Rieseberg and Wendel, 1993
; but see Rieseberg, 1997
), because of the combined variation from parental species and sometimes because of high mutation rates (Barton and Hewitt, 1985
). An hybrid origin of this variation, rather than simple divergence from var. ovalifolium for example, is also supported by the fact that E. o. var. williamsiae shares some alleles with var. ovalifolium but not var. eximium and shares others with var. eximium but not var. ovalifolium. Due to the high degree of allelic overlap between varieties, there are only a few alleles to support this pattern. However, it is at least suggestive of hybridization. E. o. var. williamsiae had only 1 out of 36 alleles that was not present in either var. ovalifolium or var. eximium (or, in fact, in any of the other varieties sampled). This allele was very rare, with a frequency of only 0.013 in one subpopulation and not occuring in the other two subpopulations.
Thus, there are several characteristics of E. o. var. williamsiae that support the possibility of an hybrid origin. Of course, there are also other possible explanations for each one of these aspects of var. williamsiae's biology, and further work is necessary to determine whether an hybridization hypothesis represents the true history of the group. Ultimately, to unravel the ancestry of E. o. var. williamsiae, to better judge its taxonomic status, and to make recommendations for its conservation, studies will have to compare nuclear and cytoplasmic DNA among E. ovalifolium varieties. It would also be helpful to have chromosomal information on these varieties. The presence of this entity on the U.S. Endangered Species List lends a certain urgency to such a study because of the "Hybrid Policy" of the Endangered Species Act (Avise, 1994
). Perhaps E. o. var. williamsiae is not a "listable" taxa at all, but rather a hybrid swarm in the process of introgression with one or more of its parents, or indeed, with the other two species of Eriogonum present in the Steamboat Hills (U.S. Fish and Wildlife Service, 1995
).
We began by arguing that information on the genetic diversity and structure of rare plant populations is important for conservation management plans. In some ways our results suggest the opposite for Steamboat buckwheat: with the critical exception of demonstrating a need to clarify its systematic status, genetic considerations are currently of minimal bearing. The relatively high genetic diversity, suggested by high allozyme diversity, and the absence of genetic structure revealed by our study make the most immediate conservation goals quite straightforward. Because genetic diversity is usually positively associated with ability to resist disease and various kinds of stress, efforts to preserve and/or increase genetic diversity should increase the chances of survival of this rare taxon. There are several direct methods of preserving genetic diversity. First, new populations could be established, but because Steamboat buckwheat appears to be an extreme habitat specialist, this option seems limited. A second approach is to maintain or augment present population size. It may be difficult to greatly increase the number of genets growing in the Steamboat Hills, but maintaining the population at current levels by careful choice of future development sites and avoiding further fragmentation of the population seems feasible. Limiting fragmentation is particularly important lest it lead to reduced gene flow, inbreeding, and/or genetic drift. Fragmentation leading to sudden inbreeding can be especially dangerous for a rare population that normally accumulates deleterious recessives through outbreeding (Hedrick and Miller, 1992
). This means that if additional facilities, e.g., roads and/or industrial plants, must be constructed, they should be sited peripherally so as to have minimal impact on population size and spatial coherence. If it is necessary to use land that presently supports Steamboat buckwheat plants, then transplantation should be to bare areas of sinter substrate. Though these recommendations are simple demographic remedies to prevent the erosion of genetic variability, they could well have differed if we had detected evidence for population structure, low genet number, or inbreeding.
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FOOTNOTES |
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4 Current address: Department of Evolution, Ecology and Organismal Biology, Ohio State University, 1735 Neil Ave., Columbus, Ohio 43210-1293 USA.
6 Author for correspondence (Phone 435-797-2559, FAX 435-797-0461, e-mail: andrena{at}cc.usu.edu
).
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