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The Journal of Heredity 2001:92(1)
© 2001 The American Genetic Association 92:65-70

Allozyme Variation of Cyclobalanopsis championii (Fagaceae), a Narrowly Distributed Species in Southern Taiwan

Y.-P. Cheng, C.-T. Chien, H.-W. Chen, and T.-P. Lin

From the Taiwan Forestry Research Institute, 53 Nan-Hai Road, Taipei, Taiwan (Cheng, Chien, and Chen) and Department of Botany, National Taiwan University, Roosevelt Road Section 4, Taipei, Taiwan (Lin).


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Allozyme genetic variability in five natural populations of Cyclobalanopsis championii (Fagaceae) in Taiwan was investigated using 12 loci from 9 enzyme systems. The average values of parameters describing within-population variation, expected heterozygosity (He = 0.151), the percentage of polymorphic loci per individual (P = 50%), the average number of alleles per locus (A = 1.7), effective number of alleles per locus (Ae = 1.25), and the average number of alleles per polymorphic loci (AP = 2.2) are comparable to those of other long-lived woody plants. The overall fixation index (Fis = 0.208) indicates a significant deficiency of heterozygotes at the population level. Allelic frequency deviation from Hardy–Weinberg equilibrium was found for different loci in different populations. An exact test for population differentiation using the Tools for Population Genetic Analyses program also indicates that allelic frequencies among populations are significantly different (P < .001). Among-population variation, Gst, accounted for 9.2% of the total heterozygosity. The population at Shouchia and the southernmost population Nanjenshan had higher inbreeding coefficients (0.177 and 0.153, respectively) than did the northern populations. Genetic drift is supported by the observations of the variance components of linkage disequilibrium and a large proportion of loci in Nanjenshan and Shouchia that show pairwise locus disequilibrium. We believe continuous genetic drift in the southern populations will increase genetic divergence among populations of C. championii in Taiwan. Significant correlation was found between elevation and expected heterozygosity. We therefore inferred that temperature is the most important ecological factor to influence the genetic diversity of C. championii.


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Cyclobalanopsis championii, a large tree in the Fagaceae family, is restricted to the Hengchun Peninsula in southern Taiwan (Liao 1996) (Figure 1). It also grows in Guangdong, Hong Kong, and Hainan Island of southern China. Thus this species has a discontinuous distribution, as do many other species in Taiwan, for example, Myrica adenophora (Cheng et al. 2000) and Castanopsis fabri. C. championii grows predominantly on windy slopes (usually northeastern aspect) close to the ridge and is not present on the other side of the same mountain. The leaves are thick, waxy, covered with hairs at a young age, but only the lower surface is covered with trichomes at maturity. It shows an outcrossing wind-breeding system. Since the habitat is narrowly restricted, C. championii has been listed as a nonendemic rare species (Su 1980). Based on phytogeography, the Hengchun Peninsula can be separated from the rest of Taiwan by drawing a line through Fengliao, Pingtung County (22°21'39 N, 120°35'16 E) and Tawu, Taitung County (22°21'41 N, 120°54'02 E) (Figure 1). This line separates the subtropical from the tropical zone (Shen 1997). C. championii is restricted to the south of this line.



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  		Figure 1.. Map of Taiwan with an enlargement of the Hengchun peninsula.

 
There are 58 species and varieties in seven genera of Fagaceae in Taiwan (Liao 1996). Most of these species occur at elevations above 1000 m, and the elevation range of 1500–2500 m in Taiwan is characterized as evergreen oak forest (Hsieh et al. 1994). We consider Fagaceae to represent the temperate elements, which were prevalent in the lowlands during the last glacial period. It was reported that the coldest period in Taiwan might have been 50,000–60,000 BP, during the prevailing Tali glacial age (Tsukada 1966). Indeed, based on the palynological record, Quercus spp. dominated the lowlands of Taiwan from 10,000 to 50,000 BP and has since declined to the low number of species seen at the present time (Tsukada 1967). The pollen density of another genus, Castanopsis, has also declined since 10,000 years ago. It is believed that temperate species of Fagaceae in Taiwan have retreated to higher elevations or have migrated to the north. C. championii, however, is one of the few species occurring at the lower elevations and restricted to the southern part of Taiwan.

To obtain a general picture of genetic variation of C. championii throughout its range on the Hengchun Peninsula we used allozyme analysis to investigate the genetic diversity and differentiation among five populations. We suggest that a warm climate has reduced the genetic diversity of populations of C. championii, especially the southernmost ones, and genetic drift has occurred to some extent.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Sampling
A total of 219 samples of C. championii were collected from five natural populations—Shouchia (N = 60), Nanjenshan (N = 56), Kaoshihfo (N = 41), Lilungshan (N = 46), and Tahanshan (N = 16) (Figure 1). Populations at Kaoshihfo and Nanjenshan grow on windy slopes at elevations of 300–400 m; the population at Shouchia is found between 300 and 600 m; the Lilungshan population grows on windy slopes at elevations between 600 and 1100 m. The population at Tahanshan has a wider altitudinal distribution compared to the other populations, and was found between 800 and 1400 m. The individuals at Tahanshan are scattered among many tree species and collection was difficult in this site, thus only 16 individuals were investigated. Young leaves were collected during August and September 1997, sealed in polyethylene bags, and stored overnight in a refrigerator at 4°C. Samples were ground with extraction buffer according to procedures described in Feret (1971), and absorbed onto Whatman 3MM filters (4 mm x 12 mm). Paper strips were arranged in a plastic Petri dish and stored at -70°C until use.

Electrophoresis
Electrophoresis and staining methods followed the procedure described in Cheliak and Pitel (1984). Buffer system H was used to resolve isocitrate dehydrogenase (IDH, EC 1.1.1.42), malate dehydrogenase (MDH, EC 1.1.1.37), phosphogluconate dehydrogenase (6PGD, EC 1.1.1.44), phosphoglucomutase (PGM, EC 5.4.2.2), and shikimate 5-dehydrogenase (SKDH, EC 1.1.1.25). Buffer system B was used to resolve carboxylesterase (EST, EC 3.1.1.1), glucose-6-phosphate isomerase (PGI, EC 5.3.1.9), meandione reductase (MR, EC 1.6.99.2), and diaphorase (DIA, EC 1.6.4.3.). Putative loci were designated sequentially, with the most anodally migrating isozyme designated as 1, the next 2, and so on. Likewise, alleles were designated sequentially with the most anodally migrating alleles designated a, the next b, and so on.

Data Analysis
Allele frequencies in each population were calculated for the 12 loci of the nine enzyme systems. BIOSYS-2 (from William C. Black IV, Department of Microbiology, Colorado State University) which is a modified version of the BIOSYS-1 program by Swofford and Selander (1981), was used to estimate the following genetic parameters: mean number of alleles per locus (A), effective number of alleles per locus (Ae), mean number of alleles per polymorphic loci (AP), percentage polymorphic loci (P) (99 % criterion), and observed (Ho) and expected (He) heterozygosities. Wright's F coefficient was used to estimate the deviation of observed heterozygosity from the Hardy–Weinberg proportion for each polymorphic locus in each population (Nei 1977; Wright 1965). Conformance of the investigated populations to the Hardy–Weinberg equilibrium was estimated using the exact test (Haldane 1954) employing the Markov chain method (Guo and Thompson 1992) (TFPGA, version 1.3, from Mark P. Miller, Northern Arizona University). Total genetic diversity (Ht), genetic diversity within populations (Hs), and the proportion of genetic diversity among populations (Gst) were computed using the GENISO program by Alfred E. Szmidt and X.-R. Wang (Department of Forest Genetics and Plant Physiology, SLU, Sweden). The TFPGA program was used to conduct cluster analysis on genetic distance via the unweighted pairwise group method using arithmetic averages (UPGMA) (Sneath and Sokal 1973) which gives the confidence interval. Linear regressions were performed to study the relationships between the expected heterozygosities (He) and the range in latitude or elevation of the five populations.

Linkage disequilibrium analysis was carried out separately on single populations (Weir 1979). Variance components of linkage disequilibrium were calculated according to Ohta (1982a) and computed using Popgene version 1.1 (from F. C. Yeh, University of Alberta, and T. Boyle, Center for International Forestry Research). Parameters of variance were Dis2 (expected variance of linkage disequilibrium within a population), Dst2 (variance of the correlation of genes of the two loci of different gametes of one population relative to that of the total population), D'is2 (variance of the correlation of two loci of one gamete in a population relative to that of the total population), and Dit2 (the total variance of disequilibrium, the correlation of two loci of a gamete in a population relative to that of different gametes of the total population).


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Twelve loci in nine enzyme systems tested could be resolved clearly enough for genetic diversity analysis: Pgi-1, Pgi-2, 6Pgd-1, 6Pgd-2, Pgm, Idh, Mdh-2, Mdh-3, Skdh, Est, Mr-2, and Dia-2. Among them, Pgi-1, Pgi-2, 6Pgd-2, Pgm, Idh, Skdh, Est, Mr-2, and Dia-2 were polymorphic (99% criterion) in at least one population (Table 1). Mdh-2, Mdh-3, and 6Pgd-1 were monomorphic. Mdh-1, Mr-1, Dia-1, Per-1, Per-2, and Per-3 were suspected to be polymorphic but were not clear enough to include for analysis. Mr-2b and Dia-2b were rare alleles found in the Nanjenshan population only (Table 1).


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  		Table 1.. Allelic frequencies for polymorphic loci in populations of C. championii

 
Genetic Diversity
At the population and species level, C. championii had moderate genetic diversity (Table 2). The expected heterozygosity (He) was 0.151 and 0.166, respectively. The species showed a considerable deficiency of heterozygotes, as can be seen in Table 2. Populations at Nanjenshan and Kaoshihfo were less genetically diverse than the other populations, and Tahanshan has higher levels of genetic diversity. Significant correlations were found between He and latitude (r = 0.86, P < .05) (Figure 2), and between He and elevation (r = 0.89, P < .05).


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  		Table 2.. Genetic variability for each population and at the species level of C. championii

 


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  		Figure 2.. Relationships of expected heterozygosity (He) with latitude and expected heterozygosity with elevation range for five populations of C. championii. For the elevation range of each population please see "Materials and Methods". Population 1, Shouchia; 2, Nanjenshan; 3, Kaoshihfo; 4, Lilungshan; 5, Tahanshan.

 
Genetic Differentiation
Wright's F statistics showed that deficiencies of heterozygotes exist for six (the value greater than 0) out of nine loci at the population (mean Fis = 0.208) and the species level (mean Fit = 0.278) (Table 3). While testing for Hardy–Weinberg equilibrium in loci within a population employing the Markov chain method (Guo and Thompson 1992), it was found that there were deviations for different loci in different populations [P(HW)]. Using the exact test for population differentiation (Raymond and Rousset 1995, in the TFPGA program), it was found that differences among all populations were significant [overall P(DAP) < 0.001; Table 3]. Gst is the measure of absolute genetic differentiation, with an average of 0.092, which is significantly different from zero (P = .005) as tested using Weir and Cockerham (1984) estimators of F statistics ({theta}) (FSTAT program). Thus about 90% of the total variation resides within populations. Genetic distance for all pairs of populations ranged from 0.0047 to 0.0402, with an average of 0.0220 (TFPGA). The UPGMA dendrogram produced clusters of populations (Figure 3). The confidence between the clades varied from 46 to 100 bootstrap replicates. The correlation between genetic distance and geographic distance was significant (r = 0.66, P < .05).


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  		Table 3.. F statistics, G statistics, and exact test for polymorphic loci in five populations of C. championii

 


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  		Figure 3.. Dendrogram generated by UPGMA method using Nei's (1978) unbiased minimum distance. The confidence level between clades resulted from bootstrapping 1000 permutations. Population 1, Shouchia; 2, Nanjenshan; 3, Kaoshihfo; 4, Lilungshan; 5, Tahanshan.

 
Linkage disequilibrium analysis was carried out for single populations, and pairwise locus disequilibrium was found for 6Pgd-2c/Est-1a and 6Pgd-2c/Est-1b (P < .05) at Shouchia. MR-2a/Dia-2a, MR-2a/Dia-2b, MR-2b/Dia-2a, and MR-2b/Dia-2b (P < .01) were found to be in disequilibrium at Nanjenshan. No linkage disequilibrium was observed for pairwise loci in the populations of Kaoshihfo, Lilungshan, or Tahanshan.

We analyzed 66 two-locus pairs for variance components of linkage disequilibrium. Without exception, D'is is larger than D'st for every pair of loci, and Dst is larger than Dis. According to Ohta's prediction (1982a,b), the relationships D'is2 > D'st2 and Dst2 > Dis2 hold if genetic drift is responsible for linkage disequilibrium but not epistatic selection. Genetic drift causes random fluctuations of gamete frequencies in the population, and hence increases the variance of the linkage disequilibrium coefficient. Here we surmise that genetic drift is responsible for linkage disequilibrium in C. championii.


   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
C. championii is one of the several narrowly distributed species of Fagaceae in Taiwan. It can only be found in locations close to mountain ridges exposed to strong seasonal winds. To our surprise, C. championii maintains high genetic diversity when compared with other local woody plants (Lin et al. 1997). This is especially evident when other restricted species are compared. The average values of parameters describing within-population variation are comparable to those of long-lived woody plants (Hamrick et al. 1992). C. championii has similar genetic diversity to wind-pollinated species, but it is higher than that of species using seed dispersal by gravity (Hamrick et al. 1992).

Since it is also distributed in southern China, C. championii in southern Taiwan could be considered a marginal population that probably has a lower genetic diversity than the population in mainland China. This inference is based on several previous observations, for example, Cunninghamia lanceolata var. konishii (Taiwan; He = 0.219) versus C. lanceolata (China; He = 0.343) (Lin et al. 1998), Chamaecyparis obtusa var. formosana (Taiwan; He = 0.052) (Lin et al. 1994) versus C. obtusa (Japan; He = 0.202) (Uchida et al. 1991), and Cyclobalanopsis glauca having higher genetic diversity (He = 0.222) in China (Chen et al. 1997) than that in Taiwan (Li 1999; He = 0.167).

The current distribution of C. championii is probably related to paleoclimatic changes. During the late Pleistocene, temperate forests dominated the lowlands of Taiwan in the Tali glacial stage from about 50,000 to 15,000 BP (Tsukada 1967). During that time, in China, the climate cooled and Taiwan probably was connected with the Chinese mainland by a land bridge (Liu 1988) and plants could have migrated toward the warmer south without a barrier. C. championii, being better adapted to a cool climate, might have survived in refugia on the Hengchun Peninsula. Glaciers retreated northward around 15,000 BP, and warming returned to the lowlands. C. championii might have been forced to migrate to higher elevations or to expand northward, and this migration would have been intensified by the massive invasion of tropical elements from the south. We do not know, however, what caused C. championii to be restricted to the Hengchun Peninsula. Knowledge of the evolutionary history, including shifts in distribution, population isolation, and refugia, would help interpret the current genetic structure.

C. championii is wind-pollinated and monoecious: the staminate catkins and pistillate flowers growing on the same or different branches. The fixation indexes, however, indicate a deficiency of heterozygotes. C. championii probably is lacking a mechanism for seed dispersal. The relatively large and heavy seeds (about 0.7 g/seed) may restrict seed dispersal in the neighborhood of the mother tree. A deficiency of heterozygotes, while a general phenomenon, is, however, especially obvious for the populations at Shouchia and Nanjenshan, as the F values deviate most from the Hardy–Weinberg proportion (Table 2). A high proportion of randomly generated disequilibrium between alleles of unlinked loci for the populations at Shouchia and Nanjenshan was also observed. As there is no direct evidence that epistatic selection is involved, we believe the cause of linkage disequilibrium is genetic drift (Bucci et al. 1997; Hill 1981; Ohta and Kimura 1969).

As we see no obvious differences of population size among these several locations, then why has inbreeding and genetic drift occurred in the south and lower-elevation populations only? Small populations located at the margin of a species natural range are expected to diverge by a larger extent based on the distance from the main gene pool (Millar and Marshall 1991). Divergence in genetic distance is small in these populations but obvious (Figure 3). If we consider the population at Tahanshan as the main pool of genetic diversity, the rest of populations have an apparent divergence from it. This probably is because the remaining populations are drifting in different directions to some extent. If genetic drift is responsible for the observed divergence, lowered genetic diversity is expected for a marginal population, as reported for many forest tree species (Furnier and Adams 1986; Hamrick et al. 1989; Millar and Marshall 1991). Indeed, the Kaoshihfo and especially the Nanjenshan populations have lower genetic diversity.

In C. championii, 9.2% of the total genetic diversity measured over the polymorphic loci is attributable to differentiation among populations. This value is higher than the mean value (7%) observed over 25 species of oaks studied for enzyme polymorphism (Kremer and Petit 1993). This is also higher than that in Cyclobalanopsis glauca, which has Gst = 0.056 in mainland China (Chen et al. 1997). We believe that genetic drift in the southern population of C. championii will continuously increase the genetic divergence among populations.

We found that the correlation coefficient between expected heterozygosities and the elevation range of populations, and the correlation between He and latitude are significant (Figure 2). Even though correlation does not imply causation, heterozygosity could be related to ecological factors that are confounded but unrelated to elevation or latitude. Based on our data, apparently elevation or average temperature could be one of the possible ecological factors that influence heterozygosity; thus a warmer environment does not favor heterozygosity in C. championii.


   Acknowledgments
 
This research was financially supported by the Taiwan Forestry Research Institute (TFRI). This article is contribution no. 168 of the TFRI.


   Footnotes
 
Address correspondence to Tsan-Piao Lin at the address above or e-mail: tpl{at}ccms.ntu.edu.tw.

Corresponding Editor: William F. Tracy

Received December 1, 1999
Accepted October 31, 2000


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 Introduction
 Materials and Methods
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 Discussion
 References
 

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