Transcript
Page 1: Genetic diversity and population structure of Korean alder (               Alnus japonica               ; Betulaceae)

Genetic diversity and population structure ofKorean alder (Alnus japonica; Betulaceae)

Man Kyu Huh

Abstract: The genetic diversity and population genetic structure ofAlnus japonica(Thunb.) Steudel in Korea werestudied and compared with those of alder from Canada. Nineteen of the 25 loci studied (76.0%) showed detectablepolymorphism. The mean genetic diversity within populations was 0.207, which was higher than that for two Canadianalder species (Alnus rugosa(Du Roi) Spreng. andAlnus crispa(Ait.) Pursh). Analysis of fixation indices, calculatedfor all polymorphic loci in each population, showed a substantial deficiency of heterozygotes relative to Hardy–Weinberg expectations. The mean population differentiation value ofA. japonica in Korea (GST = 0.095) is similar tothose ofA. rugosain Canada (GST = 0.052). These low values ofGST in two countries, reflecting little spatial geneticdifferentiation, may indicate extensive gene flow (via pollen and (or) seeds) and (or) recent colonization.

Résumé: L’auteur a étudié et comparé la diversité génétique et la structure génétique des populations d’Alnus japonica(Thunb.) Steudel en Corée à celles de l’aulne au Canada. Parmi les 25 loci étudiés, 19 (76,0%) affichaient unpolymorphisme détectable. La diversité génétique moyenne au sein des populations était de 0,207. Cette diversité étaitplus élevée que celle de deux espèces canadiennes d’aulne (Alnus rugosa(Du Roi) Spreng. etAlnus crispa(Ait.)Pursh). L’analyse des indices de fixation, tels qu’estimés pour tous les loci polymorphes au sein de chaque population,indiquait une déficience substantielle en hétérozygotes comparativement aux proportions espérées selon l’équilibred’Hardy–Weinberg. La valeur moyenne de différenciation des populations chez l’A. japonicaen Corée (GST = 0,095)était similaire à celles de l’A. rugosaau Canada (GST = 0,052). Ces faibles valeurs deGST au sein des deux paysreflètent un différenciation génétique spatiale faible, laissant supposer un flux génique important (par pollen ou pargraines) et (ou) une colonisation récente.

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IntroductionAlder is an early successional monoecious species that

forms root nodules symbiotically with the actinomyceteFrankia, which fixes nitrogen (Normand and Lalonde 1986).As revealed by early fossil record, the genusAlnus couldhave originated in the Asian land mass, around the Creta-ceous (Furlow 1979a). Alder is now distributed in Asia,Southeast Asia, and the East Indies and the species is alsofound in subtropical and tropical New World north to thesouthern United States (Woodland 1991). Speckled alder(Alnus rugosa(Du Roi) Spreng.) and green alder (Alnuscrispa (Ait.) Pursh) also occur in the region of central Que-bec in North America (Bousquet et al. 1988). It is assumedthat the differentiation of the alder species preceded thespread of the genus to the Northern Hemisphere, but thisevent has not been documented precisely in time (Furlow1979a). Fossil records suggest that species of both subgeneraexisted by the Miocene (ca. 20 million years B.P.) in NorthAmerica (Furlow 1979a).

This study investigated the genetic diversity of Korean al-der populations. It will be of interest to analyze one of theprogenitor populations, widespread plants from Korean al-der, on the amounts and patterns of genetic variation. Littleis known about the levels of genetic variation and the popu-

lation structure of alder species, despite its ecological impor-tance (furniture, forestation, firewood, and windbreak forest)and transcontinental distribution of the species. This actino-rhizal wind-pollinated tree is typically found on moist andsoggy lowland soil; it reaches a height of 10 m and maxi-mum expected stem age of 20 years, although individualsmay be actually older because of root and stump sprouting(Huenneke 1987).

Alnus rugosaand A. crispa are classified by Furlow(1979a, 1979b) as subspecies ofAlnus incana(L.) Moench(Alnus incana ssp. rugosa (Du Roi) Clausen andAlnusincanassp.crispa (Ait.) Pursh), while both are members ofsubgenusAlnus(Furlow 1979a). Bousquet et al. (1988) sug-gest that alder originated in Asia and India. Actually, Asianregions such as China, Korea, Japan, and Siberia are wellknown for various alder species. The genusAlnus in Koreais comprised of 15 species.Alnus japonica(Thunb.) Steudelis the most abundant alder species in Korea. Female flowersof alder consist of two compound, united carpels. The spe-cies is obligating outcrossing with wind pollination. Iwanted to address the following questions in this study: isthere considerably more variability in the putative area oforigin of the genusAlnusand how extensive does the loss indiversity concur with speciation, adaptation, and the spreadto different climate regions or to different continent? Thepurpose of this study was (i) to estimate how total allozymediversity is maintained inA. japonicaand (ii ) to compare thegenetic diversity and structure of alder in Korea with thoseof alder from Canada.

Can. J. For. Res.29: 1311–1316 (1999) © 1999 NRC Canada

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Received August 8, 1998. Accepted February 11, 1999.

M.K. Huh. Department of Biology Education, Pusan NationalUniversity, Pusan, 609-735, The Republic of Korea.e-mail: [email protected]

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Materials and methods

Sampling procedureAlnus japonicawas collected from 17 natural populations in Ko-

rea (Fig. 1). One leaf per plant was sampled during 1996–1998.More than 30 plants were collected from each population. Leavesgathered from natural populations were stored in plastic bags forseveral days in a refrigerator until electrophoresis was carried out.

Enzyme electrophoresisLeaves were homogenized by mechanical grinding to release en-

zymes from cell and organellar membranes with Tris-HCl grindingbuffer – polyvinylpyrrolidone solution described in Soltis et al.(1983). Electrophoresis was performed using 10% starch gel.Tris – citric acid electrophoretic buffer system (No. 5 of Soltis etal. 1983) was used for isocitrate dehydrogenase (IDH), malatedehydrogenase (MDH), malic enzyme (ME), 6-phosphoglugonatedehydrogenase (6PGD), phosphoglucomutase (PGM), shikimatedehydrogenase (SKD), and superoxide dehydrogenase (SOD); asodium borate system (No. 6 of Soltis et al. 1983) was used forglutamate oxaloacetate transaminase (GOT) and phosphoglucoseisomerase (PGI); a lithium borate system (No. 7 of Soltis et al.1983) was used for menadione reductase (MNR); and a morpholinecitrate pH 6.3 buffer (Werth 1991) was used for fluorescentesterase (FE) and peroxidase (PER). Presumptive loci were desig-nated sequentially, with the most anodally migrating one desig-nated No. 1; the next, No. 2; and so on. Likewise, alleles weredesignated sequentially with the most anodally migrating one des-ignated “a” and progressively slower forms “b,” “c,” and so on. AllA. japonicaisozymes expressed phenotypes that were consistent insubunit structure and genetic interpretation with most isozymestudies in plants, as documented by Weeden and Wendel (1989).

Analysis of dataA locus was considered polymorphic when more than one allele

was detected, regardless of their frequencies. Four standard geneticparameters were estimated using a computer program developedby M.D. Loveless and A. Schnabel (personal communication): per-centage of polymorphic loci (P), the number of alleles per poly-morphic locus (AP), mean number of alleles per locus (A), effectivenumber of alleles per locus (AE), and gene diversity (HE) (Hamricket al. 1992). Subscripts refer to species- (s) or population-level (p)parameters. Observed heterozygosity (HO) was compared withHardy–Weinberg expected value using Wright’s fixation index (F)or inbreeding coefficients (Wright 1922). These indices were testedfor deviation from zero byχ2 statistics following Li and Horvitz(1953).

Nei’s gene diversity formulae (HT, HS, DST, andGST) were usedto evaluate the distribution of genetic diversity within and amongpopulations (Nei 1973, 1977). In addition,χ2 statistics were usedto detect significant differences in allele frequencies among popu-lations for each locus (Workman and Niswander 1970). Nei’s ge-netic identity (I) and distance (D) were calculated for eachpairwise combination of populations (Nei 1972). I used the PC-SAS program (SAS Institute Inc. 1989) to conduct a cluster analy-sis on genetic distances via the unweighted pairwise groupsmethod arithmetic average (UPGMA).

The genetic structure within and among populations was alsoevaluated using Wright’s (1965)F statistics:FIT and FIS. The FITandFIS coefficients measure excesses of homozygotes or heterozy-gotes relative to the panmictic expectations within the entire sam-ples and within populations, respectively. TheGST coefficientestimates relative population differentiation. Deviation ofFIT andFIS from zero was tested usingχ2 statistics (Li and Horvitz 1953).Two indirect estimates of gene flow were calculated. One estimateof Nm (the number of migrants per generation) was based onGST

(Wright 1951) and the other estimate was based on the average fre-quency of “rare” alleles found in only one population (Slatkin1985; Barton and Slatkin 1986). The absolute population differen-tiation (Dm) was calculated using Nei’s (1973) statistics. Correla-tion between geographical and genetic distance was tested usingMantel’s test as advocated by Smouse et al. (1986).

Results

Genetic diversityNineteen of the 25 loci studied (76.0%) showed detectable

polymorphism in at least two populations. The remaining sixloci (Per-3, Per-4, Mdh-3, Gpi-1, Pgm-2, and Skd-2) weremonomorphic in all populations. An average of 62.8% of theloci were polymorphic within populations, with individualpopulation values ranging from 48.0 to 72.0% (Table 1).In the polymorphic loci, 10 loci (Fe-2, Idh-1, Mdh-2, Got,Me-2, Per-2, 6Pgd-2, Sod, Pgm-1, and Skd-1) expressedthree alleles, while the remaining ones expressed either twoalleles (six loci) or four alleles (Mdh-2 andMnr). The larg-est number of alleles per locus was five atFe-1. The numberof alleles per polymorphic locus (AP) was 2.47 (2.25–2.88).The average number of alleles per locus (A) was 1.93 across

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Fig. 1. Location of Alnus japonicapopulations sampled forisozyme analysis and mean rainfall per year. Letters show meanannual rainfall amounts. A, 800–1000 mm/year; B, 1001–1200 mm/year; C, 1201–1400 mm/year; D, 1401–1600 mm/year;E, 1601–1800 mm/year; F, 1801–2000 mm/year.

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populations, varying from 1.64 to 2.20. The effective num-ber of alleles per locus was similar at the species and thepopulation level (AEs = 1.40;AEp = 1.39). The mean geneticdiversity within populations was 0.207. Population 5 had thehighest expected diversity (0.282), while population 8 hadthe lowest (0.169). Genetic diversity at the species level washigh, whereas the value at the population level was low(HEs = 0.235 andHEp = 0.207, respectively).

Genetic structureIn general, genotype frequencies do not conform to

Hardy–Weinberg expectations. Chi-square tests indicatedsignificant deviations from Hardy–Weinberg ratio. As ex-pected from the chi-square tests,FIS, a measure of the devia-tion from random mating within 17 populations, was 0.422,ranging from 0.002 forGpi-2 to 0.797 for Idh-1 (Table 2).The observed significant positiveFIS value (0.422) indicatesa significant deficit of heterozygotes in the populations.

Wright’s F statistics in Table 2 show that significant defi-ciencies of heterozygote exist for all polymorphic loci. On aper locus basis, the proportion of total genetic variation dueto differences among populations (GST) ranged from 0.028for Per-2 to 0.263 forFe-3 with a mean of 0.095, indicatingthat about 10% of the total allozyme variation was amongpopulations (Table 2). Thus, the majority of genetic variance(90%) resided within populations. The values of genetic dis-tance (D) were below 0.10 in most cases except in pairs in-volving the population 1. The estimate of gene flow basedon GST was relatively moderate (Nm = 2.38). Nm valuesgreater than 1 are considered high. As a result, genetic driftmay not be one of the major factors inA. japonicapopula-tions. Genetic identity values among pairs of populationsrange from 0.914 to 0.992. The genetic similarity amongA. japonicapopulations can be seen in the UPGMA dendro-

gram, where all populations clustered at a genetic distancebelow 0.095. The UPGMA dendrogram provided a few in-sights into the genetic structuring of populations (Fig. 2). Inaddition, the correlation between genetic distance and geo-graphic distance was low (r = 0.30,p < 0.05), indicating thatabout 90% of the variation in genetic distance was caused byunknown factors other than distance.

Discussion

Alnus japonicain Korea maintains a higher level of allo-zyme variation (Ps = 76%, As = 2.44, andAEp = 1.40) thanmost of other long-lived, woody species, which average65% polymorphic loci (Ps), 2.22 alleles per locus (As), and1.24 effective alleles per locus (AEs) (Hamrick et al. 1992).Genetic diversity at the species level (HEs) in A. japonica(0.235) is higher than the mean for long-lived woody species(0.177) and outcrossing, wind-pollinated species (0.173).The same trend is observed at the population level too.Mean percentage of polymorphic loci (PP) for long-livedwoody perennials is 49.3%, mean number of alleles per lo-cus (AP) is 1.76, and mean effective number of alleles per lo-cus (AEp) is 1.20 (Hamrick et al. 1992). WithinA. japonicapopulationsPP is 62.8%,AP is 1.93, andAEp, 1.39.Alnus ja-ponica also maintains higher amounts of genetic diversity(HEp = 0.207) than the most gymnosperm species (meanHEp = 0.151) and long-lived, woody angiosperms (meanHEp = 0.143).

Genetic diversity ofA. japonica in Korea is comparablewith other alder species reported by Bousquet et al. (1988),although there is the difference in species (A. rugosa,A. crispa, andA. japonica) and methodology (e.g., the num-ber of loci, populations, and enzyme system, as well as sam-ple sizes) that may preclude meaningful direct comparisons

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Population N* P AP A AE HOp† HEp

1 36 60.00 2.80 2.08 1.44 0.096 (0.011) 0.223 (0.046)2 38 64.00 2.88 2.20 1.59 0.118 (0.013) 0.270 (0.047)3 39 64.00 2.50 1.96 1.39 0.090 (0.011) 0.202 (0.044)4 42 68.00 2.71 2.16 1.56 0.165 (0.014) 0.273 (0.046)5 32 72.00 2.56 2.12 1.56 0.176 (0.015) 0.282 (0.045)6 30 72.00 2.28 1.92 1.33 0.148 (0.014) 0.208 (0.035)7 32 64.00 2.50 1.96 1.32 0.121 (0.012) 0.191 (0.038)8 36 64.00 2.25 1.80 1.26 0.104 (0.012) 0.169 (0.035)9 30 52.00 2.54 1.80 1.26 0.080 (0.010) 0.158 (0.038)10 38 64.00 2.31 1.84 1.35 0.112 (0.012) 0.195 (0.041)11 36 64.00 2.31 1.84 1.28 0.098 (0.011) 0.177 (0.036)12 36 68.00 2.47 2.00 1.37 0.132 (0.013) 0.203 (0.040)13 32 64.00 2.56 2.00 1.49 0.123 (0.012) 0.226 (0.046)14 30 56.00 2.29 1.72 1.32 0.109 (0.012) 0.173 (0.040)15 35 68.00 2.47 2.00 1.42 0.123 (0.013) 0.212 (0.043)16 30 56.00 2.29 1.72 1.30 0.094 (0.011) 0.178 (0.040)17 30 48.00 2.33 1.64 1.31 0.104 (0.012) 0.170 (0.043)Mean 62.82 2.47 1.93 1.39 0.117 (0.003) 0.207 (0.010)Species 76.00 2.89 2.44 1.40 — 0.235

*Sample size.†Values are means with SD given in parentheses.

Table 1. Percentage of polymorphic loci (P), mean number of alleles per locus (A), and polymorphiclocus (AP), effective number of alleles per locus (AE), observed heterozygosity (HOp), Hardy–Weinbergexpected heterozygosity or genetic diversity (HEp) for 17 populations ofA. japonica.

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(Karron 1987). ForA. rugosa, Ps is 65%,As is 2.78,HEs is0.173,Pp is 55%,Ap is 2.42, andHEp is 0.164 (Bousquet etal. 1988).Alnus crispaalso showed the same level of hetero-zygosity and similar numbers of alleles per polymorphic lo-cus, both at the species and population levels (Bousquet etal. 1987a, 1987b). These comparisons suggest that geneticdiversity levels of the two Canadian alder species are not ashigh as those of the Korean alder species, a temperate-zonespecies. It is possible that the dispersal process may erodethe levels of genetic diversity of derived species as has beenshown in most derived species (Purdy et al. 1994).

The relatively high level of genetic variation found inA. japonica is consistent with several biological aspects ofthis species. First, geographic range of distribution has beenshown to be strongly associated with the level of variationmaintained within populations and at the species level(Hamrick et al. 1979; Hamrick and Godt 1989). Widely dis-tributed plant species tend to maintain more variation thannarrowly distributed species. Although the distribution ofA. japonicain Korea is scattered, the species has wide geo-graphic range in the Northern Hemisphere including EastAsia. Second, the breeding system of a species is an impor-tant determinant of allozyme variation. BecauseA. japonicais polygamous, this species is outcrossing and wind polli-nated. This combination is well known to be associated withhigh levels of allozyme variation (Hamrick and Godt 1989).Third, long-lived perennial species, likeA. japonica, gener-ally maintain higher levels of variation than annuals andshort-lived perennials.

The meanGST value based on 73 woody angiosperms is0.102 (Hamrick et al. 1992). Similar values were observedin A. rugosain Canada (meanGST = 0.052; Bousquet et al.1988) and inA. japonicain Korea (meanGST = 0.095), sug-

gesting that about 90–95% of the total variation in the alderspecies is common to all populations. These low values ofGST in two countries, reflecting little spatial genetic differen-tiation, may indicate extensive gene flow (via pollen and(or) seeds) and (or) recent colonization. Species with morepollen or seed movement should have less differentiationthan species with restricted gene flow. In support of thesepredictions, Loveless and Hamrick (1988) found that long-lived polycarps common to the later stages of succession hadlow GST values. These species are outcrossed, monoecious ordioecious, wind-pollinated species. BecauseA. crispa andA. japonica are so different in their ecological niches(A. crispa being found mainly on dry subsites, whereasmoist habitats were colonized mostly byA. japonica), simi-lar selection intensities from one site to another appear to bean unlikely factor explaining the apparent low among-population differentiation present in both species, even if ithas been suggested to be among the potential factors ex-plaining the low differentiation observed among populationsof A. crispa(Bousquet et al. 1987b) and other plant species(Levin and Krester 1971). Common life-history traits, suchas allogamy, wind dispersal of both pollen and seeds, highreproductive capability, similar longevity, and successionalbehavior, could more readily account for most of the homo-logy in the population genetics of these shrubby species and,most likely, for the low differentiation observed at the intra-specific level. These factors reduce the effect of geographicisolation of breeding on the chance for genetic divergence.An Nm value >1 can be considered high, and as a result, ge-netic drift should not be a major factor inA. japonicapopu-lations. Thus, the levels of gene flow I have calculated areof sufficient magnitude to counterbalance genetic drift andmay play a major role in shaping the genetic structure of the

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Locus HT HS DST FIS FIT GST Dm

Fe-1 0.623 0.538 0.086 0.394 0.477 0.137 0.091Fe-2 0.557 0.456 0.102 0.494 0.587 0.182 0.108Fe-3 0.113 0.084 0.030 0.502 0.633 0.263 0.032Mnr 0.471 0.412 0.059 0.361 0.441 0.126 0.063Idh-1 0.327 0.300 0.027 0.797 0.814 0.081 0.028Idh-2 0.224 0.218 0.006 0.431 0.447 0.029 0.007Mdh-1 0.334 0.296 0.038 0.524 0.577 0.113 0.040Mdh-2 0.257 0.233 0.024 0.416 0.470 0.093 0.025Got 0.430 0.388 0.042 0.505 0.553 0.097 0.044Me-1 0.124 0.117 0.006 0.248 0.286 0.051 0.007Me-2 0.450 0.376 0.074 0.318 0.431 0.165 0.079Per-1 0.175 0.157 0.018 0.195 0.276 0.101 0.019Per-2 0.379 0.368 0.010 0.615 0.626 0.028 0.0116Pgd-1 0.095 0.091 0.004 0.401 0.426 0.042 0.0046Pgd-2 0.295 0.278 0.017 0.451 0.482 0.056 0.018Sod 0.285 0.261 0.024 0.646 0.675 0.084 0.025Pgm-1 0.252 0.237 0.015 0.412 0.446 0.059 0.016Gpi-2 0.355 0.344 0.012 0.002 0.034 0.032 0.012Skh-1 0.118 0.110 0.008 0.305 0.351 0.067 0.008Mean 0.309 0.277 0.032 0.422 0.475 0.095 0.034

Table 2. Total genetic diversity (HT), genetic diversity within population (HS), deviations of genotypefrequencies from Hardy–Weinberg expectations over all populations (FIT) and within individualpopulations (FIS), proportion of total genetic diversity partitioned among populations (GST), andabsolute population differentiation (Dm) of A. japonica.

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populations. The gene flow of alder may be explained inplant by the natural-history information about seed and pol-len dispersal (Duncan and Duncan 1988). For example, theperiods of fruit maturation ofA. japonicais from October toNovember, and mature fruits are transported by birds and ro-dents. In addition, cutting of branches and stems have oftenbeen done from hillside to nearby farmhouse for the purposeof fire-wood during the past several hundred years. This oc-casional cutting and carrying of fruit-bearing branches andstems may have resulted in secondary seed dispersal into ad-jacent areas.

A positive correlation between genetic distance and geo-graphic distance (r = 0.30) was found. With ar value of0.30, only 9% of the variation in genetic distance value isexplained by geographic distance. In addition, the correla-tions between rainfall, altitude, and latitude with genetic di-versity per population were examined. Genetic diversityversus other factors except rainfall did not show a signifi-cant correlation with increasing rainfall. A pattern of in-creasing genetic diversity is observed with increasing meanannual rainfall (Fig. 3). Regression analysis indicates that23% (r = 0.57,p < 0.05) of the variability can be explainedby this relationship. The rainy seasons (spring and summer)and dry seasons (autumn and winter) in Korea are distinct.Water may be one of the important limiting factors during

the growing season.Alnus japonicaespecially needs a lot ofwater. Alnus japonicais a very shade-tolerant tree speciesfound within a wide range of moisture and temperature con-ditions. Of course, excess rainfall may be a problem forgrowth of alder plants, but precipitation in Korea is neverabove 2000 mm per year.

Analysis of fixation indices, calculated for all polymor-phic loci in each population, showed a substantial deficiencyof heterozygotes relative to Hardy–Weinberg expectations(Table 2). For example, 92.2% of fixation indices were posi-tive (248 of 269), and 147 of them deviated significantlyfrom zero (p < 0.05). Only 21 of these indices (7.8%) werenegative, and none of them deviated significantly from zero.All of 19 FIS values were positive with a mean of 0.422(Table 2). The observed high, significant, and positiveFISvalue indicates that homozygotes were significantly in ex-cess. This high level of inbreeding can result from a varietyof causes: positive assortative mating (i.e., preferential mat-ing among similar genotypes) (Crow and Felsenstein 1968);selection for homozygotes; family structure within a re-stricted neighborhood, causing mating relatives (Levin andKerster 1971); and the Wahlund effect, caused the artificialgrouping of individuals from different breeding populations(Wahlund 1928). The silvics and the reproductive strategy ofA. japonica could explain the observed high inbreedinglevel. Most Korean alder populations (except the populations4, 7, and 13) are relatively small in size and discrete in dis-tribution compared with those in Canada, even though thespecies is polygamous, and male and female flowers exist onthe same plant (Duncan and Duncan 1988). In addition, al-though the species has small winged seeds, the dispersal dis-tance seems to be short under rich pine–oak forests, whichmay favor the establishment of clusters of related individu-als. Such structure could lead to biparental inbreeding, caus-ing heterozygote deficiencies. It is expected that a part of theinbreeding detected is due to consanguineous matings, andthis patchy distribution of related individuals should generate

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Fig. 2. A dendrogram showing the phylogenetic relationshipsamong the 17 populations ofA. japonica, based on data ofgenetic distance obtained by starch gel electrophoresis.

Fig. 3. Relationship between rainfall and genetic diversity for17 populations ofA. japonica.

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a Wahlund effect. Mating among related individuals is ex-pected in this case because of the presence of several seed-lings or sampling in the vicinity of maternal trees that mightbe produced from related seeds in seed banks (El-Kassabyand Yanchuk 1994). It is highly probable that the combina-tion of these factors may contribute to high levels of hetero-zygote deficiencies within populations.

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