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Systematics |
2Graduate School of Environmental Earth Science, Hokkaido University, Sapporo, Hokkaido 060-0810, Japan; 3Department of Biological Sciences, Faculty of Science, Nara Women's University, Kitauoya-Nishimachi, Nara 630-8506, Japan
Received for publication July 11, 2002. Accepted for publication December 10, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: AFLP • Fagaceae • hybridization • morphological traits • Phyllonorycter • Quercus crispula • Quercus dentata
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Burger, 1975
; Van Valen, 1976
; Rieseberg and Wendel, 1993
). Previous studies on Q. robur-Q. petraea-Q. pubescens, Q. rubra-Q. ellipsoidalis, and Q. gambelii-Q. grisea complexes have indicated that sibling pairs are more distinctly discriminated by morphological or ecological (i.e., adaptive) traits than by isozyme or DNA markers (Jensen et al., 1993
; Kleinschmit et al., 1995
; Howard et al., 1997
; Bruschi et al., 2000
; Tomlinson et al., 2000
). Morphological or adaptive traits might have differentiated faster than isozymes or DNA markers. In addition, isozymes or DNA markers, which are probably not affected by natural selection, might have been transferred from species to species through hybridization, while alleles responsible for differential adaptation might not have been transferred despite hybridization (Wu, 2001
). To address these issues, information on the extent of morphological, ecological, and genetic differentiation and the frequency of hybridization is important, but still insufficient. This is partly because even identification of hybrid individuals of oaks is not simple (Jensen et al., 1993
; Kleinschmit et al., 1995
; Bruschi et al., 2000
; Tomlinson et al., 2000
).
In this paper, we investigate differentiation and hybridization between Q. crispula Blume and Q. dentata Thunberg on the basis of morphological traits, amplified fragment length polymorphism (AFLP) markers, and leafminer (Phyllonorycter; Gracillariidae; Lepidoptera) composition. These two oaks are widely distributed in central and northern Japan and often co-occur. They are normally discriminated by the presence or absence of stellate hairs on the lower surface of leaf and characteristics of the acorn cap (Ooba, 1989
). These two species also differ in some other traits such as leaf thickness and number of lobes of leaf (Ooba, 1989
). However, continuous variation is observed in these traits, especially among individuals from mixed stands (Miyazaki, 1989
; Ooba, 1989
; Hashizume et al., 1994
). In addition, there are individuals that are Q. crispula-type in some traits and Q. dentata-type in other traits. These situations, probably due to hybridization and introgression, often prevent the identification of species and hybrid individuals. In the present study, therefore, morphological data were subjected to multivariate analysis to identify linear combinations of variables that best discriminate between the species studied.
For discrimination of oak species, molecular markers such as isoenzymes, microsatellite DNA, and randomly amplified polymorphic DNA (RAPD) have also been used (Kleinschmit et al., 1995
; Samuel et al., 1995
; Bondénès et al., 1997
; Dumolin-Lapègue et al., 1997
; Bruschi et al., 2000
; Tomlinson et al., 2000
), but no diagnostic markers have been obtained except for a set of RAPD markers that distinguish between Q. gambelii and Q. grisea from North America (Howard et al., 1997
). The AFLP technique used in this study yields a large number of stable markers with which multivariate analysis can be performed. Previous studies using this technique have successfully analyzed genetic diversity and identified closely related species and their hybrids in a number of plants and animals (Hill et al., 1996
; Lu et al., 1996
; Sharma et al., 1996
; Ajmonemarsan et al., 1997
; O'Hanlon et al., 1999
; Cresswell et al., 2001
; Young et al., 2001
), but it has not yet been applied in oak taxonomy.
The patterns of herbivore attack of hybrid plants are variable (Fritz, 1999
; Orians, 2000
), most likely due to variation in the mode of inheritance of chemical traits that affect herbivore behaviors and performance (Orians, 2000
). If parental species have species-specific herbivores and if attractants to these herbivores show codominant or intermediate inheritance, hybrid individuals may harbor herbivores of both parental species. In such case, herbivore composition can be used as a surrogate for detection of hybrid individuals. It has been reported that the present two oak species harbor different Phyllonorycter species (Sato, 1991
; Fujihara et al., 2001
). Here we examined Phyllonorycter composition on oak individuals from a mixed stand and ascertained its usefulness in the detection of hybrid individuals.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Collections of leaves were made from 96 individuals that are found along a transect (about 500 m) across this Ishikari forest from the coastal side to inland. In addition, leaves were collected from nine individuals having intermediate appearance between Q. crispula and Q. dentata. These nine trees grow at distances of 5–50 m from the transect.
As references, leaves were also collected from pure populations of Q. crispula in Hamamasu and Toishiyama and a pure population of Q. dentata in Nakaotofuke. Hamamasu (43°00' N, 141°17' E) is located about 40 km north of Ishikari; Toishiyama (43°35' N, 141°28' E) is located about 40 km south of Ishikari; and Nakaotofuke (43°07' N, 143°05' E) is situated about 300 km east of Ishikari. The forests in Hamamasu and Toishiyama are dominated by broad-leaved trees such as Q. crispula, Acer mono, and Betula platyphylla, while the forest in Nakaotofuke is a windbreak dominated by Q. dentata. Leaves were collected from 50 oak trees at each location.
Morphological data
From each of 255 trees, 10 shade leaves were collected in mid-summer 1999 and measured for area, perimeter, length, width, number of lobes, and dry mass (i.e., mass after dehydration at 60°C for 48 h). The first two traits (area and perimeter) were measured using the public domain NIH Image program (developed at the U.S. National Institutes of Health and available on the Internet at http://rsb.info.nih.gov/nih-image/) after leaf shape was scanned by an image scanner (JX-270, Sharp, Tokyo, Japan). In addition, the density and length of stellate hairs and the presence or absence of solitary and short hairs (Hardin, 1975
; Ooba, 1989
; Kim et al., 1992
) on the lower surface were determined for three leaves from each tree. The measurements were made on a piece (3.46 mm2) that was punched off from the intervein area near the base of each leaf. Analyses were made using mean values of 10 or three leaves.
AFLP data
The AFLP data were collected only for individuals from the mixed stand at Ishikari. Winter buds were collected from 104 out of 105 trees at Ishikari in autumn 1999 and stored at –70°C (buds could not be obtained from one individual). Buds (100 mg) were ground in liquid nitrogen, and total genomic DNA was extracted with QIAquick DNeasy Plant Mini Kit (QIAGEN, Valencia, California, USA) according to the supplier's instruction. The DNA extracts (about 1.5 µg from each tree) were stored in 70% ethanol until further manipulations.
The AFLP Ligation and Preselective Amplification Module and EcoRI/MseI primers were purchased from PE Applied Biosystems (Foster City, California, USA). The extensions of the primer pairs used in this study are EcoRI-ACA/MseI-CAG, EcoRI-AAG/MseI-CAC, and EcoRI-AAC/MseI-CTG. Digestion and amplification of sample DNA were performed according to the supplier's instruction, and amplified products were electrophoresed on an ABI 373A automated sequencer (PE Applied Biosystems).
The relative mobility of fragments was calculated by the inclusion of an internal size standard within each sample. Digital profiles were visualized with the aid of ABI Genescan software (PE Applied Biosystems). The consistency of amplification was ascertained using DNA samples from two or three different buds on each of five trees; fragments that were not observed in all the samples from the same trees were assumed to be unstable and were not scored.
Phyllonorycter composition
Nine species of Phyllonorycter (leafminers) were observed on oaks in the study area; seven species have been reported to be specific to Q. crispula [P. acutissimae (Kumata), P. similis Kumata, P. crenata (Kumata), P. pseudolautella (Kumata), P. pygmaea (Kumata) and P. mongolicae (Kumata) and P. matsudai Kumata] and two to Q. dentata [P. persimilis Fujihara, Sato and Kumata and P. leucocorona (Kumata)] (Sato, 1991
; Shibata et al., 2001
). They are discriminated to species by the pupal exuviae (Sato, 1991
; Fujihara et al., 2001
).
The Phyllonorycter composition was examined only for individuals from the mixed stand at Ishikari. In the pure populations at Nakaotofuke, Toishiyama, and Hamamasu, the density of Phyllonorycter species was low, and it was also difficult to collect a large number of leaves because they were located at 20–30 m in height. In 2000, 61–476 leaves were collected from each of 104 oak trees at Ishikari in late October. In 2001, 123–259 leaves were collected from each of 36 selected trees at Ishikari in mid-October: 15 trees had morphological characteristics of Q. dentata, 13 had those of Q. crispula, and eight had intermediate morphology (see Results). These leaves were stored outdoors until almost all of Phyllonorycter larvae grew to pupae. Phyllonorycter pupae were then collected from these leaves and identified to species. Individuals remaining as larvae were reared in plastic cases until pupation.
Analysis
The morphological characteristics of individuals from the mixed Ishikari stand were examined with reference to morphology of pure populations at Nakaotofuke (Q. dentata), Toishiyama, and Hamamasu (Q. crispula). First, we examined whether each morphological trait significantly differed between Q. dentata and Q. crispula from the pure populations. In this analysis, ANOVA was applied for traits that showed normal distribution according to a Kolmogorov-Smirnov test (P > 0.05); a Kruskal-Wallis test was applied for traits that did not show normal distribution; and a 
2 test was made for contingency data. The traits that showed significant difference between the two species were then applied to factor analysis to examine multicollinearity, which may bring confusion in discriminant analysis, and traits that varied independently were selected. Then, using the selected traits, canonical discriminant analysis was made on individuals from the three pure populations. A discriminant formula obtained with the above analysis was then used to calculate canonical variate (CV) scores for individuals from the mixed stand at Ishikari. All the statistical analyses except for the Kolmogorov-Smirnov test were performed with JMP 4.0 (SAS Institute, Cary, North Carolina, USA); the Kolmogorov-Smirnov test was made with SPSS 6.1 (SPSS, Chicago, Illinois, USA).
On AFLP data, we performed principal coordinate analysis (PCOA) to assess genetic differentiation between these two oak species. A PCOA allows the assessment of the dimensionality of the data and a description of the major patterns of variation within and between populations (Cresswell et al., 2001
). The similarity between each pair of trees was estimated using the Dice's ecological similarity index, Sij (Dice, 1945
): Sij = 2Nij/(Ni + Nj), where Nij is the number of markers shared by plants i and j, Ni is the number of markers found in plant i, and Nj the number of markers found in plant j. The genetic dissimilarity was expressed by the formula Dij = 1 – Sij. The analysis was performed with a dissimilarity matrix using R PACKAGE 4.0 (Casgrain and Legendre, 2001
).
With data on Phyllonorycter composition, a Phyllonorycter index (PI) was calculated for each tree with the following formula, PI = (PD – PC)/(PD + PC), where PD is the number of individuals of two Phyllonorycter species specific to Q. dentata and PC is the number of individuals of seven species specific to Q. crispula.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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2 tests revealed significant differences in all leaf traits between the two species and in some traits among the three pure populations (Table 2). Factor analysis was performed on these traits for the three pure populations (Table 3). Dry mass, area, perimeter, length, and width showed high loadings to Factor 1 in all populations. Therefore, only area was used among these five traits in the canonical discriminant analysis.
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Genetic analysis
A total of 175 fragments ranging from approximately 100 to 400 base pairs (bp) were identified from individuals from Ishikari in the present analysis using the three primer pairs. Additional fragments were present but could not be scored either because of faint, inconsistent amplification or difficulty in differentiating two or more fragments of a similar mass.
The principal coordinate analysis was performed using these 175 markers for individuals from Ishikari. The first principal coordinate, which accounted for 6.7% of the variance, showed two clusters that discriminated between the two species, but individuals with intermediate morphological scores occurred in both clusters. The second principal coordinate, which accounted for 4.3% of the variance, did not separate the present oaks (Fig. 2). There was an association between the first PCO score in the AFLP analysis and the CV score in the morphological analysis (Fig. 3).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Kleinschmit et al., 1995
; Bruschi et al., 2000
; Tomlinson et al., 2000
). This is true for Quercus crispula and Q. dentata, predominant members of cool-temperate forests of Japan. These two species differ in various morphological, ecological, and genetical traits (also see Ooba, 1989
; Lee et al., 1996
; Fujihara et al., 2001
), and the density of stellate hairs and the characteristics of the acorn cap have been claimed as reliable criteria for their discrimination (Ooba, 1989
). However, the detection of hybrids is not always possible only by these traits, because there is considerable within-species variation but only a small between-species gap. For example, the mean density of stellate hairs was 0–1.4 hairs/mm2 in Q. crispula trees from pure stands at Toishiyama and Hamamasu and 2.2–6.8 hairs/mm2 in Q. dentata trees from a pure stand at Nakaotofuke. If the density of stellate hairs shows intermediate inheritance, hybrids between an individual of Q. crispula with 1 hair/mm2 and an individual of Q. dentata with 5 hairs/mm2 are expected to have 3 hairs/mm2, a score within the range of Q. dentata. In addition, hybrids may have characteristics of either of the parental species due to dominant or recessive inheritance. These problems can be solved by multivariate analysis that identifies linear combinations of variables. In this study, we carried out canonical discriminant analysis with eight morphological traits using pure populations of the two oak species as reference and revealed that nine out of 105 individuals in a mixed stand at Ishikari had intermediate morphology.
The composition of Phyllonorycter (leafminer) species was applied for the discrimination of hybrid oaks for the first time in this study. The Phyllonorycter composition analysis was consistent with the multivariate analysis of morphological traits for eight individuals among nine, suggesting the usefulness of the leafminer information for predicting hybridization. The utility of leafminers for the identification of hybrids relies on their high host specificity. In general, leafminers are known to have narrow host preferences (Schoonhoven et al., 1998
). In fact, the present Phyllonorycter species seem to be specific to either of Q. dentata or Q. crispula (Sato, 1991
; Fujihara et al., 2001
). At Ishikari, however, some putative Q. crispula and Q. dentata were mined by the species that were not specific to the species. The Phyllonorycter species may not be complete in host selection, or leaf chemical characteristics of these oaks may have changed according to introgression (host selection of leafminers is expected to depend on chemical characteristics of leaves).
The PCOA using AFLP data revealed that Q. dentata and Q. crispula have also differentiated at the molecular level. However, the degree of differentiation was low, and the AFLP data were less informative for the identification of hybrids. In addition, no diagnostic AFLP marker was obtained; i.e., markers that were observed in all individuals of one species were also observed in the other species at high frequencies (>0.95), and markers observed only in either of the two oak species were low in frequency (<0.16). Previous studies also reported that the degree of molecular differentiation is low between some sibling pairs; Q. robur-Q. petraea (Kleinschmit et al., 1995
), Q. grisea-Q. gambelii (Howard et al., 1997
) and Q. petraea-Q. pubescent (Bruschi et al., 2000
).
Despite Q. crispula and Q. dentata hybridizing in nature, they remain morphologically, genetically, and ecologically distinct as do other sibling pairs of Quercus (Kleinschmit et al., 1995
; Howard et al., 1997
; Bruschi et al., 2000
; Tomlinson et al., 2000
). Jiggins and Mallet (2000)
suggested that such bimodal hybrid zones are more effectively maintained by ecological divergence between parental species than by their genetic incompatibility. In fact, most pairs of Quercus species that remain distinct despite hybridization differ in ecological niches (Kleinschmit et al., 1995
; Howard et al., 1997
; Bruschi et al., 2000
; Tomlinson et al., 2000
; Williams et al., 2001
). The difference in leaf traits (e.g., the density of stellate hairs or LMA) between the present study species would also reflect the difference in their adaptations to environmental conditions such as humidity or light regimes (Zhou et al., 1995
; Lambers et al., 1998
). In addition, Wu (2001)
suggested that if reproductive isolation has once developed between species or populations to some degree, genes responsible for that isolation and submitted to differential selection might not transfer across species even if hybridization occurs.
In conclusion, Q. crispula and Q. dentata were revealed to have differentiated in morphological traits, molecular (AFLP) markers, and composition of Phyllonorycter species. Morphological traits and Phyllonorycter composition were useful for the identification of hybrids, while AFLP data were less informative because the degree of molecular differentiation between the parental species was low. Out of 105 individuals from a mixed forest, nine were morphologically intermediate, and eight out of these nine individuals were also intermediate in the Phyllonorycter composition. These eight individuals were tentatively assigned to be hybrids or to have hybrid origins.
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FOOTNOTES |
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4 Author for reprint requests (mtk{at}ees.hokudai.ac.jp
; FAX: +81-11-706-2225)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, putative Q. crispula; 
, morphologically intermediate individuals