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2Muséum National d'Histoire Naturelle—CNRS UMR 8571, Laboratoire d'Ecologie générale, 4 avenue du Petit Château, 91800 Brunoy, France; and 3Muséum National d'Histoire Naturelle—CNRS FR 1541, Systématique Moléculaire, CNRS ESA 8044, Laboratoire de Biologie des Invertébrés Marins et Malacologie, 55 rue Buffon, 75005 Paris, France
Received for publication December 16, 1999. Accepted for publication July 11, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Bromeliaceae • genetic diversity • genotypic disequilibrium • inselbergs • isozymes • sexual reproduction • South America; • spatial autocorrelation • vegetative spread
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The origin of the present vegetation, strikingly different from the surroundings, in such characteristic habitats, is not well understood. The inselbergs are traditionally interpreted as isolated refuges for a xeric savanna flora in a landscape which otherwise is characterized by a humid climate with tropical rain forest (Hurault, 1974
; de Granville, 1982
). This xeric flora was probably much more widespread throughout South America during the glacial episodes, especially the Würm (22 000–13 000 BP) and other shorter dry periods during the Holocene (de Granville, 1982
). The distribution of tropical rain forest during the last glacial epoch is under debate (Hooghiemstra and van der Hammen, 1998
), but one hypothesis is that climatic changes in Amazonia resulted in successive waves of rain forest expansion and regression, with the current situation sometimes being inverted and patches of rain forest being present instead as islands within the savanna (Haffer, 1969
; Prance, 1973, 1983
; van der Hammen, 1974
; Hooghiemstra and van der Hammen, 1998
). Consequently, we can imagine that in times of rain forest regression, population sizes of inselberg species increased, and during times of rain forest advancement, these species have been relegated to inselbergs.
These historical factors have led to the observed disjunct populations, and such fragmentation is supposed to strongly influence the genetic structure of populations. The rain forest expansion leads to reduced population sizes in xeric flora. These reductions could generate bottlenecks that result in loss of genetic diversity. The examination of genetic diversity in pilot species is helpful in determining the sources of current populations and the effects of history on genetic structure. Moreover, these outcrops constitute singular environments, due to the thin and poorly developed soils and severe microclimatic variations, and the biology of plants growing in these xeric environments, such as breeding systems, seed dispersal mechanisms, vegetative reproduction, and spread, is poorly documented. One way to investigate these biological characteristics is to quantify the levels and distribution of genetic diversity within and among plant populations (Hamrick, Linhart, and Mitton, 1979
; Loveless and Hamrick, 1984
; Hamrick and Godt, 1989
).
Among the plants living on the South American inselbergs, bromeliad species are especially well represented (Barthlott, Gröger, and Porembski, 1993
; Ibisch et al., 1995
; Porembski et al., 1998
; Sarthou and Villiers, 1998
). Generally, they build very dense mats on these rocky habitats. Pitcairnia geyskesii is the most common bromeliad colonizing the French Guianan inselbergs and represents the dominant species of the most widespread epilithic plant community found on these outcrops (Sarthou and Villiers, 1998
). Although little is known about its life history and reproductive behavior, these rhizomatous plants are supposed to propagate both sexually and asexually. Surveys of such plants generally indicate that genetic diversity is not reduced within populations compared to plants with primarily or exclusively sexual reproduction (Ellstrand and Roose, 1987
; Hamrick and Godt, 1989
; Widen, Cronberg, and Widen, 1994
; McLellan et al., 1997
).
This study investigated the genetic structure and the spatial distribution of genotypes of Pitcairnia geyskesii growing on three inselbergs, using enzyme electrophoresis. Each inselberg, interpreted as a xeric refuge, represents a geographically isolated population of this bromeliad. Analyses were performed at different levels: among inselbergs, within inselbergs but among mats, and within mats. Our goals were to provide insights into the reproductive strategy of P. geyskesii in colonization and establishment on these fragmented habitats and to determine the relative contributions of sexual and asexual reproduction.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) belongs to the Bromeliaceae, a widespread and characteristic family of the American tropics and subtropics. Over this vast range, bromeliads are found in a variety of habitats. Although they are generally thought of as rain forest epiphytes, they also occur on soil and sand, and many are saxicolous. Pitcairnia geyskesii is endemic to French Guiana and Suriname and is specific to the rocky outcrops of inselbergs. This herbaceous perennial species is common on all the few inselbergs explored until now. However, no estimate is available to indicate how many populations may exist and how large the populations are in size. The plant is known as a clonal species because it has creeping rhizomes producing new shoots and builds dense mats on the granitic surfaces. Mats are generally well delimited and grow in size with age. They vary in size, but mats are typically between 10 and 25 m2. The rhizomes bear an apical rosette of spiny leaves and 1–2 m high red inflorescences composed of zygomorphic flowers. Flowering occurs mainly in March and April during the short dry season in French Guiana, and the rosettes produce inflorescences with hermaphroditic flowers. The small and light seeds are dispersed by wind. The flowering induces the death of the rosette and is coupled with the production of two lateral ramets by vegetative reproduction. Due to the progressive loss of physical connections between ramets, the extent of clonal growth is difficult to document by direct examination.
Sampling
Fieldwork was undertaken in French Guiana during botanical expeditions. The inselbergs cannot be reached easily and expeditions require helicopter transports. Populations were sampled on three granitic inselbergs (Fig. 1) of different sizes in 1997, 1998, and 1999: Mont-Chauve (3°49' N, 52°44' W, altitude 265 m), Trinité (4°35' N, 53°21' W, altitude 400 m), and Nouragues (4°3' N, 52°42' W, altitude 410 m). The distances between the different inselbergs are: Mont-Chauve and Nouragues, 26 km; Nouragues and Trinité, 94 km; and Mont-Chauve and Trinité, 110 km. The shoots were collected on a grid pattern with a distance of 20 m between each sampling point with the aim of working at the genet level. The sampling spanned the entire area of each population. The summit population of the Mont-Chauve inselberg consisted of two subpopulations separated by a forest: 47 shoots were sampled on the south side and 33 on the north. Fifty-five shoots were collected on the inselberg of Trinité. Sampling was done on both the south slopes (50 shoots) and summit (32 shoots) of the Nouragues inselberg. The two subpopulations were separated by a 100 m high cliff.
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1.5 m2 (A, 13 shoots and B, 10 shoots), and partially (1/10) for a larger mat, (6 m2 C, 10 shoots).
Methods
Allozyme analysis
Entire rosettes were collected and brought to the laboratory after eliminating the older leaves. The plants were cleaned in the laboratory, and 500 mg of fresh material (basal tissues of young leaves) was homogenized with sand in 50 mL of a tris-glycine (4.95 mmol/L, pH 8.3) extraction buffer containing 0.17% mercaptoethanol, polyvinyl pyrrolidone (10 mg/mL), and saccharose (86 mg/mL) and subsequently were centrifuged at 137 000 m/s2 for 15 min. Vertical acrylamide gels on discontinuous systems (Hoefer apparatus) were used for the electrophoresis, with tris-glycine pH 8.3 as running buffer. We screened eight enzyme systems: aconitase, ACO, EC 4.2.1.3; alcohol dehydrogenase, ADH, EC 1.1.1.1; aspartate aminotransferase, AAT, EC 2.6.1.1; esterases, EST, EC 3.1.1.1; isocitrate dehydrogenase, IDH, EC 1.1.1.42; malic enzyme, ME, EC 1.1.1.40; phosphoglucomutase, PGM, EC 5.4.2.2; and superoxide dismutase, SOD, EC 1.15.1.1. When enzymes were encoded by genes at several presumptive loci, these were numbered in order of decreasing mobility. The alleles were numbered accordingly.
Genetic analysis
The data matrix of individual genotypes was analysed using the BIOSYS software package (Swofford and Selander, 1981
) for calculation of standard measures of allozyme diversity: allele frequencies, percentage of polymorphic loci (P), number of alleles per polymorphic locus (AP), genetic diversity (mean observed and expected heterozygoties), and Nei's (1972)
genetic identities (or distances) between populations. The GENEPOP population genetic software package (Raymond and Rousset, 1995
) was used to explore the genetic structure within and between populations. Adequacy of genotypic proportions to Hardy-Weinberg expectations was tested by an exact test. The HWE is rejected when the probability of occurrence of the observed sample is <0.05.
To quantify levels of allelic variation within and among populations and to infer the degree of population subdivision, F statistics were calculated. They were computed according to Weir and Cockerham (1984)
, 
being an estimate of FST (fixation index measuring the effects of population subdivision). For the three inselbergs, F statistics were calculated, and, independently, F statistics were calculated for each of the inselbergs of Mont-Chauve and Nouragues where two subpopulations were clearly distinguishable, in order to evaluate genetic heterogeneity between the two subpopulations.
Following Crow and Aoki (1984)
, gene flow between inselbergs was estimated using the relation FST = 1/(1 + 4Nm
), because only a small number of populations was sampled. The abbreviation Nm represents the number of individuals exchanged between populations per generation, and = [n/(n - 1)]2, where n is the number of populations.
Multilocus linkage disequilibrium
At each generation, clonal reproduction duplicates multilocus genotypes, whereas sexual reproduction creates novel multilocus combinations of alleles. Thus, in populations where individuals reproduce both sexually and asexually, parental multilocus genotypes are overrepresented in the following generation. As a general consequence, a population that uses a mixture of sexual and vegetative reproduction will, depending on the amount of vegetative reproduction, more or less rapidly develop multilocus linkage disequilibrium. The presence of multilocus linkage disequilibrium therefore could indicate the existence of asexual reproduction. This disequilibrium could be enhanced by genetic drift and/or natural selection or by a preexisting disequilibrium at population founding. In order to test for this disequilibrium, we first calculated the probability pobs that two individuals randomly sampled from a given population have the same genotype, using the matrix of complete multilocus genotypes observed in this population. We then resampled this matrix of individual genotypes by permuting individual genotypes at each locus. For each of the 10 000 random samples, the value of p was calculated in order to obtain its probability distribution. The hypothesis of no multilocus linkage disequilibrium was rejected if the area of the distribution covered by the values of p 
pobs represented <5% of the total surface.
Genotypic analysis of mats
As a test of vegetative growth within the three mats collected on the Trinité inselberg, we attempted to answer the following question: are the individuals sampled in a mat a random sample of the inselberg population? From the allelic frequencies calculated for each locus in the inselberg population, we created 10 000 random samples with the same number of individuals as those sampled in the mats (13, 10, and 10 for mats A, B, and C, respectively). For each random sample, we calculated the number of individuals sharing the most common genotype (nG). We then evaluated the area of the distribution such that nG nGobs (nGobs being the observed number of individuals exhibiting the most common genotype within each mat). If the area was <5% of the total area, we rejected the null hypothesis that the given mat sample is a random sample of the inselberg population. The test was performed for each of the three mats.
Spatial distribution of genotypes
The spatial structure of genetic variation is expected to differ from random distribution for a number of reasons, including differences in breeding system and asexual reproduction. The objective of this analysis was to study the distribution of the analyzed genotypes to point out eventual patches of identical genotypes that could be due to a step-by-step progression of news shoots arising from rhizomes. The random distribution of multilocus genotypes in space was tested by spatial autocorrelation (Epperson, 1993
; Epperson and Li, 1996
), using distances between sample sites within populations. For each population, seven equifrequent distance classes were determined. Nearly the same number of distances in each class (including at least 100 distances) is a prerequisite for a reliable statistical significance. Then, multivariate spatial autocorrelograms were computed for genotypic dissimilarity. For each distance class l, the Mantel's standardized statistic r (Smouse, Long, and Sokal, 1986
), and the corresponding significance value, were calculated between two square matrices A and Bl (l varying from 1 to 7). Here, Bl is a binary matrix of coefficients bj,k, with bj,k = 1 if the distance between sites j and k belongs to the class l and bj,k = 0 if not, and A is the binary matrix of genotypic dissimilarity between sites. If the same multilocus genotype is found in sites j and k, the matrix coefficient aj,k = 0, in the other cases aj,k = 1. Computations were performed using the software "R" (Legendre and Vaudor, 1991
).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Table 4 reports F statistics that gave components providing information on inbreeding within inselberg populations (FIS), within the total population (FIT), and on the amount of variation due to differentiation among populations (FST). The mean FIS value was negligible and the major component of FIT was FST (0.322), suggesting genetic heterogeneity among populations. Effectively, most alleles of the seven polymorphic loci were present in the populations of the three inselbergs, but with different allele frequencies. Moreover, only two alleles at two different loci were restricted to one inselberg, Aco-1 to Mont-Chauve and Pgm-1 to Trinité, both in low frequencies.
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The value of FST calculated for the three populations led to a low estimate of the number of migrants per generation as Nm = 0.234.
Multilocus linkage disequilibrium
The populations sampled on each of the inselbergs did not exhibit multilocus linkage disequilibrium. In contrast, when the population collected on Mont-Chauve was subdivided into the two subpopulations, a significant (P = 0.025) multilocus linkage disequilibrium was detected for the southern subpopulation. Within this subpopulation, nine individuals had the same multilocus genotype (over the 47 sampled individuals). No multilocus linkage disequilibrium was observed when the Nouragues population was subdivided.
Genotypic composition of mats
Allozyme analyses of individual mats demonstrated their multigenotypic constitution. Five genotypes were observed in mat A: one frequent (seven shoots), two represented by two shoots, and two found in a single shoot. Three genotypes were present in the entire mat B sample: one most frequent (six shoots), one identical in three shoots, and one found in a single shoot. Six different genotypes were found in mat C, partly sampled: one frequent (five shoots) and five rare (one shoot each). The hypothesis of random sampling of the inselberg population was rejected for each mat with a probability of 0.07%, 0.83%, and 4.23% for mats A, B, and C, respectively.
Spatial distribution of genotypes
Tests of spatial genetic structure showed that genotypic dissimilarity and geographic distances, divided into equifrequent distance classes, were not correlated at Nouragues where numerous unique genotypes are found (Fig. 2). In contrast, the second distance class (between 45 and 82 m) at Mont-Chauve was negatively correlated (r = -0.042, P = 0.050) with genotypic dissimilarity, indicating a patchy distribution of genotypes (Fig. 3). Probably due to sample size, grid pattern, and absence of rectangular form, the first distance did not present significant correlation. At Trinité (Fig. 4), the second class (between 45 and 72 m) was positively correlated (r = 0.052, P = 0.039), whereas the fourth class (between 88 and 113 m) was negatively correlated (r = -0.055 and P = 0.047). Probably for the same reasons as in Mont Chauve, no significant correlation was observed for the first distance class. This pattern (alternation of positive and negative correlation) could be interpreted as the consequence of a few large genetically identical patches. Indeed, two large patches sharing the same genotype appeared at a distance of 100 m (Fig. 4). Two factors may explain this patchy distribution of genets: (a) an actual clonal spread originated by the breaking off of a rhizome that was carried and lodged some distance away and (b) by chance, separate patches of P. geyskesii actually have the same genotype. To reject one of these alternative hypotheses, we would need additional variable genetic markers.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Murawski and Hamrick, 1990
). These three bromeliads have smaller population sizes than Pitcairnia geyskesii, a factor that could influence the level of genetic variability within populations through genetic drift (Wright, 1951
; Nei, 1987
). However, the mean values of number of alleles per locus and percentage of polymorphic loci are of the same magnitude in P. geyskesii as those previously reported for allozyme data from species that share similar ecological or life history traits (Hamrick and Godt, 1989
). Genetic diversity within populations of P. geyskesii is substantial: a high number of different genotypes were distinguished on the three inselbergs. The highest number was found at Nouragues, especially on the summit of the inselberg where all the sampled plants, collected only 20 m apart, proved to be genetically different. However, this high genetic diversity does not exclude local (<20 m) vegetative spread. Surveys of genetic variation in plants with clonal growth generally indicate nonreduced genetic diversity within populations compared to plants with primarily or exclusively sexual reproduction (Ellstrand and Roose, 1987
; Hamrick and Godt, 1989
; Widen, Cronberg, and Widen, 1994
; McLellan et al., 1997
). Eriksson (1993)
, McFadden (1997)
, and Schläpfer and Fischer (1998)
proposed two possible hypotheses to explain the high genetic diversity observed in local clonal populations: (1) association of high genet longevity with high diversity at population foundation and no competitive exclusion of genets, or (2) low but continuous seed recruitment over time. The present results do not allow us to reject one of these hypotheses.
Reproductive strategy
Although little is known about the reproductive biology of P. geyskesii, isozyme data provide some insights into the mating system of the species. At the inselberg level, the data, in general, conform with Hardy-Weinberg expectations and suggest panmixia. The hypothesis of outbreeding is in agreement with the observation of hummingbirds (Phaethornis bourcieirii) frequently visiting the hermaphroditic flowers of Pitcairnia geyskesii (C. Sarthou, personal observation). They may act as the major pollinators in the bromeliad patches. The grid pattern of 20 x 20 m gave effectively a genet sampling at the inselberg level, on the three inselbergs.
At the mat level, both vegetative spread and seed recruitment were demonstrated. Mats do not form strict clonal units but consist of one major genotype and other intermixed genotypes. The dominant genotype of each mat was probably due to vegetative reproduction. The hypothesis of production of minor genotypes by self-fertilization of the dominant genotype is rejected for mats A and B. Indeed, at least at one locus, all minor genotypes exhibited an allele that did not belong to the dominant genotype. This hypothesis is rejected for only one minor genotype in mat C. The hypothesis of minor genotypes being the outcrossed seedling of the dominant genotype is rejected for only one genotype in mat B, because it is unrelated to the dominant genotype since it is homozygous for a distinct allele. Thus, the observed minor genotypes came either from the inselberg population (via dispersed seeds) or corresponded to the outcrossed or selfed progeny of the dominant genotype. Several seedlings are involved in established mats, either during the first stages of mat building, or, subsequently, after the vegetative multiplication of the first shoot. The hypothesis of several seedlings at mat initiation is based on the presence of cyanobacterial crusts on the rock surface before mat initiation. Cyanobacteria produce organic matter with high nutrient contents that maintain wet microconditions favoring seedling establishment (Sarthou and Grimaldi, 1992
; Sarthou, Thérézien, and Couté, 1995
). Thereafter, one or a few genotypes may be multiplied by vegetative spread by ramet production from rhizomes. This multiplication may be strictly vegetative or subsequent to flowering by production of two lateral ramets. The physical structure of established mats is such that new seedlings are thought unlikely to survive. High shoot density does not seem to favor the establishment of seedlings. Evidence might by inferred by genetic analyses and the study of spatial distribution of genotypes within mats of different sizes. These additional data might give some insights to estimate competition and to test the possibility of establishment of seedlings in mats.
A multilocus genotypic linkage disequilibrium is obvious at the subpopulation level for the southern side of Mont-Chauve. This disequilibrium is probably a consequence of establishment of new mats by vegetative multiplication. Indeed, vegetative spread, associated with sexual reproduction, may account for both multilocus disequilibrium and panmictic behavior of each locus analyzed. Indeed, if clonal multilocus genotypes are involved in the sexual reproduction, a panmictic structure is expected in only one generation for each locus, without overlapping generations.
The spatial analyses performed on the inselberg of Trinité and Mont-Chauve show a patchy distribution of the genotypes. This observation suggests that clonal reproduction, demonstrated within mats, is also involved in the establishment of new mats. Fragmentation of peripheral young shoots of established mats (C. Sarthou, personal observation) should be involved in this process. Clonal reproduction was not demonstrated on the inselberg of Nouragues. This population is genetically more polymorphic than the two others of Trinité and Mont-Chauve, with many unique genotypes. Our results indicate that vegetative reproduction is important mainly at the mat level (<20 m in diameter). Indeed, Murawski and Hamrick (1990)
have shown local clonal spread in the bromeliad Aechmea magdalenae, with ramets generally occurring within 10 m. More recently, Reusch et al. (1999)
demonstrated clonal spread in Zostera marina, but a panmictic structure was detected with sampling at distances >27 m. It seems likely that every species and even every population can exhibit their own specific genet–ramet structure.
Population structure
Although all populations share common alleles, interpopulational differences in allele frequencies were detected that indicate substantial differentiation among populations. The FST value calculated on all polymorphic loci is relatively high (0.322) compared to the values recorded for species sharing the same ecological and life history traits (Hamrick and Godt, 1989
). The P. geyskesii populations, as suggested by the observed level and structure of genetic variation, appear to share features with populations with outcrossing breeding system approaching panmixia. Pitcairnia geyskesii seems to consist of a series of disjunct populations, more or less isolated from each other. Restricted gene flow (Nm = 0.234) and genetic drift might have influenced the extent of differentiation among the populations of the three inselbergs. The Mont-Chauve and Nouragues populations, geographically neighboring, are genetically close, whereas the Trinité population, located farther to the north in French Guiana, is genetically more distant. The genetic identities coincide perfectly with the geographic distances.
The analyses performed at different levels (inselbergs and mats) give different but complementary information on the reproductive behavior of P. geyskesii. (1) Efficient sexual reproduction leads to seed recruitment at the level of the inselberg. (2) Both clonality and seed recruitment occur within mats. (3) Vegetative spread by fragmentation is involved in the establishment of new mats.
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FOOTNOTES |
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4 Author for correspondence (Phone 33 1 40 79 30 94, FAX 33 1 40 79 30 89, e-mail dubayle{at}mnhn.fr
).
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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J. GONZALEZ-ASTORGA, A. CRUZ-ANGON, A. FLORES-PALACIOS, and A. P. VOVIDES Diversity and Genetic Structure of the Mexican Endemic Epiphyte Tillandsia achyrostachys E. Morr. ex Baker var. achyrostachys (Bromeliaceae) Ann. Bot., October 1, 2004; 94(4): 545 - 551. [Abstract] [Full Text] [PDF]
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 D. L. Gustine and G. F. Elwinger Spatiotemporal Genetic Structure within White Clover Populations in Grazed Swards Crop Sci., January 1, 2003; 43(1): 337 - 344. [Abstract] [Full Text] [PDF]
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