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1 Department of Molecular and Cell Biology, University of the Witwatersrand, Johannesburg, Private Bag 3, Wits 2050, South Africa; and 2 Department of Animal, Plant and Environmental Sciences, University of the Witwatersrand, Johannesburg, Private Bag 3, Wits 2050, South Africa
Received for publication October 15, 1998. Accepted for publication June 25, 1999.
ABSTRACT
Begonia dregei and B. homonyma (Begoniaceae), rare plants endemic to coastal forests of eastern South Africa, are two closely related species with high levels of variation among populations in the shape of leaves. Distribution of genetic variation and genetic relatedness were investigated in 12 populations of B. dregei and seven of B. homonyma using polyacrylamide gel electrophoresis. Twelve of the 15 enzyme loci examined were polymorphic, but only seven loci were polymorphic within at least one population. Genetic diversity measures indicated that the among-population gene differentiation represents >90% of the total genetic component in both species considered individually or combined. This indicated restricted gene flow, consistent with the limited dispersal abilities of Begonia generally and the ancient separation of isolated forest patches. Genetic distances among populations are much higher than usually found within species. Allozyme data provide no support for the recognition of B. dregei and B. homonyma as distinct species.
Key Words: African coastal forests • Begonia • Begoniaceae • genetic drift • genetic population structure • habitat fragmentation
Excellent models for the study
of evolutionary processes are often provided by taxa that pose the greatest
problems in systematics (Wolf, Soltis, and Soltis, 1991
). Endemic plants provide a
superb tool for studying the dynamic processes of speciation and evolution,
particularly island endemic plants (Ito and Ono, 1990
; Aradya, Mueller-Dombois, and Ranker,
1991
; Barrett,
1996
). Evidence
of most evolutionary events that formed continental biota has been lost
because such biota are so ancient (Carson, 1987
). Complex patterns of variation may blur
species boundaries and lead to taxonomic complexity.
Fragmentation of
populations may result from recent disruption of a habitat by human
activities and historical biogeographic factors, or may be due to the
naturally patchy distribution of appropriate environmental conditions.
Several recent studies have investigated the relationship between genetic
variation and the degree of isolation in plant species with fragmented
distributions (e.g., Ouborg, van Treuren, and van Damme, 1991
; van Treuren et al.,
1991
; Godt
and Hamrick, 1993
). In species with disjunct distributions,
the effects of various evolutionary processes such as genetic drift, mating
systems, and natural selection are expected to be reflected in the genetic
population structure (Lönn and Prentice, 1995
). Based on the assumption that genetic
markers such as allozymes are selectively neutral (Hamrick, Linhart, and
Mitton, 1979
),
genetic drift should influence all loci equally, whereas natural selection
might affect loci differentially. Many studies of population structure have
focussed on spatial distribution of allelic variation for allozymes
(Podolsky and Holtsford, 1995
). Hamrick and Godt
(1990)
determined associations between variation
of allozymes and life history attributes, such as mating system and life
span. Nonetheless, the degree to which population structure revealed by
allozymes is representative of the entire genome and reflects that of
quantitative traits is still unresolved (Podolsky and Holtsford,
1995
).
The present study investigates
allozyme variation in Begonia dregei Otto and Dietr. and of B.
homonyma Steudl. These two species form a highly variable and complex
group and are distinguished from each other solely on the size and shape of
leaves according to the most recent taxonomic revision (Hilliard,
1976
). They
share similar floral morphology and a caudex, or swollen stem base, which
is not known from any other species of Begonia (Smith et al.,
1986
). There is
considerable variation among populations in the size, margin, and lobing of
leaves, particularly in the smaller leaved B. dregei (Hilliard,
1976
).
Begonia dregei and B. homonyma are herbaceous perennials
endemic to subtropical forests along the east coast of South Africa, where
they occur in small, discrete populations on deeply shaded, south-facing
slopes. They are monoecious, self compatible, and pollinated by insects.
Their tiny seeds are dispersed by gravity a short distance from the parent
plant. The distinctive hemispherical caudex forms only in plants that have
grown from seed and was present on over 1000 plants observed in the wild,
suggesting that asexual reproduction does not occur. In cultivation, the
plants are easy to cross both within and between the two species, but there
is no evidence for hybridization from the distribution of variation in the
wild. Begonia homonyma is collected from the wild for use in
traditional medicine (Cunningham, 1988
), but such plant use does not involve
either cultivation or moving of plants.
The coastal forests in South
Africa consist of patches, ranging in size from less than 1 to 1787 ha
(Cooper and Swart, 1992
), separated by grassland, much like an
archipelago of islands. There are several hypotheses about the processes
that have led to this pattern. The present distribution of forests might
have resulted from human land use, involving grazing and burning over the
past 300 yr, particularly the last century (Granger, 1984
; Acocks, 1988
). An alternate hypothesis
is that the pattern is ancient and due to environmental factors including
increasing aridity (Feeley, 1986
; Rutherford and Westfall, 1986
; Geldenhuys,
1994
). The
flora of coastal forests of eastern Africa, to the north of the range of
B. dregei and B. homonyma, includes many endemic species
with disjunct distributions that may be relicts from the breakup of the Pan
African rainforests that started 17–18 million yr ago (Burgess,
Clarke, and Rodgers, 1998
).
This paper reports the results of an electrophoretic survey to examine genetic variation within and divergence among populations. The objectives were to: (1) describe the distribution of genetic variation, using allozymes, within and among populations of B. dregei and B. homonyma; (2) investigate genetic relatedness among populations in both species; (3) determine the relationship, if any, between genetic distance and geographic proximity of the populations; and (4) investigate whether patterns of variation in allozymes are consistent with the current taxonomic treatment. The study also explores the extent to which the structure of genetic variation of forest floor taxa can elucidate the history of the habitat.
MATERIALS AND METHODS
Study sites
and collection of samples
Plant material was collected throughout
the known geographical ranges of B. dregei and B.
homonyma (Hilliard, 1976
) which occur in only two provinces along
the east coast of South Africa. In KwaZulu/Natal, populations occur further
inland than in the Eastern Cape, where they are restricted to northern and
central regions of the province (Fig.
1). A total of 19 populations, including 12 of B.
dregei and seven of B. homonyma, covering most of the
variation in leaf shape in the group, was sampled (Table 1). We attempted to collect 20 individuals
from each population, but several places had fewer than 20 plants, notably
at the mouth of the Mtentu River, where an intensive search produced four
plants. Populations occurred in limited areas, and population size was
estimated by counting all plants observed. The names of forests or rivers
with which populations were associated were used to refer to them; the
populations are numbered from north to south for each species (Table 1).
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). Fresh leaves were homogenized in a
concentrated alkaline buffer made of 1.0 mol/L tris-HCl pH 8.9, 20%
w/v sucrose, 50 mg/mL PVP 40 (polyvinylpyrolidone), 2.5 mg/mL DIECA
(diethyldithiocarbamic acid), 2.5 mg/mL DTT (dithiotreitol), and 5 µL/mL
Triton X100. Bromophenol blue was added as tracking dye. Gels were composed
of 5% acrylamide (5% was bisacrylamide) and were 140 mm wide,
143 mm long, and 1.5 mm thick. Several buffer systems were tested to
determine which buffer gave the best resolution for each enzyme locus.
Tris-borate pH 8.7 (0.5 mol/L tris and 0.2 mol/L boric acid) and
histidine-MOPS pH 6.6 (0.25 mol/L histidine and 0.3 mol/L MOPS) continuous
buffer systems (McLellan, 1982
) were selected. Buffers were diluted to a
ratio of 1:9 for both electrode and gel buffers. The histidine-MOPS buffer
system was used for phosphoglucoisomerase (Pgi),
phosphoglucomutase (Pgm), fructosebiphosphate aldolase
(Fba), glucose-6-phosphate dehydrogenase (G6pd),
6-phosphogluconate dehydrogenase (6Pgd), and malate dehydrogenase
(Mdh). Peroxidase (Per), superoxide dismutase
(Sod), glutamic dehydrogenase (Gldh), malic enzyme
(Me), formic dehydrogenase (Fdh), and esterase
(Est) were best resolved in the tris-borate buffer system. Enzymes
were stained using assay protocols modified from Wendel and Weeden
(1989)
. Loci and alleles were numbered
sequentially in order of decreasing anodal mobility. Allelism was tested
with crosses between plants from eight of the populations; in all cases,
inheritance of allozyme bands proved to be Mendelian (Ntloko,
1997
).
Analysis of allozyme
variation within populations
Allele frequencies for each population
were calculated from isozyme phenotypes. A locus was considered polymorphic
if it had more than one allele. Population variation within and over all
populations was quantified by calculating the following metrics from allele
frequencies: percentage of loci polymorphic (P), number of alleles per
locus (A), and expected (He) and observed
(Ho) frequencies of heterozygotes. Polymorphism and
allelic diversity have been shown to be reliable indicators of population
structure and can show the effects of bottlenecks and genetic drift (Nei,
1978
; Leberg,
1992
; Thomas and
Bond, 1997
).
Analysis of allozyme
variation among populations
The distribution of genetic variation
within and among populations was determined by calculating Wright's
(1951)
F statistics (Fst, Fis and
Fit) from variance components based on Weir and
Cockerham's (1984) estimators 
, f, and
F, using the program FSTAT (Goudet, 1995
), which calculates unbiased estimates,
standard deviations, and levels of significance. Values equal to 0 occur in
a randomly mating population and those equal to 1 in a selfing population,
as these F statistics represent correlations between uniting
gametes (Wright, 1951
). Variance components of
Fit and Fis measure heterozygosity
of an individual relative to the total population and its subpopulations,
respectively; Fst is a measure of genetic
differentiation among populations (Wright, 1951
; Weir and Cockerham, 1984
; Weir, 1996
).
Cluster
analysis and genetic divergence among populations
The genetic
divergence between populations was estimated from their genetic distances
(D) obtained from Nei's (1978)
index of genetic similarity
calculated using Genetic Data Analysis (GDA), a computer program written by
Lewis and Zaykin (1997). Dendrograms for both species separately
and together were constructed using the UPGMA (unweighted pair group method
using arithmetic means) algorithm using NTSYS-PC (Rohlf, 1993
). The relationship between
distances among populations and levels of genetic differentiation were
determined with Mantel tests to compare matrices and by using
Slatkin's (1993)
isolation by distance program. Plotting
of 
(an estimate of gene flow)
instead of genetic distance against geographic distances and then
performing a regression analysis between the two variables has many
advantages, ranging from increased resolution power to nonbiased estimates
(Slatkin, 1993
).
RESULTS
Allelic
variation
Twelve enzymes, presumably coded by 15 loci, were scored:
Fba, Fdh, Gldh, G6pdh, Mdh, Me, Per, Pgi, and 6Pgd each
exhibited one locus while Est, Pgm and Sod exhibited two
loci. Twelve of these loci were polymorphic over all populations of both
species, and seven had more than one allele within at least one population
(Appendix). In all the enzyme loci, consistent banding patterns with the
same subunit structure for each enzyme were observed throughout all the
populations. The number of isozymes detected for all of the enzymes was the
same as those commonly found in diploid plants (Gottlieb and Weeden,
1979
), and
there was no evidence for duplication of genes in any enzyme system
(Ntloko, 1997
).
These observations together with the known small chromosome number of these
plants (Legro and Doorenbos, 1969, 1971
) are consistent with
diploidy.
Genetic diversity
Four of the seven
populations of B. homonyma had no variation at any locus; the
others averaged 1.07–1.2 alleles per locus, with an average over all
populations of 1.07 (Table 2). These
values were lower than those found in B. dregei, which ranged
between 1.07 and 1.27, with an average of 1.16 alleles per locus.
Percentage of polymorphic loci ranged from 0 to 20%, with an average
of 5.7% among the seven populations of B. homonyma. Begonia
dregei had an average of 13.9% loci that were polymorphic,
ranging from 7 to 27%. The values of these measures of genetic
diversity were low relative to averages found within populations of other
species of plants (Hamrick and Godt, 1996
). Across all populations of both species,
80% of loci were polymorphic, with an average of 3.5 alleles per
locus; these values were higher than the averages reported for variation
within species (Hamrick and Godt, 1996
).
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Observed and expected
heterozygosities, Ho and He, varied
among populations, with no value >0.10 for either species (Table 2). Intrapopulation variation was higher in
B. dregei than in B. homonyma. On average, the expected
heterozygosity (He = 0.043) was lower than that
reported for endemic species (He = 0.063) by
Hamrick and Godt (1996)
, which in general are expected to have
much less genetic variation than more widespread species. Significant
departure from Hardy Weinberg expectations was found for most loci
(Table 2), with a deficiency of
heterozygotes. The negative fixation index values may indicate an outbred
population, although this may be a function of sampling error since those
populations were polymorphic at only one locus (Table
2). The four populations of B. homonyma, 13, 15, 16,
and 18, that had no polymorphism at all, had a fixation index of 1.00; one
other population of B. homonyma (17) and three of B.
dregei (3, 4, and 5) had fixation indexes above 0.60. The mean
fixation index for B. dregei was 0.277 and for B.
homonyma was 0.562, indicating that B. homonyma is more
highly inbred than B. dregei.
Relatedness
between populations
Nei's genetic distances in both B.
dregei and B. homonyma (Table
3) were high compared to those usually found for populations
within a species. The mean genetic distances were 0.640 and 0.520,
respectively. Clustering of populations based on D shows that only
one pair of populations, 13 and 19, in B. homonyma cluster closely
together (Fig. 2a, b), but
others do not show an overall pattern of clear groups (Fig. 2a). When both species are
considered together, B. dregei and B. homonyma do not
form separate groups (Fig.
2c). The highest genetic distance values of 1.00 were found
within B. dregei and B. homonyma, as well as in the
comparisons between the two species (Table
3).
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against
the log of geographic distance showed that these populations did not fit a
model of isolation by distance (P = 0.15) (Fig. 3). Negative values of log
mean that the true values of
Fst for those pairs of locations were extremely high.
Presence of unique alleles and high rates of fixation at some loci
contributed to the low values of . The linear distance between populations is unlikely to be the route of dispersal; it is more likely that gene flow would occur along watercourses, where forests are more or less continuous. However, the four populations from the Umzimvubu River (7, 8, 17, and 18) were not similar to each other, nor were the two from the Umtamvuna River valley (3 and 14).
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). These estimates for all three metrics were higher than those reported for other groups of plants (Linhart et al., 1981
; Guries and Ledig, 1982
; Alvarez-Buylla and Garay, 1994
).
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The pattern of distribution of allozyme variation in both species includes low genetic variation within populations and pronounced divergence among populations, consistent with the prediction for the effects of limited gene flow among small populations that have been separated for a long time. Heterozygote deficiency might be due to self-fertilization in these self-compatible plants or inevitable mating between relatives in small populations. Begonia dregei and B. homonyma occur in populations with total numbers ranging from four to a few hundred individuals; B. homonyma has both less genetic variation and smaller populations than B. dregei. Over the summer flowering season, from 10 to 50% of the individuals in a population may produce flowers, and not all of those will produce seed (data not shown).
There is evidence for little, if any, gene flow among populations of either B. dregei or B. homonyma or between the species. Unique alleles and the high values of Fst are indicators that there is little exchange of genes among populations, even those that are a few kilometres apart within the same forest. The structuring of variation, with very high average values of Fst, is above average even for selfing plants. Populations 8 and 18 in the same forest patch within a kilometre of each other exhibit very little gene flow between them.
The high values of Fst and genetic distance compared to those found in other surveys of plant population structure might possibly be due to greater resolution of variants by polyacrylamide gel electrophoresis rather than the more routinely used starch gels. The first estimates of population heterozygosities were based on polyacrylamide gels (Hubby and Lewontin, 1966
), and estimates based on starch gels do not differ substantially. Only a few studies have compared the resolution of the different types of gels with the same samples. A few more electrophoretic variants of human blood proteins were detected on starch rather than on polyacrylamide gels (McLellan, Jorde, and Skolnick, 1984
). Comparison of an enzyme from Drosophila showed that each type of gel revealed unique variants, and that there were differences between laboratories in the resolution of starch gels (Coyne et al., 1979
). Therefore, the resolution of allelic variants on polyacrylamide gels performed in this study is likely to be within the range of results obtained from starch gels.
Limited potential for dispersal is likely to contribute to the low rates of gene flow between populations. Ågren and Schemske (1993)
also found very low outcrossing rates and substantial inbreeding in Begonia hirsuta Aubl. and Begonia semiovata Liebm. due to lack of pollen transfer and short-distance seed dispersal. The distribution of variation among populations of B. dregei and B. homonyma may in part be attributable to a lack of seed dispersal among populations. The lack of correlation between geographic and genetic distances might be a result of genetic drift, over a long period of time, obscuring any geographic pattern in the distribution of genetic variation. The lack of similarity between populations along the same river is consistent with a lack of gene flow as well.
The distinction between B. dregei and B. homonyma, based on the size and shape of leaves (Hilliard, 1976
), is not supported by the allozyme data. Most populations appear too divergent for allozymes to be informative about relatedness and evolutionary history, although allozymes are effective indicators of gene flow in these plants. The high differentiation among populations, with mean genetic distances of over 0.50 in both species, suggests that perhaps additional taxa should be recognized. There is heterogeneity within both B. dregei and B. homonyma in leaf shape and size (Hilliard, 1976
; McLellan, 2000). The two populations with the lowest value of genetic distance, populations 13 and 19, despite their geographic separation, are similar in terms of leaf shape and other aspects of morphology. For the remainder of the group, perhaps additional information from morphology, as well as other molecular data, will clarify an appropriate taxonomic framework. Some populations with similar leaf shapes and near each other geographically differ greatly in allozymes (populations 8 and 9 in B. dregei; populations 14, 15, and 16 in B. homonyma). The lack of concordance between leaf shape and allozymes suggests a lack of linkage between genes for the two sets of traits, so that they could have evolved independently of each other. It is possible that leaf shape and size are influenced by selection, and allozymes, which are usually assumed to be selectively neutral, are more affected by genetic drift, but we do not have data to distinguish selection from drift for either source of data.
Although many plant species have declined rapidly during the past few hundred years due to human activities, many others owe their population disjunctions to climatic changes during the quaternary (Sage and Wolff, 1986
). The small patches of coastal forest in which B. dregei and B. homonyma occur are apparently remnants of a once continuous forest, which began to break up in the Miocene (Burgess, Clarke, and Rodgers, 1998
). The distribution of genetic variation in B. dregei and B. homonyma is consistent with the ancient separation of forest patches, limiting the dispersal of plants that are specific to forest habitats.
By current categories for threatened taxa (IUCN, 1994
), neither B. dregei nor B. homonyma would be considered threatened. We have found 50 populations; there are likely to be at least twice that many. Although population sizes are small, with an average of <20 mature individuals, the total number of individuals is reasonably high. Most of the forests are well protected, and we have seen only a few cases of recent habitat destruction. Begonia homonyma is collected for traditional medicine in KwaZulu/Natal (Cunningham, 1988
; N. Crouch, personal communication, 1998). The probability of extinction of any single population is high, since the populations are so small (Hughes, Daily, and Ehrlich, 1997
). Almost every one of the populations that we have considered here is unique in its combination of molecular and morphological traits. It is highly likely that additional species from African coastal forests and other habitats with this sort of island distribution and limited dispersal abilities will show similar patterns of variation. This type of variation demonstrates that conservation efforts should be oriented below the level of species, especially in highly variable taxa.
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1 The authors thank David Wopula and Jo Arkell for assistance with the collection of plants; and M. Slatkin, P. Lewis, and J. Goudet for programs. This study was supported by grants from the South African Foundation for Research Development (FRD) and Mellon Foundation. 
2 Author for correspondence: Department of Molecular and Cell Biology, University of the Witwatersrand, Johannesburg, Private Bag 3, Wits 2050, South Africa. Phone: + 27 11 716 2178; FAX: + 27 11 403 1733; e-mail: 108mal{at}cosmos.wits.ac.za
LITERATURE CITED
Acocks, J. P. H. 1988 Veld types of South Africa. Memoirs of the Botanical Survey of South Africa 28: 1–146.
Ågren, J., and D. W. Schemske. 1993 Outcrossing rate and inbreeding depression in two annual monoecious herbs, Begonia hirsuta and B. semiovata. Evolution 47: 125–135.
Alvarez-buylla, E. R., and A. A. Garay. 1994 Population genetic structure of Crecropia obtusifolia, a tropical tree species. Evolution 48: 437–453. [CrossRef][Web of Science]
Aradya, K. M., D. Mueller-dombois, and T. A. Ranker. 1991 Genetic evidence for recent and incipient speciation in the evolution of Hawaiian Metrosideros (Myrtaceae). Heredity 67:129–138.
Barrett, S. H. C. 1996 The reproductive biology and genetics of island plants. Philosophical Transactions of the Royal Society of London 351: 725–733. [CrossRef]
Burgess, N. D., G. P. Clarke, and W. A. Rodgers. 1998 Coastal forests of eastern Africa: status, endemism patterns and their potential causes. Biological Journal of the Linnean Society 64: 337–367.
Carson, H. L. 1987 The processes whereby species originate. BioScience 37: 715–720. [CrossRef][Web of Science]
Cooper, K. H., and W. Swart. 1992 Transkei forest survey. Wildlife Society of Southern Africa, Durban, South Africa.
Coyne, J. A., W. F. Eanes, J. A. M. Ramshaw, and R. K. Koehn. 1979 Electrophoretic heterogeneity of 
-glycerophorphate dehydrogenase among many species of Drosophila. Systematic Zoology 28: 164–175.
Cunningham, A. B. 1988 An investigation into the herbal medicine trade in Natal/KwaZulu. Institute of Natural Resources, University of Natal, Pietermaritzburg, South Africa.
Feeley, J. M. 1986 The distribution of iron age farming settlement in Transkei: 470–1870. Master's thesis, University of Natal, Pietermaritzburg, South Africa.
Geldenhuys, C. J. 1994 Bergwind fires and the location pattern of forest patches in the southern Cape landscape, South Africa. Journal of Biogeography 21: 49–62.
Godt, M. J., and J. L. Hamrick. 1993 Genetic diversity and population structure in Tradescantia hirsuticaulis (Commelinaceae). American Journal of Botany 80: 959–966. [CrossRef][Web of Science]
Gottlieb, L. D., and N. F. Weeden. 1979 Gene duplication and phylogeny in Clarkia. Evolution 33: 1024–1039. [CrossRef]
Goudet, J. 1995 FSTAT (Version 1.2): a computer program to calculate F-statistics. Journal of Heredity 86: 485–486.
Granger, J. E. 1984 Fire in forests. In P. de V. Booysen and N. M. Tainton [eds.], Ecological effects of fire in South African ecosystems, 177–197. Springer-Verlag, Berlin, Germany.
Guries, R. P., and F. T. Ledig. 1982 Genetic diversity and population structure in pitch pine (Pinus rigida Mill.). Evolution 36: 387–402. [CrossRef][Web of Science]
Hamrick, J. L., and M. J. W. Godt. 1990 Allozyme diversity in plant species. In H. D. Brown, M. T. Clegg, M. A. Kahler, and B. S. Weir [eds.], Plant population genetics, breeding and genetic resources, 43–63. Sinauer, Sunderland, Massachusetts, USA.
———, and ———. 1996 Conservation genetics of endemic plant species. In J. C. Avis and J. L. Hamrick [eds.], Conservation genetics: case histories from nature, 281–304. Chapman and Hall, New York, New York, USA.
Hamrick, J. L., Y. B. Linhart, and J. B. Mitton. 1979 Relationship between life history characteristics and electrophoretically detectable genetic variation in plants. Annual Review of Ecology and Systematics 10: 173–200.
Hilliard, O. M. 1976 Begoniaceae. In J. H. Ross [ed.], Flora of Southern Africa, vol. 22, 136–144. Botanical Research Institute, Department of Agriculture Technical Services, Pretoria, South Africa.
Hubby, J., and R. C. Lewontin. 1966 A molecular approach to the study of genic heterozygosity in natural populations. I. The number of alleles at different loci in Drosophila pseudoobscura. Genetics 54: 577–594.
Hughes, J. B., G. C. Daily, and P. R. Ehrlich. 1997 Population diversity: its extent and extinction. Science 278: 689–692.
Ito, M., and M. Ono. 1990 Allozyme diversity and the evolution of Crepidiastrum (Compositae) on the Bonin (Ogasawara) Islands. Tokyo Botanical Magazine 103: 449–459.
IUCN. 1994 IUCN Red list categories. IUCN, Gland, Switzerland.
Leberg, P. L. 1992 Effect of population bottlenecks on genetic diversity as measured by allozyme electrophoresis. Evolution 46: 477–494. [CrossRef][Web of Science]
Legro, R. A. H., and J. Doorenbos. 1969 Chromosome numbers in Begonia. Netherlands Journal of Agricultural Science 17: 189–202.
———, and ———. 1971 Chromosome numbers in Begonia, 2. Netherlands Journal of Agricultural Science 19: 176–183.
Lewis, P., and D. Zaykin. 1997 Genetic data analysis, version 1 d 10, University of New Mexico, Albequerque, New Mexico, USA.
Linhart, Y. B., J. B. Mitton, K. B. Sturgeon, and M. L. Davis. 1981 Genetic variation in space and time in a population of ponderosa pine. Heredity 46: 407–426. [Web of Science]
Lönn, M., and H. C. Prentice. 1995 The allozyme structure and leaf shape variation in isolated range-margin populations of the shrub Hippocrepis emerus (Leguminosae). Ecography 18: 276–285. [CrossRef][Web of Science]
McLellan, T. 1982 Electrophoresis buffers for polyacrylamide gels at various pH. Analytical Biochemistry 126: 94–99. [CrossRef][Web of Science][Medline]
———. 2000 Geographic variation and plasticity of leaf shape and size in Begonia dregei and B. homonyma (Begoniaceae). Botanical Journal of the Linnean Society 132: 79–95. [CrossRef]
———, L. B. Jorde, and M. H. Skolnick. 1984 Genetic distances between the Utah Mormons and related populations. American Journal of Human Genetics 36: 836–857. [Web of Science][Medline]
Nei, M. 1978 Estimation of average heterozygosity and genetic distance from small numbers of individuals. Genetics 89: 330–590.
Ntloko, T. S. S. 1997 Molecular variation in Begonia dregei. M.Sc. Thesis, University of the Witwatersrand, Johannesburg, South Africa.
Ouborg, N. J., R. van Treuren, and J. M. M. van Damme. 1991 The significance of genetic erosion. II. Morphological variation and fitness components in populations of varying size of Salvia pratensis L. and Scabiosa columbaria L. Oecologia 86: 359–367. [CrossRef][Web of Science]
Podolsky, R. H., and T. P. Holtsford. 1995 Population structure of morphological traits in Clarkia dudleyana I. Comparison of FST between allozymes and morphological traits. Genetics 140: 733–744. [Abstract]
Rohlf, F. J. 1993 NTSYS-pc. Numerical taxonomy and multivariate analysis system, version 1.80. Exeter Software, Setauket, New York, USA.
Rutherford, M. C., and R. H. Westfall. 1986 Biomes of southern Africa—an objective categorization. Memoirs of the Botanical Survey of South Africa 54: 1–98.
Sage, R. D., and J. O. Wolff. 1986 Pleistocene glaciations, fluctuating ranges, and low genetic variability in a large mammal (Ovis dalli). Evolution 40: 1092–1095. [CrossRef][Web of Science]
Slatkin, M. 1993 Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47: 264–279. [CrossRef][Web of Science]
Smith, L. B., D. C. Wasshausen, J. Golding, and C. E. Karegeannes. 1986 Begoniaceae. Part I: illustrated key, Part II: annotated species list. Smithsonian Institution Press, Washington, DC, USA.
Thomas, J. C., and W. J. Bond. 1997 Genetic variation in an endangered cedar (Widdringtonia cedarbergensis) versus two congeneric species. South African Journal of Botany 63: 133–140. [Web of Science]
van Treuren, R., R. Bijlsma, W. Van Delden, and N. J. Ouborg. 1991 The significance of genetic erosion in the process of extinction. I. Genetic differentiation in Salvia pratensis and Scabiosa columbaria in relation to population size. Heredity 66: 181–189. [Web of Science]
Weir, B. S. 1996 Genetic data analysis II. Methods for discrete population genetic data. Sinauer, Sunderland, Massachusetts, USA.
———, and C. C. Cockerham. 1984 Estimating F-statistics for the analysis of population structure. Evolution 38: 1358–1370. [CrossRef][Web of Science]
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. Chapman and Hall, Washington, DC, USA.
Wolf, P. S., P. S. Soltis, and D. E. Soltis. 1991 Genetic relationships and patterns of allozymic divergence in the Ipomopsis aggregata complex and related species (Polemoniaceae). American Journal of Botany 78: 515–526. [CrossRef][Web of Science]
Wright, S. 1951 The genetic structure of populations. Annals of Eugenetics 15: 323–354.
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