| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
2Department of Biology, Southwest Texas State University, San Marcos, Texas 78666; and 3Department of Biological Sciences, Texas Tech University, Lubbock, Texas 79409-3131
Received for publication October 14, 1997. Accepted for publication June 19, 1998.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Key Words: Abronia • allozyme • endangered species • endemic • gene flow • genetic variation • isozyme • Nyctaginaceae
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
). Rare species may become genetically depauperate, historically or prehistorically, owing to small population size ("bottlenecking"), to strong directional selection for specialized niches, or to a combination of these factors (Barrett and Kohn, 1991
). Such genetic depauperation may itself be a cause of rarity by virtue of constraining the adaptive flexibility of populations, thus contributing to reduced mean fitness. However, some species of concern possess substantial levels of genetic variation, indicating that despite their rarity they have not been bottlenecked (Ranker et al., 1994
; Lewis and Crawford, 1995
; Smith and Pham, 1996
).
Herein we address genetic variation in a federally endangered species, Abronia macrocarpa Galloway (large-fruited sand-verbena). The easternmost representative of a genus comprising 30 species, A. macrocarpa is a very narrow endemic whose entire range is within three counties (Freestone, Leon, and Robertson) of eastern central Texas. A tap-rooted, herbaceous, spring-flowering perennial bearing heads of magenta flowers, A. macrocarpa is distinguished from congenerics by its large anthocarps that are thinner walled and more papery than other species (Galloway, 1972
, 1975
). When originally described and subsequently listed as endangered (U.S. Fish and Wildlife Service, 1988
), only one population, from Leon County, was known. Over the past five years, intensive searching of the region resulted in discovery of nine additional populations, all occurring in deep sandy soils of Post Oak Savannah Woodlands (Poole and Riskind, 1987
; Williamson and Bazeer, 1997
).
We used allozyme electrophoresis to address the following questions relative to the amount and distribution of genetic variation in this species. (1) What is the level of genetic variation in the populations of A. macrocarpa as compared to other narrow endemic species? (2) Is genetic variation distributed evenly among populations, suggesting a substantial rate of gene flow and integration of the populations so that the effective population size of the species is relatively high or alternatively, is variation distributed unevenly, indicating low rates of gene flow such that populations exist as independent units? (3) Does the geographic pattern of genetic variation help elucidate the migrational history of the species? (4) What is the distributional pattern of genetic variation within populations, especially genotype proportions relative to Hardy-Weinberg expectations, in relation to the breeding system and the degree of population structuring?
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
|
|
) fortified with 5% polyvinylpyrrolidone (molecular mass 40 000) and 1% 2-mercaptoethanol. Sand adhering to the leaves facilitated the homogenization. Homogenates were either introduced into gels immediately after homogenizing or more often stored at -85°C until being electrophoresed. Starch gels (12% Sigma starch; Sigma, St. Louis, MO) were electrophoresed and assayed for enzymes following standard methodology (Soltis et al., 1983
; Werth, 1985
; Murphy et al., 1990
). Most enzymes were assayed using premixed frozen assays (the "zymecicle" technique of Werth, 1990
). Esterase (EST), glutamate oxaloacetate transaminase (GOT), hexokinase (HK), and leucine aminopeptidase (LAP) were assayed on the lithium-hydroxide buffer (Werth, 1985
); phosphoglucose isomerase (PGI), phosphoglucomutase (PGM), and triose-phosphate isomerase (TPI) were assayed on system number 6 of Soltis et al. (1983)
; aldolase (ALD), isocitrate dehydrogenase (IDH), malate dehydrogenase (MDH), 6-phosphogluconate dehydrogenase (6-PGD), and shikimate dehydrogenase (SKDH) were assayed on morpholine-citrate pH 8.2 (Werth, 1991
); acid phosphatase (ACPH) and glucose-6-phosphate dehydrogenase (G-6PD) were assayed on tris-citrate pH 8.0 (Werth, 1985
).
Isozyme phenotypes were interpreted genetically according to standard principles (Wendel and Weeden, 1989
) and data were analyzed using BIOSYS-1 (Swofford and Selander, 1981
), NTSYS (Rohlf, 1988
), and StatView (Roth et al., 1995
).
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
), and several were apparently the result of duplicate gene expression, necessitating the following detailed explication of band interpretation.
|
|
G6PD (Fig. 8) exhibited four or more bands in all individuals. The three most anodal bands were invariant and were interpreted as an array of enzymes resulting from posttranslational modification of the product coded by a single monomorphic locus, G6pd-1 (coding by two or three loci is a viable alternative hypothesis, but viewed by the authors as a less conservative interpretation). The most cathodal band was highly variable and exhibited an array of single banded homozygous and three-banded heterozygous phenotypes (G6PD is widely reported as a dimeric enzyme) combining four allozymes and clearly interpretable as a single locus comprising a segregating polymorphism.
IDH exhibited two sets of bands, the more anodal of which was a single dark invariant band interpreted as a monomorphic locus Idh-1. The less anodal region, Idh-2, exhibited three-banded arrays of different migration, interpreted as homozygous phenotypes for alternate alleles involving posttranslational modification of gene products, and five-banded phenotypes that spanned the position of both allozymes, interpreted as heterozygotes.
LAP (Fig. 2) exhibited a single set of bands, most individuals possessing a single banded homozygous phenotype for the commonest allele (Lap1), with less frequent single-banded homozygotes for slower migrating allozymes and two-banded heterozygotes.
MDH (Fig. 3) exhibited a complex pattern with the four most anodal bands invariant and interpreted as a minimum of two monomorphic loci, Mdh-1 and Mdh-2. Cathodal to these four bands appeared a variable band zone comprising predominantly three-banded phenotypes with the middle band darkest, suggesting a nonsegregating heterozygous phenotype resulting from duplicate gene expression. This interpretation was supported by the occurrence of occasional single-banded homozygous phenotypes and asymmetrical three-banded phenotypes, consistent with at least one of the duplicate loci possessing a polymorphism. These duplicate loci were designated as Mdh-3a and Mdh-3b, the former assumed to possess predominantly the faster migrating allozyme (Mdh-3a1) and the latter the slower migrating allozyme (Mdh-3b2). To account for asymmetrical heterozygotes and rare homozygotes, both loci were interpreted as including the alternative allele as a polymorphism in some populations. A rare, even slower migrating allozyme (Mdh-3b3) was observed in a single individual. Additional MDH bands were observed in the vicinity of the gel origin, but were not considered consistently scorable.
PGI (Fig. 9) exhibited two sets of bands. The more anodally migrating band, although often poorly resolved, appeared to be nearly invariant and was interpreted as a single locus, Pgi-1. The more cathodal band was variable, appearing in individuals as either single-banded homozygotes or three-banded heterozygotes for various combinations of four allozymes, and thus was interpreted as a single locus, Pgi-2, with segregating polymorphism. As is frequently observed in isozyme patterns for PGI, additional bands interpretable as secondary isozymes ("ghost" bands) were often present.
PGM (Fig. 6) exhibited two sets of bands, each of which showed as many as four bands in some individuals and often uneven band intensities, suggesting differing gene doses in asymmetrical heterozygotes. These phenotypes were interpreted as resulting from duplicate gene expression, and four loci were designated: Pgm-1a, Pgm-1b, Pgm-2a, and Pgm-2b. The high level of variation and occurrence of some individuals that were single-banded (homozygous) made it difficult to confidently assign genotypes to one or the other duplicate locus. A "best guess" was made by assuming that particular alleles predominated at one or the other of each duplicate locus pair (cf. MDH), and genotypes were assigned based on band positions and dosages. These tentative genotype designations were used to estimate relatedness and structure of populations, for which they provided results comparable to those at other loci, but were not evaluated for conformance to Hardy-Weinberg proportions.
SKDH (Fig. 4) exhibited variation for one-banded homozygotes and two-banded heterozygotes for various combinations of three allozymes. Faint secondary isozymes were also apparent.
6PGD (Fig. 10) showed an array of multibanded phenotypes of varying complexity, minimally three-banded. These phenotypes strongly imply gene duplication for this dimeric enzyme, but they could not be confidently assigned genotype designations, and so this enzyme was not included in the tabulated data set.
TPI (Fig. 7) exhibited variation for complex arrays of bands that were somewhat suggestive of duplicate expression of at least one of the loci. TPI is noted for a propensity to produce complex band arrays (Hickey, Guttman, and Eshbaugh, 1989
), rendering it difficult to confidently interpret gene-copy number. This enzyme was not considered consistently interpretable and was not included in the tabulated data set.
Genetic variability
Forty-three alleles were detected among the 18 interpretable loci and their frequencies tallied (Table 2). Five loci (Got-1, G6pd-1, Idh-1, Mdh-1, Mdh-2) were monomorphic across all populations. For most of the 13 polymorphic loci, populations tended to share most of the alleles observed, the one notable exception being Pgi-1, which was slightly polymorphic only in one population (FC1). However, there were substantial differences in allele frequencies among the populations; at most (eight of 13) polymorphic loci, no single allele was consistently of highest frequency across populations (Table 2).
|
).
|
0.05) such that the computed value of F was not significantly different from 0, while 24 cases were significantly different from Hardy-Weinberg expectations. In each of the statistically significant cases, the value of F was greater than 0, indicating a deficiency of heterozygotes. These results mirror those frequently encountered in plant populations wherein many or most loci are in Hardy-Weinberg equilibrium owing to predominant outcrossing, yet unexpectedly high numbers of loci exhibit heterozygote deficits due to population substructuring, evaluated using F statistics as described below.
|
, 1969
) and pairwise values for Nei's Genetic Identity I (Nei, 1978
) and Rogers' Genetic Similarity S (Rogers, 1972
). Of the F statistics presented in Table 5, the most relevant is FST, which may be used as an indicator of divergence among populations; FST values range from 0 indicating no divergence to 1 indicating maximum divergence. Values of FST ranged from 0.021 (Pgi-1) to 0.481 (Pgm-1a), with a mean value of FST = 0.272 (Table 5). All values were found to be statistically greater than 0 (most at P < 0.001) using contingency chi-square analysis.
|
). However, these values were not as high as typically encountered, owing to the substantial level of genetic variation and its uneven distribution among the populations as quantified by the high FST values.
|
2 km, were placed as closest relatives, as were the three northern Leon County populations (LC2a, LC2b, and LC2c), these separated by similar distances. Of the remaining two populations, the southern Leon County population (LC1), 20 km distant from its nearest neighbors in Robertson County (and 40 km from the northern Leon County populations), was placed outside all populations, while the Freestone County population (FC1) was clustered with the northern Leon County populations despite being 47 km distant from them. Thus, it appears that while populations of closest geographic proximity tended to have high similarity values and were clustered together in the dendrogram, geographic distance did not robustly predict the affinities of the more outlying populations. This was confirmed statistically by carrying out regression of Nei's genetic identity (I) on geographic distance (D). When all 21 pairs of populations were included, the regression was statistically significant (I = 0.945–0.002D; r2 = 0.262; P = 0.018). When the three population pairs that were only 2 km or less apart were excluded, the regression for the remaining 18 pairs was not statistically significant (I = 0.917–0.001D; r2 = 0.063; P = 0.315). To evaluate degree and patterning of genetic substructure within and among populations, hierarchical FST analysis was carried out using BIOSYS-1. The designated hierarchy consisted of regions, populations, and subpopulations as indicated in Table 1. In the hierarchical analysis (Table 7), the greatest amount of variance was exhibited among subpopulations with respect to the total population sample (FXY = 0.367). A large component of this value was explained by variance among regions with respect to the total (FXY = 0.266), a result consistent with the strong geographic effect indicated by UPGMA. Variance among subpopulations with respect to region was substantial (FXY = 0.138), with the greater portion of this value explained by variance among subpopulations within populations (FXY = 0.095) and the lesser portion attributed to variance among populations with respect to region (FXY = 0.047). This latter result is consistent with significant microgeographic population substructuring (i.e., allele frequency heterogeneity among subpopulations) as predicted above on the basis of heterozygote deficiencies.
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
), motivating numerous recent investigations of diversity for allozymes and other molecular polymorphisms in such species (e.g., Godt and Hamrick, 1996
; Maki, Masuda, and Inoue, 1996
; McDonald and Hamrick, 1996
; Odasz and Savolainen, 1996
; Smith and Pham, 1996
; Arft and Ranker, 1998
). While the tendency is for rare and/or endemic species to possess low levels of genetic variation as compared to widespread congeners (e.g., Purdy and Bayer, 1995
; Godt and Hamrick, 1996
) or to seed plants in general (Hamrick et al., 1991
), less commonly rare species possess high levels of genetic variability (Ranker et al., 1994
; Lewis and Crawford, 1995
; Smith and Pham, 1996
). The potential causes of differential amounts of genetic variation among rare plants are numerous, although all are related to effective population size, and predominantly of an historical nature that may not easily be ascertained (reviewed by Barrett and Kohn, 1991
; Maki, Masuda, and Inoue, 1996
; Smith and Pham, 1996
). Clearly Abronia macrocarpa, with genetic variability index values exceeding means for widespread species, belongs to that subset of narrow endemics possessing high levels of genetic variability. This is noteworthy, given the extremely small geographic range of this species, less than 70 km between southern and northern extremes (Fig. 1).
Abronia macrocarpa is the easternmost species of a predominantly western North American genus. It is isolated from A. fragrans Nutt. ex Hook., the commonest and most widespread species in the genus, by a distance of 300 km to the west, and by a similar distance to the south from A. ameliae Lundell, another narrow endemic restricted to the Gulf coast of southern Texas. The occurrence of these two isolated eastern outlying species suggests that they may be derived from A. fragrans, a hypothesis supported by their similar morphology (Galloway, 1975
). Speciation events giving rise to these eastern outliers may have come about through divergence that followed either (1) long-distance dispersal or (2) isolation of a relict from a once more continuous eastward distribution. The high level of genetic variation encountered in A. macrocarpa is more consistent with an hypothesis of relictual origin for this species, as a foundered origin would likely have been accompanied by a loss of genetic variation.
A substantial level of duplicate gene expression was evident in A. macrocarpa, higher than that typically encountered in fully diploid or diploidized plant species (Gottlieb, 1982
; Wendel and Weeden, 1989
; Soltis and Soltis, 1993
). Duplicate gene expression was inferred for band phenotypes of Mdh-3, Pgm-1, and Pgm-2 among scorable loci and was apparently the cause for uninterpretable phenotype complexity of 6PGD and TPI. Thus, four of the 14 enzymes visualized (both scorable and not) included at least one duplicated gene relative to the number of genes that are ordinarily encountered in diploid angiosperms for these enzymes (Gottlieb, 1982
). This level of duplication suggests polyploid ancestry for the lineage that includes A. macrocarpa. As the majority of enzymes were not duplicated (i.e., expressed the number of loci typical for angiosperms), the presumed polyploidy would appear to be ancient, having undergone substantial gene silencing (Soltis and Soltis, 1993
). The chromosome number of A. macrocarpa is unknown, and the cytology of the genus Abronia is poorly characterized, apparently due to the difficult nature of the material. Counts that have been made suggest a haploid chromosome number in the genus of n = 45 (Snow in Munz and Keck, 1959
; Tillett, 1959
; Galloway, 1971
), consistent with a history of polyploidy. Polyploidy may well have contributed to diversification in Abronia through processes involving gene silencing as have been hypothesized to occur (Werth and Windham, 1991
; Soltis and Soltis, 1993
, 1995
).
The preponderance of loci that are in Hardy-Weinberg proportion indicates that outcrossing is the prevalent mode of breeding in A. macrocarpa. These results are consistent with hand-pollination experiments that indicate obligate outcrossing mediated by a self-incompatibility system (Williamson, Muliani, and Janssen, 1994
; Williamson, Bazeer, and Janssen, 1996
; Williamson and Bazeer, 1997
). However, the large minority (24 out of 67) of loci exhibiting heterozygote deficiencies in each population, many of them highly significant, cannot be explained by chance, nor do they imply intensive inbreeding, which should result in heterozygote deficiencies at all loci. Rather, they suggest that the A. macrocarpa populations may be genetically structured, i.e., composed of subpopulations within which mating is approximately random but between which mating may be infrequent. Such structuring is a frequently occurring attribute of plant populations (Heywood, 1991
; McCauley et al., 1996
). In structured populations, polymorphic loci with even distribution of alleles approximate Hardy-Weinberg values, but loci for which allele distribution is uneven exhibit heterozygote deficiencies. Genetic structure in A. macrocarpa populations was indicated by the hierarchical analysis that resulted in a value of FXY = 0.095 for subpopulations within populations.
The species also appears to have genetic structure at a larger spatial scale, as indicated by the mean among-population FST value of 0.272, and by UPGMA clustering that indicated a strong correlation between interpopulation relatedness and close geographic proximity. Wright (1965)
indicated that FST values in excess of 0.2 reflect low rates of gene flow among populations. Inasmuch as most (nine out of 13 loci) FST values were 0.2 or greater, these results suggest surprisingly little gene flow among A. macrocarpa populations despite their proximity within a narrow geographic range.
Gene flow in A. macrocarpa may be constrained by low vagility of seeds and pollen. Dispersal units of the genus Abronia comprise one-seeded anthocarps, consisting of achenes encased within a dry, winged structure formed by the enlarged basal portion of the calyx, apparently adapted for wind-dispersal. As suggested by its epithet, anthocarps of A. macrocarpa are among the largest in the genus, ranging from 8 to 16 mm long by 5–13 mm wide, but are thinner walled and more papery than other Abronia species (Galloway, 1972
). Wind dispersal of A. macrocarpa fruits is very limited, as the seed shadow is highly leptokurtic, with the vast majority of fruits remaining within 30 cm of the mother plant, and virtually none having been observed to disperse > 1 m (Williamson, unpublished data). Dispersal of pollen in A. macrocarpa is effected primarily by hawk moths (Sphingidae) and noctuid moths (Noctuidae) (Williamson, Muliani, and Janssen, 1994
). Although moths are capable of long-distance flights, studies on other moth-pollinated plants indicate that long-distance pollination events are rare. For example, fruit set by female Silene alba plants placed at various distances from a pollen source declined dramatically at distances exceeding 40 m (C. Richards, S. Paderewski, and D. McCauley, Vanderbilt University, personal communication).
A primary determinant of level of genetic variation is effective population size (Barrett and Kohn, 1991
). While none of the populations of A. macrocarpa are exceedingly small, there are significant differences in their estimated size, ranging from 500 to 8000 (e.g., see Table 1), with a projected estimate of between 15 000 and 25 000 individuals for the entire species. The amount of genetic variability also differed among populations (range of H = 0.122–0.179). Unexpectedly, the largest populations, LC1 and FC1, exhibited the lowest levels of genetic variability, H = 0.135 and 0.122, respectively. The two smallest populations, LC2a and RC1b, possessed respectively intermediate (H = 0.205) and high (H = 0.279) levels of genetic variability. A similar lack of correlation between population size and genetic variation has been reported in other investigations (e.g., Maki, Masuda, and Inoue, 1996
) and likely reflects overriding historical factors belied by present-day populations sizes. It is interesting to note that the two largest and least variable populations of A. macrocarpa both are relatively isolated and somewhat outlying.
The results of this study have implications for the evolutionary history, potential for continued survival, and focus of management strategies for Abronia macrocarpa. The especially high levels of genetic variation, unusual for so narrow an endemic, indicate a lack of genetic bottlenecking in this species and suggest that crosses between members of the same population would be unlikely to lead to inbreeding depression that might result from combining genetically related gametes. However, genetic variation was unevenly distributed in A. macrocarpa, as indicated by the significant structuring both within and among populations, and was not correlated with population size (P = 0.315, Spearman rank correlation). The significant degree of differentiation among populations suggests a long history of isolation, while their high levels of genetic variation indicate that they have continuously maintained sufficient numbers of individuals to deter bottleneck effects. Isolation of A. macrocarpa populations apparently results from the disjunct occurrence of the deep sandy soils that comprise suitable habitat. In that A. macrocarpa presently can be found only in a subset of such habitats in the area, it is possible that isolation has been accentuated by extinction of populations through human disturbance. The consequence of loss of any populations, all of which occur on private land, or even portions of populations, would result in a loss of genetic variation in the species. Such loss has indeed been observed in recent years due to oil well construction. Should this trend continue and reintroduction be necessary, the genetic structure of the species inevitably will be altered.
|
FOOTNOTES |
|---|
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Barrett, S. C. H., and J. R. Kohn. 1991 Genetic and evolutionary consequences of small population size in plants: implications for conservation. In D. A. Falk and K. E. Holsinger [eds.], Genetics and conservation of rare plants, 3–30. Oxford University Press, New York, NY.
Falk, D. A., and K. E. Holsinger [eds.]. 1991 Genetics and conservation of rare plants. Oxford University Press, New York, NY.
Galloway, L. A. 1971 Systematics of the North American desert species of Abronia Jussieu and Tripterocalyx (Torrey) Hooker (Nyctaginaceae). Ph.D. dissertation, Texas Tech University, Lubbock, TX.
———. 1972 Abronia macrocarpa (Nyctaginaceae): a new species from Texas. Brittonia 24: 148–149.
———. 1975 Systematics of the North American desert species of Abronia and Tripterocalyx (Nyctaginaceae). Brittonia 27: 328–347.[CrossRef][ISI]
Godt, M. J. W., and J. L. Hamrick. 1996 Genetic structure of two endangered pitcher plants, Sarracenia jonesii and Sarracenia oreophila (Sarraceniaceae). American Journal of Botany 83: 1016–1023.[CrossRef][ISI]
Gottlieb, L. D. 1977 Electrophoretic evidence and plant systematics. Annals of the Missouri Botanical Garden 64: 161–180.[CrossRef][ISI]
———. 1982 Conservation and duplication of isozymes in plants. Science 216: 373–380.
Hamrick, J. L., and M. J. W. Godt. 1989 Allozyme diversity in plant species. In A.H.D. Brown, M. T. Clegg, A. L. Kahler, and B. S. Weir [eds.] Plant population genetics, breeding and genetic resources, 43–63. Sinauer, Sunderland, MA.
———, ———, D. A. Murawski, and M. D. Loveless. 1991 Correlations between species traits and allozyme diversity: implications for conservation biology. In D. A. Falk and K. E. Holsinger [eds.], Genetics and conservation of rare plants, 75–86. Oxford University Press, New York, NY.
Heywood, J. S. 1991 Spatial analysis of genetic variation in plant populations. Annual Review of Ecology and Systematics 22: 335–355.[CrossRef][ISI]
Hickey, R. J., S. I. Guttman, and W. H. Eshbaugh. 1989 Evidence for post-translational modification of triose-phosphate isomerase (TPI) in Isoetes (Isoetaceae). American Journal of Botany 76: 215–221.[CrossRef][ISI]
Lewis, P. O., and D. J. Crawford. 1995 Pleistocene refugium endemics exhibit greater allozymic diversity than widespread congeners in the genus Polygonella (Polygonaceae). American Journal of Botany 82: 141–149.
Maki, M., M. Masuda, and K. Inoue. 1996 Genetic diversity and hierarchical population structure of a rare autotetraploid plant, Aster kantoensis (Asteraceae). American Journal of Botany 83: 296–303.[CrossRef][ISI]
McCauley, D. E., J. E. Stevens, P. A. Peroni, and J. A. Raveill. 1996 The spatial distribution of chloroplast DNA and allozyme polymorphisms within a population of Silene alba (Caryophyllaceae). American Journal of Botany 83: 727–731.[CrossRef][ISI]
McDonald, D. B., and J. L. Hamrick. 1996 Genetic variation in some plants of the Florida scrub. American Journal of Botany 83: 21–27.[CrossRef][ISI]
Munz, P. A., and D. D. Keck. 1959 A flora of California. University of California Press, Berkeley, CA.
Murphy, R. W., J. W. Sites, Jr., D. G. Buth, and C. H. Haufler. 1990 Proteins. I. Isozyme electrophoresis. In D. Hillis and C. Moritz [eds.], Molecular systematics, 44–124. Sinauer, Sunderland, MA.
Nei, M. 1978 Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89: 583–590.
Odasz, A. M., and O. Savolainen. 1996 Genetic variation in populations of the arctic perennial Pedicularis dasyantha (Scrophulariaceae) on Svalbard, Norway. American Journal of Botany 83: 1379–1385.[CrossRef][ISI]
Poole, J. M., and R. D. Riskind. 1987 Endangered, threatened, or protected native plants of Texas (update issued 1990). Texas Parks and Wildlife Department, Austin, TX.
Purdy, B. G., and R. J. Bayer. 1995 Allozyme variation in the Athabasca Sand Dune endemic Salix silicicola, and the widespread species, S. alaxensis. Systematic Botany 20: 179–190.
Ranker, T. A., S. K. Floyd, M. D. Windham, and P. G. Trapp. 1994 Historical biogeography of Asplenium adiantum-nigrum (Aspleniaceae) in North America and implications for speciation theory in homosporous pteridophytes. American Journal of Botany 81: 776–781.[CrossRef][ISI]
Rogers, J. S. 1972 Measures of genetic similarity and genetic distance. Studies in Genetics, University of Texas Publication 7213: 145–153.
Rohlf, F. J. 1988 NTSYS-pc: Numerical taxonomy and multivariate analysis system. Exeter Publishing, Setauket, NY.
Roth, J., K. Haycock, J. Gagnon, C. Soper, and J. Caldarola. 1995 StatView. Abacus Concepts, Berkeley, CA.
Smith, J. F., and T. V. Pham. 1996 Genetic diversity of the narrow endemic Allium aaseae (Alliaceae). American Journal of Botany 83: 717–726.[CrossRef][ISI]
Soltis, D. E., C. H. Haufler, D. C. Darrow, and G. J. Gastony. 1983 Starch gel electrophoresis of ferns: a compilation of grinding buffers, gel and electrode buffers, and staining schedules. American Fern Journal 73: 9–27.[CrossRef][ISI]
———, and P. S. Soltis. 1993 Molecular data and the dynamic nature of polyploidy. Critical Reviews in Plant Sciences 12: 243–273.
———, and ———. 1995 The dynamic nature of polyploid genomes. Proceedings of National Academy of Sciences, USA 92: 8089–8091.
Swofford, D., and R. Selander. 1981 BIOSYS -1. A FORTRAN program for the comprehensive analysis of electrophoretic data in population genetics and systematics. Journal of Heredity 72: 281–283.
Tillett, S. S. 1959 The maritime species of Abronia. Ph.D. dissertation, Claremont Graduate School, Claremont, CA.
U.S. Fish and Wildlife Service. 1988 Endangered and threatened wildlife and plants; determination of endangered status for Abronia macrocarpa (large-fruited sand-verbena). Federal Register 43: 37975.
Wendel, J. F., and N. F. Weeden. 1989 Visualization and interpretation of plant isozymes. In D. E. Soltis and P. S. Soltis [eds.], Isozymes in plant biology, 5–45. Dioscorides Press, Portland, OR.
Werth, C. R. 1985 Implementing an isozyme laboratory at a field station. Virginia Journal of Science 36: 53–76.
———. 1990 Zymecicles: pre-prepared frozen isozyme assays. Isozyme Bulletin 23: 109.
———. 1991 Isozyme studies on the Dryopteris "spinulosa" complex. I. The origin of the log fern D. celsa. Systematic Botany 16: 446–461.
———, and M. D. Windham. 1991 A model for divergent, allopatric speciation of polyploid pteridophytes resulting from silencing of duplicate gene expression. American Naturalist 137: 515–526.[CrossRef][ISI]
Williamson, P. S., and S. K. Bazeer. 1997 Self-incompatibility in Abronia macrocarpa (Nyctaginaceae). Southwestern Naturalist 42: 409–415.[ISI]
———, ———, and G. K. Janssen. 1996 Self-incompatibility in Abronia macrocarpa (Nyctaginaceae), an endangered Texas endemic: comparison of self- and outcross pollen tube growth. In J. Maschinski, D. H. Hammond, and H. Louella [eds.], Southwestern rare and endangered plants: Proceedings of the second conference, 171–178. General Technical Report RM-GTR-283. USDA Forest Service, Rocky Mountain Forest and Range Experiment Station, Fort Collins, CO.
———, L. Muliani, and G. K. Janssen. 1994 Pollination biology of Abronia macrocarpa (Nyctaginaceae), an endangered Texas species. Southwestern Naturalist 39: 336–341.[ISI]
Wright, S. 1965 The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 19: 395–420.[CrossRef][ISI]
———. 1969 Evolution and the genetics of populations, vol. 2, The theory of gene frequencies. University of Chicago Press, Chicago, IL.
This article has been cited by other articles:
|
|
 |
|
  E. PEREZ-COLLAZOS and P. CATALAN Palaeopolyploidy, Spatial Structure and Conservation Genetics of the Narrow Steppe Plant Vella pseudocytisus subsp. paui (Vellinae, Cruciferae) Ann. Bot., April 1, 2006; 97(4): 635 - 647. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. BATISTA and P. A. SOSA Allozyme Diversity in Natural Populations of Viola palmensis Webb & Berth. (Violaceae) from La Palma (Canary Islands): Implications for Conservation Genetics Ann. Bot., December 1, 2002; 90(6): 725 - 733. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 F. Batista, A. Banares, J. Caujape-Castells, E. Carque, M. Marrero-Gomez, and P. A. Sosa Allozyme diversity in three endemic species of Cistus (Cistaceae) from the Canary Islands: intraspecific and interspecific comparisons and implications for genetic conservation Am. J. Botany, September 1, 2001; 88(9): 1582 - 1592. [Abstract] [Full Text]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
