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Population Biology |
2Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de México, Antigua Carretera a Pátzcuaro No. 8701, Col. Ex-Hacienda de San José de la Huerta, Morelia, 58190 Michoacán, México; 3Centro de Educación Ambiental e Investigación Sierra de Huautla, Universidad Autónoma del Estado de Morelos, Av. Universidad 1001, Col. Chamilpa, Cuernavaca, 62210, Morelos, México; 4Departamento de Biología, Facultad de Ciencias, Universidad Nacional Autónoma de México, México, D.F. 04510, México
Received for publication April 8, 2003. Accepted for publication September 18, 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: hybrid zones • hybridization • Quercus affinis • Quercus laurina • RAPD markers
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Rieseberg and Wendel, 1993
; Arnold, 1997
). The genus Quercus (the oaks) has long been considered a group with an unusually high frequency of interspecific hybridization (Burger, 1975
; Van Valen, 1976
). Although morphological patterns of variation that support or are consistent with hybridization between many oak species pairs have been reported (Palmer, 1948
; Cooperrider, 1957
; Brophy and Parnell, 1974
; Hardin, 1975
; Jensen et al., 1993
; Bacon and Spellenberg, 1996
), detailed studies of the patterns and frequency of interspecific nuclear and cytoplasmic genetic exchange have focused on only a few species complexes, notably European and North American white oaks. The results of these studies include the demonstration of extensive local sharing of cytoplasmic haplotypes (i.e., cytoplasmic introgression) among sympatric white oak species (Whittemore and Schaal, 1991
; Dumolin-Lapègue et al., 1999
), low genetic differentiation between possibly hybridizing species as measured by allozymes and nuclear molecular markers (Hokanson et al., 1993
; Kleinschmit et al., 1995
; Samuel et al., 1995
; Bodénès et al., 1997
; Howard et al., 1997
; Bruschi et al., 2000
), direct evidence of considerable asymmetric pollination of Q. robur progenies by Q. petraea in a local stand (Bacilieri et al., 1996b
), and the documentation of a mosaic hybrid zone between Q. grisea and Q. gambelli in New Mexico (Howard et al., 1997
).
Red oaks are restricted to the New World and are in general thought to hybridize more extensively than white oaks (Guttman and Weigt, 1989
; Jensen et al., 1993
), but fewer detailed studies of hybridization processes have been conducted on this group (Jensen et al., 1993
; Bacon and Spellenberg, 1996
). Mexico is considered the center of diversity of Quercus in the Western Hemisphere, with an estimated total number of species between 135 and 150 and 86 endemics (Nixon, 1993a
). Of these, 55 species are red oaks, with 41 of them endemic. Diverse topography, climate, and habitat probably exerted an important influence in the process of radiation and maintenance of oak species diversity in this region (Nixon, 1993a
). Paleobotanical evidence suggests that the cooler, drier, and more variable climates that developed after the Eocene-Oligocene transition in North America encouraged the evolution and migration of Quercus (Daghlian and Crepet, 1983
; Borgardt and Pigg, 1999
). The history of oaks in Mexico was probably characterized by range shifts, expansions, and contractions, a product of climatic changes producing the opportunity for periods of differentiation followed by secondary contact between taxa (Bacon and Spellenberg, 1996
). However, very few studies have been conducted on population genetics, hybridization processes, and speciation of Mexican oaks.
Recently, several red oak complexes have been identified in Mexico by specialists (Valencia, 1994
; Bacon and Spellenberg, 1996
). One of these complexes is formed by the closely related species Quercus affinis Scheidweiler and Q. laurina Humboldt et Bonpland (subgenus Quercus, section Lobate; Nixon, 1993b
), which have partially overlapping distributions and show morphological intergradation within the region of overlap, but otherwise remain distinct in localities outside of this area. The objective of this study was to gain insight into the origin and structure of this hybrid zone.
The two species in this complex show a wide range of morphological variation and are difficult to delimit taxonomically. Quercus laurina probably also hybridizes with at least four other red oak species besides Q. affinis (Q. crassifolia, Q. crassipes, Q. mexicana, and Q. rubramenta). According to a recent systematic study, 25 taxa, including species and varieties, are synonymous with Q. laurina and nine with Q. affinis (Valencia, 1994
). An analysis of phenology, wood anatomy, foliar architecture, and pollen ultrastructure revealed that few characters are consistently differentiated between both species across the whole range of their geographical distribution (Valencia, 1994
). Morphological intergradation occurs in localities situated in the eastern portion of the Trans-Mexican Volcanic Belt and northern Oaxaca, while individuals from populations outside of these areas usually can be unambiguously determined (Valencia, 1994
). Morphologically representative populations of Q. laurina are distributed along elevations of the Sierra Madre del Sur and the western region of the volcanic belt, at altitudes that vary between 2440 and 3065 m, and morphologically representative populations of Q. affinis are along the Sierra Madre Oriental, with an altitudinal range of 1600–2800 m (Fig. 1). From this pattern of morphological geographic variation, Q. affinis and Q. laurina were hypothesized to be two closely related species that may have diverged in isolation (Q. affinis in the Sierra Madre Oriental and Q. laurina in the Sierra Madre del Sur) probably during the mid- or late Pliocene and entered into secondary contact in the volcanic belt after a period of range expansion favored by climatic conditions at the beginning of the Pleistocene. The climatic pulsations of the Pleistocene probably determined recurrent periods of secondary contact and periods of range contraction and divergence (Valencia, 1994
). According to this hypothesis, as a result of frequent hybridization and introgression during periods of secondary contact, the morphological differences between the two species have been obscured in some localities (Valencia, 1994
).
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). In the second case, morphological and genetic intermediacy represents the ancestral state, and apparent parents are the result of divergence from a common gene pool (Beckstrom-Sternberg et al., 1991
). Although sometimes it may be difficult to discriminate between either scenario (Endler, 1977
), features of hybrid zones such as parallel patterns in the changeovers from the character states of one parental population to those of the other for several presumably independent characters across the area of intergradation and nonrandom associations among markers derived from the same parental population in the center of the zone (i.e., linkage disequilibrium) are generally considered strong indications of an origin via secondary contact (Durrett et al., 2000
). Molecular markers can provide a large number of neutral and independent characters that are extremely useful in the genetic analysis of hybrid zones (Rieseberg and Ellstrand, 1993
). Compared to allozymes, markers such as AFLP or RAPD are more appropriate for the study of oak hybrid zones, because they have usually provided better discrimination between closely related, hybridizing oak species (Bodénès et al., 1997
; Coart et al., 2002
). RAPD markers have already been used in the study of oak hybrid zones (Howard et al., 1997
). In this study we measured foliar attributes to characterize phenotypic differentiation between isolated populations of Q. affinis and Q. laurina, identified several RAPD markers that showed substantial frequency variation between these populations, and then used these traits to assess the structure of morphological and genetic variation at a macrogeographic level, which included the distribution area of both species and the intergradation zone. The particular goals were (a) to determine if the hypothesis of a secondary hybrid zone between Q. affinis and Q. laurina is supported, (b) to assess the degree of congruence between morphological and molecular variation, and (c) to gain insight into the macrogeographic spatial structure of the intergradation zone.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Fourteen other populations situated along the volcanic belt (most of them in the eastern region) and northern Oaxaca with various degrees of morphological intergradation were also chosen for sampling (Table 1, Fig. 1). The populations were numbered according to a geographic gradient that reflects their position relative to the distribution areas of the two species and the intergradation zone. This was done by jointly considering localities' latitude and longitude. In this way populations follow and order from more western–southern populations to more eastern–northern populations.
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RAPD markers
Markers that could differentiate between the two species were developed through randomly amplified polymorphic DNA (RAPD). DNA of individuals from a morphologically representative population of each species (Zacualtipán [16] and Tequila [1], respectively; Table 1) was amplified using 131 10-bp random oligonucleotides (Series A–L; Operon Technologies, Alameda, California, USA). Satisfactory amplifications were obtained with 94 of these primers, from which 79 gave reproducible results, according to a second round of assays. In total, 711 fragments were consistently amplified in both series of assays. From these 711 bands nine, produced by seven primers, had substantial differences in frequency between the two species (Table 2). The reproducibility of these nine markers was corroborated in a third round of assays, and their presence/absence was later scored in all individuals.
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with only minor modifications. Isolated DNA was stored in deionized water at –20°C. The concentration of DNA in solution was determined with a DNA fluorometer (Hoefer Pharmacia Biotech, San Francisco, California, USA), following procedures supplied by the manufacturer. Amplification reactions were carried out in a 25-µL mix containing 10 ng template DNA, 50 mM KCl, 10 mM Tris-HCl; pH 9, 0.1% Triton x-100, 2 mM MgCl2, 0.1 mM each dNTP, 0.2 µM of a single 10-mer primer, and 1 unit Taq polymerase (Gibco/Invitrogen, San Diego, California, USA). The thermal cycling program was run on a MJ Research (Waterton, Massachusetts, USA) thermal cycler. The program consisted of 45 cycles, each at 94°C for 1 min, annealing at 36°C for 1 min, and extension at 72°C for 2 min. A final extension at 72°C for 15 min was included. The amplification products were electrophoresed in 1.5% (m/v) agarose gels with TBE buffer at 200 V for 2 h and stained with ethidium bromide. Gels with amplification fragments were visualized and photographed under UV light. Molecular mass of the RAPD bands was estimated by reference to a 123-bp ladder (Gibco/Invitrogen, San Diego, California, USA), with aid of the Alpha Ease Version 4 program (Alpha Innotech, San Leandro, California, USA).
Morphological analyses
The following morphological variables were quantified in 10 randomly chosen leaves from each individual: total length (TL), lamina length (LL), petiole length (PL), maximal width (MW), distance from the base of the leaf to the point of maximal width (PMW), and teeth number (TN). Additionally, the ratios of PL/TL, MW/LL, and PMW/LL were calculated. Individual tree means were obtained for each variable and used in further analysis.
Data analysis
Because none of the markers identified as useful was completely diagnostic, a maximum likelihood estimate of hybrid index scores was used, instead of the conventional arithmetic index employed when completely diagnostic markers are available. The algorithm used was the one developed by Hardig et al. (2000)
specifically for RAPD markers (M. Morgan, Washington State University, personal communication). The program standardizes the resulting scores to range between zero and one. In the program, populations Tequila and Zacualtipán represented Q. laurina and Q. affinis, respectively. The frequency of the nine RAPD markers in these two populations thus constituted the end points for calculating hybrid index scores of all plants. These two populations constitute geographical extremes, are morphologically representative of their respective species, and had the largest frequency differences in the nine RAPD markers.
Discriminant function analysis (Tabachnick and Fidell, 1989
) was used to assess multivariate morphological differentiation between representative populations of Q. affinis and Q. laurina. Individuals from populations Tequila and Zacualtipán were first analyzed to obtain a canonical discriminant function. Discriminant scores calculated with this function were then obtained for trees from all populations.
To identify geographical patterns of variation in the genetic and morphological composition of populations, product-moment correlations (Sokal and Rohlf, 1995
) were calculated for the populations' hybrid index scores and morphological discriminant scores with each localities' latitude and longitude.
We calculated pairwise correlations among the frequencies of the RAPD markers on a population-by-population basis, as well as among frequencies of RAPD markers and mean values of morphological characters to determine possible associations in the patterns of change of these presumably independent characters across the area of intergradation that may indicate an origin for this area from secondary contact between the two oak species. To better visualize the patterns, plots for the frequency of markers that had high correlation coefficients were constructed, with populations following their order in the macrogeographic gradient. To ease the comparison between RAPD marker frequencies and morphological characters in these plots, values of morphological characters were transformed to range between zero and unity, with values close to zero representing Q. laurina and values closer to one representing Q. affinis.
To test for linear associations between RAPD markers and morphological variables at the level of individual trees, a multiple regression analysis was performed between maximum likelihood hybrid index scores and the set of morphological variables. Additionally, each morphological variable was regressed against the set of RAPD markers. These analyses were performed on the total set of individuals over all populations and then separately within each population.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The first canonical function derived from discriminant analysis on the morphological traits explained 100% of the variation and provided highly significant discrimination (Wilks' lambda = 0.105; df = 18; P < 0.001) between Q. laurina individuals from population Tequila and Q. affinis individuals from population Zacualtipán. The standardized canonical discriminant function coefficient of each morphological variable is given in Table 3. The variable with the highest coefficient was petiole length. Scores for trees from population Tequila calculated with this canonical discriminant function ranged from –5.911 to –2.320, while Q. affinis trees from population Zacualtipán had scores that varied between 0.108 and 4.945. Figure 2B shows the frequency distributions of morphological discriminant scores in all populations. Individuals with scores similar to those observed in morphologically representative populations of Q. laurina were preponderant in more western and/or southern populations, with an increasing proportion of intermediate individuals towards the intergradation zone and a majority of individuals with Q. affinis morphology in northeastern populations.
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Pairwise correlations of the frequency of RAPD markers across populations are presented in Table 4. All correlations were of the expected sign, that is, negative frequency correlations among semidiagnostic markers of the two species and positive correlations among markers of the same species. Eleven of 36 (31%) of these comparisons were significant. As expected from these correlations, the patterns of frequency changeover on a population-by-population basis among several RAPD fragments were relatively parallel (Fig. 3). Significant associations were also found between the frequency of individual RAPD markers and population mean values of morphological characters (Table 5). Marked patterns of parallel change were found between the frequency of marker A5–7 and mean teeth number and between marker B17–4 and mean petiole length (Fig. 3).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Leaf morphology might certainly experience natural selection by the environment, but under a primary origin scenario, to explain the correlated changeover patterns observed here would require physical linkage of most RAPD markers with loci controlling foliar traits, which seems improbable a priori. Although congruent in general, the frequency changeovers of only a few marker pairs had high correlation coefficients and were patently parallel. This could indicate that some differential introgression between markers has occurred after secondary contact. Several studies have shown that differential introgression of neutral markers in secondary zones can occur and depends on linkage to loci under selection and time since contact (Durrett et al., 2000
). Localized and parallel introgression of all species-specific markers is expected in very recent contact zones (Rieseberg and Ellstrand, 1993
; Durrett et al., 2000
). In taxa with a longer history of interaction, chromosome segments containing genes with advantageous or neutral effects in heterospecific backgrounds may have a more widespread introgression, while negatively selected ones will be impeded from crossing species' boundaries and will remain localized. This may create nonconcordant patterns of variation among different markers (Martinsen et al., 2001
). In the original hypothesis of a secondary contact between Q. affinis and Q. laurina, and based on biogeographic considerations and paleobotanical evidence, Valencia (1994)
postulated that genetic interactions between these two species probably date from the beginning of the Pleistocene. Even if this estimation is not very accurate, it nevertheless seems like the hybrid zone between these two species is not very recent. It is thus probable that enough time has elapsed for some differential introgression to occur.
In this study, we observed significant global multivariate correlations between phenotypic and molecular variation. However, these correlation coefficients were quite low, and for most populations, the degree of genetic and morphological intermediacy indicated by frequency distributions of hybrid index scores and morphological discriminant scores (Fig. 2A and B) were only partially congruent. In general, the number of morphologically intermediate individuals is smaller than the number of genetically intermediate individuals and, in fact, clear incongruence is observed in populations Cerro Navajas [12], Puerto Aire [8], and El Chico [10], in which nearly all individuals appeared genetically intermediate or even closer to Q. affinis, but were morphologically more similar to isolated Q. laurina. Other studies of hybridization between oak species have also found incongruence or only partial congruence between morphological and molecular variation. For example, although nuclear and cytoplasmic markers support extensive genetic exchange between the two species in the Q. petraea-Q. robur complex, several studies have found that morphologically intermediate individuals are very infrequent (Bacilieri et al., 1996a
; Kremer et al., 2002
). Possible explanations for this phenomenon include maternal effects (i.e., hybrids are more similar to the species of their maternal parent), as well as selection against intermediate forms (Bacilieri et al., 1996a
; Kremer et al., 2002
). In a mixed stand of Q. lobata and Q. douglasii, Craft et al. (2002)
found phenotypically intermediate trees that had little evidence of mixed ancestry according to microsatellites. On the other hand, only one of four trees with the highest probability of hybrid ancestry was intermediate in appearance. In contrast, a remarkably high correspondence between morphological variables and genetic markers was found in a hybrid zone between Q. gambelli and Q. grisea in New Mexico (Howard et al., 1997
). It is possible that the result was obtained because a highly optimized set of discriminant markers was used and the data were subjected to a canonical correlation analysis, which resulted in a high correlation between both first canonical variates on markers and morphological traits.
Incongruence between morphology and molecular markers has been observed many times in plant hybrid zones (Rieseberg and Ellstrand, 1993
), and in general, introgression of morphological characters is more restricted than introgression of molecular markers (Rieseberg and Wendel, 1993
). It is thought that recombination of adaptively relevant morphological or physiological characters with a polygenic basis may result in individuals with unfit phenotypes, while this is not expected for individuals that combine neutral markers from different species (Shoemaker et al., 1996
). Several times it has been asserted that hybridizing oak species are capable of remaining morphologically or ecologically different in the face of considerable introgression (Whittemore and Schaal, 1991
; Howard et al., 1997
) and this may be also occurring in the case of Q. affinis and Q. laurina, despite a probably ancient event of secondary contact between them. It is possible that species distinctness in hybridizing oaks is maintained because natural selection operates against the exchange of genes that constitute the basis of functional divergence (i.e., differential adaptation) between species, while considerable gene flow can occur at the rest of the genome, as suggested by Wu (2001)
in the genic view of the process of speciation. Which ecological factors, as well as which traits and genes may account for the functional divergence between the two oaks studied here merits considerable future attention.
Another major theme in the literature on hybrid zones concerns the organization of such areas as simple clines or geographically more complex mosaics (Rand and Harrison, 1989
). In the first case, a gradual transition is observed between the character states typical of each parental population (Barton and Hewitt, 1989
). In our case, frequency distributions of hybrid index scores and morphological discriminant scores were significantly correlated to geographic coordinates and change (although with weak concordance, as discussed before) from isolated populations of Q. laurina to isolated populations of Q. affinis with a series of more or less intermediate populations in between. This would argue in favor of a clinal structure for this hybrid zone. However, the frequencies of single RAPD markers as well as the values of morphological variables seem to follow a more complex pattern of change across localities than what would be expected for a clinal hybrid zone. In general, mosaic zones can be characterized as patches of pure species populations and mixed populations scattered across a zone of overlap (Howard et al., 1997
). At this moment, we cannot firmly argue in favor of such structure for the hybrid zone between Q. affinis and Q. laurina, because we primarily focused on populations that previously showed some morphological evidence of intergradation. The sampled populations are in fact scattered among populations that were judged to be pure according to the appearance of herbarium specimens, but it would nevertheless be necessary to include a sample of such populations in a larger survey using molecular markers to better understand the structure of this hybrid zone.
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Bacilieri R. A. Ducousso A. Kremer 1996a Comparison of morphological characters and molecular markers for the analysis of hybridization in sessile and pedunculate oak. Annales des Sciences Forestieres 53: 79-91
Bacilieri R. A. Ducousso R. J. Petit A. Kremer 1996b Mating system and asymmetric hybridization in a mixed stand of European oaks. Evolution 50: 900-908[CrossRef][ISI]
Bacon J. R. R. Spellenberg 1996 Hybridization in two distantly related Mexican black oaks Quercus conzattii and Quercus eduardii (Fagaceae: Quercus: Section Lobatae). Sida 17: 17-41
Barton N. H. G. M. Hewitt 1989 Adaptation, speciation and hybrid zones. Nature 341: 497-503[CrossRef][Medline]
Beckstrom-Sternberg S. M. L. H. Rieseberg K. Doan 1991 Gene lineage analysis in populations of Helianthus niveus and H. petiolaris (Asteraceae). Plant Systematics and Evolution 175: 125-138[CrossRef][ISI]
Bodénès C. S. Joandet F. Laigret A. Kremer 1997 Detection of genomic regions differentiating two closely related oak species Quercus petraea (Matt.) Liebl. and Quercus robur L. Heredity 78: 433-444[CrossRef][ISI]
Borgardt S. J. K. B. Pigg 1999 Anatomical and developmental study of petrified Quercus (Fagaceae) fruits from the Middle Miocene, Yakima Canyon, Washington, USA. American Journal of Botany 86: 307-325
Brophy W. B. D. R. Parnell 1974 Hybridization between Quercus agrifolia and Quercus wislizenii (Fagaceae). Madroño 22: 290-302
Bruschi P. G. G. Vendramin F. Bussotti P. Grossoni 2000 Morphological and molecular differentiation between Quercus petraea (Matt.) Liebl. and Quercus pubescens Willd. (Fagaceae) in northern and central Italy. Annals of Botany 85: 325-333
Burger W. C. 1975 The species concept in Quercus. Taxon 24: 45-50[CrossRef]
Coart E. V. Lamote M. De Loose E. Van Bockstaele P. Lootens I. Roldán-Ruiz 2002 AFLP markers demonstrate local genetic differentiation between two indigenous oak species [Quercus robur L. and Quercus petraea (Matt.) Liebl.] in Flemish populations. Theoretical and Applied Genetics 105: 431-439[CrossRef][ISI][Medline]
Cooperrider M. 1957 Introgressive hybridization between Quercus macrocarpa and Quercus velutina in Iowa. American Journal of Botany 44: 804-810[CrossRef][ISI]
Craft K. J. M. V. Ashley W. D. Koenig 2002 Limited hybridization between Quercus lobata and Quercus douglasii (Fagaceae) in a mixed stand in central and coastal California. American Journal of Botany 89: 1792-1798
Daghlian C. P. W. L. Crepet 1983 Oak catkins, leaves and fruits from the Oligocene Catahoula Formation and their evolutionary significance. American Journal of Botany 70: 639-649
Dumolin-Lapegue S. A. Kremer R. J. Petit 1999 Are chloroplast and mitochondrial DNA variation species independent in oaks?. Evolution 53: 1406-1413[CrossRef][ISI]
Durrett R. L. Buttel R. Harrison 2000 Spatial models for hybrid zones. Heredity 84: 9-19
Endler J. A. 1977 Geographic variation, speciation and clines. Princeton University Press, Princeton, New Jersey, USA
Ferrusquia-Villafranca I. 1993 Geology of Mexico: a synopsis. In T. P. Ramammoorthy, R. Bye, A. Lot, and J. Fa [eds.], Biological diversity of Mexico: origins and distribution, 3–107. Oxford University Press, New York, New York, USA
Guttman S. I. L. A. Weigt 1989 Electrophoretic evidence of relationships among Quercus (oaks) of eastern North America. Canadian Journal of Botany 67: 339-351
Hardig T. M. S. J. Brunsfeld R. S. Fritz M. Morgan M. Orians 2000 Morphological and molecular evidence for hybridization and introgression in a willow (Salix) hybrid zone. Molecular Ecology 9: 9-24[CrossRef][Medline]
Hardin J. W. 1975 Hybridization and introgression in Quercus alba. Journal of the Arnold Arboretum 56: 336-363[ISI]
Hokanson S. C. J. G. Isebrands R. J. Jensen J. F. Hancock 1993 Isozyme variation in oaks of the Apostle Islands in Wisconsin: genetic structure and levels of inbreeding in Quercus rubra and Q. ellipsoidalis (Fagaceae). American Journal of Botany 80: 1349-1357[CrossRef][ISI]
Howard D. J. R. W. Preszler J. Williams S. Fenchel W. J. Boecklen 1997 How discrete are oak species? Insights from a hybrid zone between Quercus grisea and Quercus gambelli. Evolution 51: 747-755[CrossRef][ISI]
Jensen R. J. S. C. Hokanson J. G. Isebrands J. F. Hancock 1993 Morphometric variation in oaks of the Apostle Islands in Wisconsin: evidence of hybridization between Quercus rubra and Q. ellipsoidalis (Fagaceae). American Journal of Botany 80: 1358-1366[CrossRef][ISI]
Kleinschmit J. R. G. R. Bacilieri A. Kremer A. Roloff 1995 Comparison of morphological and genetic traits of pedunculate oak (Q. robur L.) and sessile oak (Q. petraea (Matt.) Liebl). Silvae Genetica 44: 256-269[ISI]
Kremer A. et al 2002 Leaf morphological differentiation between Quercus robur and Quercus petraea is stable across western European mixed oak stands. Annals of Forest Science 59: 777-787[CrossRef][ISI]
Lefort F. G. C. Douglas 1999 An efficient micro-method of DNA isolation from mature leaves of four hardwood tree species Acer, Fraxinus, Prunus and Quercus. Annals of Forest Science 56: 259-263[CrossRef][ISI]
Martinsen G. D. T. G. Whitham R. J. Turek P. Keim 2001 Hybrid populations selectively filter gene introgression between species. Evolution 55: 1325-1335[CrossRef][ISI][Medline]
Nixon K. C. 1993a The genus Quercus in Mexico. In T. P. Ramammoorthy, R. Bye, A. Lot, and J. Fa [eds.], Biological diversity of Mexico: origins and distribution, 447–458. Oxford University Press, New York, New York, USA
Nixon K. C. 1993b Infrageneric classification of Quercus (Fagaceae) and typification of sectional names. Annales des Sciences Forestieres 50: 255-345
Palmer E. J. 1948 Hybrid oaks of North America. Journal of the Arnold Arboretum 29: 1-48
Rand D. M. R. G. Harrison 1989 Ecological genetics of a mosaic hybrid zone: mitochondrial, nuclear and reproductive differentiation of crickets by soil type. Evolution 43: 432-449[CrossRef][ISI]
Rieseberg L. H. N. C. Ellstrand 1993 What can molecular and morphological markers tell us about plant hybridization?. Critical Reviews in Plant Sciences 12: 213-241[CrossRef][ISI]
Rieseberg L. H. J. F. Wendel 1993 Introgression and its consequences in plants. In R. G. Harrison [ed.], Hybrid zones and the evolutionary process, 70–109. Oxford University Press, New York, New York, USA
Samuel R. W. Pinsker F. Ehrendorfer 1995 Electrophoretic analysis of genetic variation within and between populations of Quercus cerris, Q. pubescens, Q. petraea and Q. robur (Fagaceae) from Eastern Austria. Botanica Acta 108: 290-299[ISI]
Shoemaker D. D. K. G. Ross M. L. Arnold 1996 Genetic structure and evolution of a fire ant hybrid zone. Evolution 50: 1958-1976[CrossRef][ISI]
Sokal R. R. F. J. Rohlf 1995 Biometry: the principles and practice of statistics in biological research. Freeman and Company, New York, New York, USA
Tabachnick B. G. L. S. Fidell 1989 Using multivariate statistics. Harper Collins, New York, New York, USA
Valencia S. 1994 Contribución a la delimitación taxonómica de tres especies del género Quercus subgénero Erythrobalanus. Tesis de Maestría, Facultad de Ciencias, Universidad Nacional Autónoma de México, México, D.F., México
Van Valen L. 1976 Ecological species, multispecies and oaks. Taxon 25: 233-239[CrossRef][ISI]
Whittemore A. T. B. A. Schaal 1991 Interspecific gene flow in sympatric oaks. Proceedings of the National Academy of Sciences, USA 88: 2240-2544
Wu C. I. 2001 The genic view of the process of speciation. Journal of Evolutionary Biology 14: 851-865[CrossRef][ISI]
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