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Population Biology |
Centro de Investigaciones en Ecosistemas, UNAM (Universidad Nacional Autónama de México), Campus Morelia, Antigua Carretera a Pátzcuaro No. 8701, Col. San José de la Huerta, C.P. 58190, Morelia, Michoacán, México
Received for publication July 10, 2003. Accepted for publication May 20, 2004.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Fagaceae • hybrid zones • hybridization • leaf morphology • Mexico • Quercus • RAPDs
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). This process produces new genetic combinations by the introduction of semi-compatible genes into another genotype, upon which interaction of environment and genetic variation can isolate a novel taxon from parental types. Hybrids may be defined as species, subspecies, variants, or races, depending on the degree of divergence (Futuyma, 1998
). Interspecific gene transfer is an important evolutionary force, because the genetic material introduced by introgression exceeds that which is produced directly by mutation (Anderson, 1949
).
The genus Quercus (Fagaceae) is one of the most diversified groups of temperate trees with more than 500 species distributed worldwide (Nixon, 1993
). Hybridization and hybrid zones are common among oaks (Trelease, 1924
; Palmer, 1948
; Muller, 1952
; Tucker, 1961
; Cottam et al., 1982
; Jensen et al., 1993
; Spellenberg, 1995
; Howard et al., 1997
; Ishida et al., 2003
). However, despite the perception that hybrid zones are well documented among oaks, few comparative analyses of oak hybrid zones have used both morphological characters and genetic markers (Howard et al., 1997
).
Hybridization in oaks was initially detected based on morphological characters (Stebbins et al., 1947
; Barlett, 1951
; Tucker, 1961
; Benson et al., 1967
; Hardin, 1975
; Cottam et al., 1982
; Rushton, 1993
). Leaf morphology in particular has been useful to demonstrate hybridization (Bacon and Spellenberg, 1996
). However, in some cases morphological characters alone do not confirm unequivocally the existence of hybridization (Bacilieri et al., 1995
; Manos et al., 1999
; Mayol and Rosselló, 2001
) requiring other methods such as DNA markers (Crawford et al., 1993
; Rieseberg and Ellstrand, 1993
). Random amplified polymorphic DNA (RAPD) markers have been particularly successful in the detection of interspecific hybridization and introgression in plants (Arnold et al., 1991
; Arnold, 1993
; Crawford et al., 1993
; Cruzan and Arnold, 1993
; Marsolais et al., 1993
; Fritz et al., 1994
; Smith et al., 1996
; Samuel, 1999
).
Mexico is considered one of the centers of diversification of the genus Quercus (oaks) (Muller and McVaugh, 1972
; Rzedowski, 1978
; González, 1993
; Nixon, 1993
), with 135– 150 species that include 86 endemics (Nixon, 1993
). However, hybridization has only recently been reported for some species of Mexican oaks (McVaugh, 1974
; Boecklen and Spellenberg, 1990
; Spellenberg, 1992
, 1995
; Spellenberg and Bacon, 1996
; González-Rodríguez et al., 2004
, in press
). The taxonomy and evolutionary relationships of Mexican oaks are currently being studied, and some species complexes formed by potential parental species and putative hybrids have been recently detected by oak specialists. We chose two red oak species (subg. Erythrobalanus) for this study, Q. crassifolia H. & B. and Q. crassipes H. & B. These species have noticeable differences in several morphological characters (Romero, 1993
) when they form allopatric pure stands. However, intermediate trees with atypical leaf shapes are observed when both species occur in sympatry, suggesting that hybridization may explain the observed variations. It is important to indicate that other oak species that can be considered as reasonable putative parents as judged from the morphological features of Q. dysophylla do not occur in the area. The taxonomic status of Q. dysophylla is still under discussion; some authors consider this species as a hybrid formed by Q. crassifolia x Q. crassipes (K. Nixon and S. Valencia, Cornell University and UNAM [Universidad Nacional Autónama de México], respectively, personal communication), while others recognize it as a different species (Romero, 1993
; Zavala Chávez, 1995).
In this paper, we describe and compare the patterns of morphological and genetic variation of the Q. crassifolia x Q. crassipes complex, document the structure of overlapping zones and hybridization in the Eje Neovolcánico and Central Mexico, and assess the taxonomic distinctness of the two species and the putative hybrid.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Seven sympatric zones were chosen in the Eje Neovolcánico and Sierra Madre Oriental, where Q. crassifolia and Q. crassipes overlap geographically: Cantera, Canalejas, Tlaxco, Acajete, Esperanza, Agua Blanca, and Palo Bendito. These localities were chosen because they contain the highest numbers of intermediate individuals of this complex. Two localities were also chosen for each parental species, where they are dominant and no hybrids were observed (Fig. 1). In general, the hybrids occur in a very low frequency sporadically interspersed and near to the putative parents. Intermediate trees occur in more disturbed habitats but we cannot assess the preference of hybrids for some type of habitats (e.g., type of soils, forest gaps). It is rare to find intermediate trees outside of the contact zones. No evidence exists on another oak species hybridizing with trees of the species studied. When other oak species were found, they were white oaks that cannot hybridize with red oak species.
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; Williams et al., 1990
), and the polymerase chain reaction (PCR). Forty-eight 10-base pair (bp) primers of random sequence (Kits A, B, C; Operon Technologies, Alameda, California, USA) were tested to find specific, diagnostic markers for each parental species. Diagnostic markers are those that are present in all individuals of one species and absent in a second species, while species-specific markers are those unique to one species but not necessarily present in all individuals within the species (Howard et al., 1997
). Lastly, 250 individuals were tested using six primers (four species-specific markers [two for Q. crassifolia, OPA-09 and OPA-13, and two for Q. crassipes, OPB-01 and OPC-06], and two diagnostic markers [Q. crassifolia, OPA-14, and Q. crassipes, OPB-18]). DNA fragments were separated by electrophoresis on 1.5% agarose gel, stained with ethidium bromide, and developed on a UV table. The molecular mass of the DNA fragments was estimated with a 1-kilo base (kb) DNA ladder.
Statistical analysis
Nested variance analyses were conducted (ANOVA) to determine the effects of oak species, locality, and individual (tree) on the morphological leaf variability of each of the 17 studied characters (Table 1). Hybrids were not included in this analysis. Trees were considered as a random factor nested within species, because they were representative of each population. Percentage data were corrected as X = arcsin (%)
, and discontinuous data were transformed as X = (x) + 0.5 (Zar, 1999
).
To quantify variation in leaf morphology among oak species and hybrids, we randomly selected 30 leaves from vouchered specimens, and all the 17 characters were measured. All morphological characters were used for discriminant analysis to assess the most useful character for taxonomic discrimination between Q. crassifolia and Q. crassipes and to determine how leaf morphological characters separate individuals into groups. Seventeen characters were measured for the character count procedure to determine hybrids with intermediate leaf morphology of the Q. crassifolia x Q. crassipes complex following the procedure of Wilson (1992)
. Variation in size and shape due to shape alone was quantified using the ratios of the sums of eigen values from the discriminant analysis (Darroch and Mosimann, 1985
).
In the seven mixed stands, the Anderson hybrid index (Anderson, 1949
, 1953
) was used to identify intermediate individuals and possible backcrosses. A histogram for each mixed stand was obtained. The Anderson hybrid index was calculated using the 17 morphological characters because they demonstrated differences between parental species. The representative characters of Q. crassipes received a rank of 2; Q. crassifolia characters were assigned a rank of 0; while intermediate characters were assigned a rank of 1 (Wilson, 1992
).
A general cluster diagram for all zones was obtained, including pure and mixed stands. STATISTICA 6.0 for Windows was used for all the statistical analyses (Statsoft, 1998
).
The maximum likelihood (ML) hybrid index score from RAPD analysis was calculated using Hardig-Hybrid software (Hardig et al., 2000
). This index is useful to identify intermediate individuals, showing backcrosses as well as the structures of hybrid swarms. The results were represented in a frequency histogram for each mixed stand and for the pure sites. A Mantel Z-test matrix and Tools for Population Genetic Analyses (TFPGA, version 1.3) were used to test isolation by distance, as well as to create a general cluster diagram for the mixed stands and the four pure zones (Miller, 1997
).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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In a global cluster analysis based on morphological leaf traits for the seven mixed stands and four pure populations (two for Q. crassifolia and two for Q. crassipes), the populations having the same parental species were more similar to each other. For the five hybrid zones located on the Eje Neovolcánico (mixed stands from 1 to 5), nearness of the hybrid zones to the allopatric putative parent correlated with increasing similarity of the complex to the parental species. Lastly, mixed stands 6 and 7, located on the Sierra Madre Oriental, were more similar to Q. crassifolia (Fig. 3, left).
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Genetic analysis (RAPDs) of parental and hybrid plants
We used six primers to estimate the genetic status of Q. crassifolia and Q. crassipes plants morphologically identified as "pure" or "hybrid" plants. These primers yielded 49 distinct markers (bands). The RAPD analysis proved to be a powerful tool for characterizing hybrid individuals between Q. crassifolia and Q. crassipes. The analysis of the ML hybrid index using six RAPD markers supported the field identification of 250 plants (Fig. 5). Individuals A10 (Cantera); A1, A7, and A8 (Tlaxco); and A5 and A6 (Palo Bendito) were classified as Q. crassifolia in the field, but the RAPD showed that they were backcrosses toward Q. crassifolia. Individuals B4 and B8 (Tlaxco) and B2 (Esperanza) were originally marked as Q. crassipes, but RAPDs analysis confirmed that they were backcrosses toward Q. crassipes. The individuals AB9 (Agua Blanca) and AB7 (Tlaxco) were marked as hybrids, but RAPDs and subsequent field examinations showed that they were individuals of Q. crassifolia and Q. crassipes, respectively. Individuals AB10 (Cantera), AB1 (Agua Blanca), and AB3, AB5, and AB7 (Palo Bendito) were classified as hybrid plants, but the molecular analysis indicated that they were backcrosses toward Q. crassifolia. Lastly, AB3, AB6, and AB9 (Tlaxco) ; AB4, AB5, AB8, AB9, and AB10 (Acajete); and AB2 and AB10 (Esperanza) were identified as hybrids, but RAPD data showed that they were backcrosses toward Q. crassipes (Fig. 5).
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The mean ML hybrid index for Q. crassifolia individuals was 0.85 (SD 0.07), for Q. crassipes was 0.08 (SD 0.06), and for the hybrids, 0.48 (SD 0.09).
The Hardig hybrid index showed the same general pattern as the Anderson hybrid index (see earlier). No introgression was registered only in Canalejas (Fig. 5).
The cluster analysis for genetic (RAPDs) and morphological data showed that these are very similar. The allopatric zones (two zones for Q. crassifolia and two for Q. crassipes) were located at the edges, while the seven hybrid zones were located between them (Fig. 3).
The Mantel Z-test matrix showed that no correlation exists between the geographic distances and the genetic distances for any of the species (Q. crassifolia, r = 0.37, P > 0.05 ; and Q. crassipes, r = 0.14, P > 0.05).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Interspecific hybridization and shared ancestral polymorphisms are two of the most common explanations for the observed pattern of variation (Jensen et al., 1993
; Kleinschmit et al., 1995
; Bruschi et al., 2000
). Quercus crassifolia and Q. crassipes form hybrids, but they remain morphologically distinct in their allopatric and sympatric distributions. All the examined morphological leaf characters in these species differed significantly by localities, populations, and individuals. Relatively few diagnostic molecular markers differentiated between Q. crassifolia and Q. crassipes. However, these markers demonstrated geographic consistency in support of the morphological evidence, indicating that each species is distinct and that each has some degree of genetic cohesiveness. Furthermore, the character count procedure has allowed us to confirm statistically that Q. dysophylla is the result of hybridization between Q. crassifolia and Q. crassipes in the seven hybrid zones. The ordination analysis also demonstrated that hybrids presented intermediate morphology between the parental species and that leaf shape explains a major percentage of variation.
Quercus crassifolia ranges from the Sierra Madre Occidental (SMOc) to the center of Mexico along the Eje Neovolcánico, whereas Q. crassipes ranges from the Sierra Madre Oriental (SMOr) to the Eje Neovolcánico, where both species overlap producing hybrid zones. The Eje Neovolcánico, an orographic system that traverses the central part of the country in an east–west direction, is considered geologically the youngest mountain range in Mexico and contains valleys higher than 2000 m in altitude and the tallest mountains in Mexico (Ferrusquia-Villafranca, 1993
). Phylogeographic studies are in progress to understand the process of migration and the colonization routes of this oak complex, as has been done for other oak species (e.g., Dumolin-Lapègue et al., 1997
).
The genetic results indicate that the introgression process is present in both species, but the direction changes depending on the localization of the hybrid zone. The hybrid zones closest to the SMOc (Cantera and Canalejas) registered unidirectional introgression towards Q. crassifolia, while the hybrids from the intermediate locality between the two mountain ranges (Tlaxco) showed bidirectional introgression, and the hybrids from the two closest localities to the SMOr registered unidirectional introgression towards Q. crassipes. These findings suggest that the closeness of hybrids to an allopatric site of either parental species is directly related to their similarity and vice versa. Thus, the Eje Neovolcánico acts as a corridor where the proximity to an allopatric site favors the introgression of the hybrid towards the parental species, increasing its variation from the species with which it is maintaining a genetic exchange, diluting the limits with the parental species in the allopatric site. Lastly, the two hybrid zones located north of Tlaxco (SMOr) showed unidirectional introgression towards Q. crassifolia. These results confirm that patterns of variation in oaks do not follow simple monotonic clines (e.g., Barton and Hewit, 1985
) but form complex mosaic zones characterized by patches of pure populations and mixed populations scattered across a zone of overlap (Howard et al., 1997
). A bidirectional hybrid zone was detected for Q. crassifolia and Q. crassipes.
In the seven hybrid zones studied along the Eje Neovolcánico, where intermediate plants are mixed with their parental species, hybrids are rare and they are in a narrow contact zone between well-differentiated taxa. The presence of hybrid individuals in the hybrid zones was very low (between 10 and 17 trees), requiring an extensive field search. Oak hybrids are produced in an isolated and sporadic manner and they may introgress with parental species (Bacon and Spellenberg, 1996
). Hybrid zones with high levels of disturbance (i.e., Canalejas, Acajete, and Esperanza) were the ones with the highest number of hybrid individuals (mostly juveniles). Disturbances produced by human activities such as logging, deforestation, fires, and agriculture, may enhance the establishment of hybrids as they modify reproductive barriers (Arnold et al., 1990
; Klier et al., 1991
).
Our results suggest that the sympatric zones of Q. crassifolia and Q. crassipes are mosaic hybrid zones as proposed by Howard (1982
, 1986
) and Harrison (1986
, 1990
), because of the patchy distribution pattern of the parental species in sympatric and allopatric sites and the lack of a gradual transition from Q. crassipes to Q. crassifolia. It is important to mention that hybrid plants were less frequent than putative parents in the mixed stands and that Q. crassipes prefers drier habitats and lower sites than Q. crassifolia. Ecological divergence rather than genetic incompatibility may maintain hybrid zones (Jiggins and Mallet, 2000
) by causing local adaptations to different environmental conditions (e.g., Howard et al., 1997
).
In summary, we found that molecular markers (RAPD) and morphological leaf traits are highly coincident and support the phenomenon of hybridization between Q. crassifolia and Q. crassipes complex (Fig. 3). Inasmuch as hybridization was evident, both species remain distinct in mixed stands. We also observed that the Eje Neovolcánico acts as a corridor where proximity to an allopatric site favors the introgression of the hybrid with its parental species, increasing its divergence from the species with which it maintains a genetic exchange, and thus diluting the limits with parental species in the allopatric site. Hybrid plants constitute a heterogeneous group in which many individuals were F1 and others appeared as backcrosses of Q. crassifolia or Q. crassipes, depending on the locality.
Our data and field observations suggest that the sympatric zones of Q. crassifolia and Q. crassipes must be considered as mosaic hybrid zones (e.g., Howard, 1982
, 1986
; Harrison, 1986
, 1990
), because of the patchy distribution pattern of the parental species in sympatric and allopatric sites, and there is not a gradual transition from Q. crassipes to Q. crassifolia. Finally, we suggest that Q. dysophylla does not deserve the status of species but it must be recognized as an entity of potential evolutionary importance, named as Quercus x dysophylla Benth. pro sp.
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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