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Population Biology |
2Department of Biological Sciences, University of Illinois at Chicago, 845 West Taylor Street, Chicago, Illinois 60607 USA; 3Hastings Natural History Reservation, University of California, Berkeley, 38601 E. Carmel Valley Road, Carmel Valley, California 93924 USA
Received for publication March 14, 2002. Accepted for publication May 23, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Bayesian clustering • California oaks • Fagaceae • hybridization • microsatellites • Quercus douglasii • Quercus lobata
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Natural hybrids form between species that are clearly distinguishable in morphology, physiology, and ecology. The propensity for oaks to hybridize, together with extensive edaphic and clinal variation, have led species concepts to be challenged in Quercus (Burger, 1975
; Van Valen, 1976
). Clearly, infertility between species cannot fully explain why closely related oaks usually remain distinct even in areas of sympatry.
Here we used nuclear DNA microsatellite markers to study hybridization of two widely overlapping species, Q. lobata and Q. douglasii, growing in a mixed stand in California. These species are closely related and have been reported to hybridize (Little, 1979
; Holstein, 1984
), yet are distinct in morphology and ecology. At our study site in central coastal California, Q. lobata and Q. douglasii are found together in extensive mixed woodlands with occasional trees intermediate in appearance.
We applied DNA microsatellite markers to study hybridization between Q. lobata and Q. douglasii. Microsatellites, rather than other available molecular markers, were chosen for several reasons. First, cytoplasmic genomes such as chloroplast (cp) and mitochondrial (mt) DNA variants show high rates of introgression among plant species (Rieseberg and Soltis, 1991
) and may occur in the absence of significant nuclear gene flow (Rieseberg, 1995
). Whittemore and Schaal (1991)
found extensive exchange of chloroplast genomes between white oak species (subgenus Quercus), whereas a nuclear ribosomal marker was species specific. Since then, many reports of cytoplasmic exchange among Quercus species have been made (Petit, Kremer, and Wagner, 1993
; Bacilieri et al., 1996
; Dumolin-Lapegue, Pemonge, and Petit, 1998
; Dumolin-Lapegue, Kremer, and Petit, 1999
), always within the same subgenus but not necessarily between species that are otherwise closely related (Belahbib et al., 2001
). Generally, morphologically recognizable hybrids are rarer in nature than would be predicted from estimates of cytoplasmic gene flow (Whittemore and Schaal, 1991
). Thus, cytoplasmic markers may provide a distorted view of genetic exchange among Quercus species.
Nuclear genes may be more indicative of natural introgression levels and thus more useful for studies of hybridization in plants. Certain nuclear markers, however, may be problematic in Quercus due to the nature of molecular evolution at these loci. Muir, Fleming, and Schlötterer (2001)
report that the ITS2 regions of the ribosomal DNA (rDNA) of the European oaks Q. robur and Q. petraea show no species-specific differences. Three very divergent rDNA families exist in both species and indeed were found within single individuals, limiting their application to hybridization studies.
In contrast, the characteristics of microsatellite markers (highly variable, codominantly inherited length variants) make them well suited for studies of hybridization and introgression (Muir, Fleming, and Schlötterer, 2000
). Their relatively rapid rate of mutation allows for differentiation between closely related species, and differences in allele frequencies as well as species-specific alleles can be used to estimate levels of interspecific gene flow. For example, microsatellite data distinguish between Q. robur and Q. petraea, whereas chloroplast markers, RAPDs, ITS sequences, and allozymes do not (Muir, Fleming, and Schlötterer, 2000
, 2001
).
To date, microsatellites studies in plants have been mostly used for studies of pollination and seed dispersal that involve parentage assignment (Chase et al., 1996
; Dow and Ashley, 1996
, 1998
; Aldrich and Hamrick, 1998
; Streiff et al., 1999
) and studies assessing population genetic structure within species (Reusch, Stam, and Olsen, 2000
; Friar et al., 2001
) rather than for hybridization studies. Before conducting either mating system or population genetic studies in species that co-occur with potentially hybridizing species, however, it is necessary to characterize levels of microsatellite differentiation and exchange between species. This study was undertaken to obtain such information for Q. douglasii and Q. lobata.
Our study differs from others using genetic markers to study hybridization in plants in that we applied a Bayesian clustering approach to identify genetic structure in the mixed population in addition to more conventional analyses. That is, we tested for the presence of population structure in the combined multilocus genotype data without assigning individual trees to "Q. lobata" and "Q. douglasii" or "intermediate." We then asked how well the genetic structure of the mixed population corresponded to species assignments. This approach allows identification of hybrid individuals irrespective of their physical appearance. It also allows evaluation of the statistical significance of clusters, and the origin of individuals can be inferred by calculating the probability that individual multilocus genotypes belong to different genetic clusters, or alternatively, are hybrid in origin (Pritchard, Stephens, and Donnelly, 2000
; Randi et al., 2001
).
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Little, 1979
). It once occurred as the only tree in extensive savannas, but this habitat has largely been cleared for farmland, vineyards, and other development. Quercus lobata also grows in riparian forest and in mixed oak stands in foothill woodlands. It is the largest North American oak with trees 10–25 m tall and 0.5–0.7 m diameter at breast height (dbh) (Munz, 1973
). While valley oaks may live 500 yr, mature stands are typically 100–200 yr old.
Quercus douglasii is also endemic to California, with a distribution that circles the Central Valley, in valleys and foothills of the Coast Ranges and the Sierra Nevada. Communities where Q. douglasii occur range from open savanna to fairly dense woodland. It generally grows shorter and straighter than Q. lobata, ranging in height from 6 to 20 m and from 36 to 60 cm dbh (Burns and Honkala, 1990
).
Study area
Trees were sampled at Hastings Reservation, a 900-ha reserve in the Santa Lucia Mountains of central coastal California. Hastings is located about 40 km inland at an elevation of 460–950 m above sea level and experiences a Mediterranean climate with an extended dry season from June to September. Three species of oak are common at Hastings, Q. lobata, Q. douglasii, and Q. agrifolia. Quercus lobata and Q. douglasii both belong to the "white oak" section Quercus, whereas Q. agrifolia belongs to the distantly related "red oak" section Lobatae (Nixon, 1993
; Manos, Doyle, and Nixon, 1999
). Thus only the two sampled species are candidates for hybridization. Based on vegetation surveys conducted throughout the Reservation, we estimate that Q. douglasii, which occur at densities averaging 69 trees/ha, are approximately three times more abundant than Q. lobata (W. D. Koenig, unpublished data).
Sampling
Mature leaves were collected from 109 Q. lobata and 26 Q. douglasii growing together in a mixed stand within an area of approximately 1.8 km2. Sample sizes between species were different because Q. lobata was being exhaustively sampled for part of a pollination study. In addition to these trees, five individuals sampled were identified by one of us with extensive experience with oaks in this area (W. D. Koenig) as being of intermediate phenotype, indicated primarily by having bark that was not deeply furrowed or leaves that were somewhat bluish (as in Q. douglasii), but with leaves having the characteristic lobate shape of Q. lobata. This combination of characters is not common, and thus these trees were considered putative hybrids between the two species.
Both species appear to be regenerating poorly throughout much of California (Standiford, 2002
), and saplings were in general not present within the study area. Thus, all individuals sampled were mature adults with the exception of two saplings, identified morphologically as Q. lobata, growing naturally within an exclosure present within the study area.
Microsatellite data collection
Approximately 1 g of frozen leaf material was ground to a fine powder in liquid nitrogen for extraction following Kleim et al. (1989)
. DNA was further purified using the Qiagen Tissue DNA Extraction Kit to remove proteins and other secondary compounds that inhibit polymerase chain reaction (PCR) reactions. Two of the microsatellite primers we used (MSQ13 and MSQ4) were developed for Quercus macrocarpa by Dow, Ashley, and Howe (1995)
and Dow and Ashley (1996)
, and two (QpZAG9 and QpZAG110) were developed for Q. petrea by Steinkellner et al. (1997)
(Table 1). One primer of each pair was fluorescently labeled. Polymerase chain reaction amplification was performed in reactions containing 0.2–0.4 µg genomic DNA, 100 µmol/L dNTP's, 0.15–0.6 µmol/L of each primer, 1.0 µg/µL bovine serum albumin, 2.0–3.0 mmol/L MgCl2, PCR buffer, and 0.04 µL Taq polymerase (Promega). All PCR reactions consist of a 3-min preheat period at 95°C followed by 38 cycles of denaturing at 94°C for 30 s, annealing at 54°C for 30 s, and extension at 72°C for 45 s and a final extension at 72°C for 5 min. The PCR products were then run along with the fluorescent size standard Tamara 350 on an MJBaseStation automated sequencer (MJ Research, Waltham, Massachusetts, USA). Cartographer software (MJ Research) was used to size and score genotypes.
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). We used GENEPOP (Raymond and Rousset, 1995
) to implement the private allele method for estimating the number of migrants per generation (Slatkin, 1985
; Barton and Slatkin, 1986
), to test for homogeneity of allele distributions between species, and to test for deviations from Hardy-Weinberg equilibrium. GENEPOP calculates unbiased estimates of P values using a Markov chain method. Because null alleles had been observed in Q. macrocarpa for at least one of the loci used (Dow and Ashley, 1996
), we estimated the proportion of observed heterozygote deficiencies (D) and the frequencies of null alleles (r) according to Chakraborty et al. (1992)
using the expressions: D = HE – HO /HE and r = (HE – HO)/(HE + HO).
We also used GENEPOP to calculate an estimate of Wright's FST (
, Weir and Cockerham, 1984
). GENEPOP uses standardized allele sizes to determine variance components at each locus and calculates 
, an estimator of RST (Slatkin, 1995
). RST is an index of genetic differentiation estimated from the sum of squared number of repeat differences (Michalakis and Excoffier, 1996
; Rousset, 1996
). Although typically applied to population subdivision within species, these statistics were used here to assess genetic differentiation between the two species.
We also applied a Bayesian clustering approach to assign individual trees to species on the basis of their genotypes alone. This allowed us to determine how well the genetic structure in the entire data set corresponded to phenotypic assignment to species. This approach, implemented using the program structure (Pritchard, Stephens, and Donnelly, 2000
), uses a model-based clustering method for inferring population structure from multilocus genotype data and to simultaneously assign individuals to clusters. It also allows for the identification of hybrid individuals and estimates the fraction of their alleles that are derived from each species.
To verify that our data set showed genetic differentiation between the two species, we ran five independent runs of the Gibbs sampler in structure at population numbers (K) at K = 1 (no structure), K = 2 (two genetic clusters), and K = 3 (three genetic clusters), using a burn-in period of 30 000 iterations and collected data for 106 iterations. These initial runs were performed without using any information regarding species identification (USEPOPINFO = 0). Results at a given K were highly consistent across runs. Given X, the observed genotypes, ln Pr(X|K) = –2583 for K = 1, –2434 for K = 2, and –2463 for K = 3. The corresponding values for Pr (K|X) assuming a uniform prior on K = 1, 2, 3, yields a probability of about 0.0 for K = 1 and K = 3 and about 1.0 for K = 2. This confirms that the data set represents two clusters that are genetically strongly defined. To make sure our skewed sampling of species did not influence this result, we repeated the analyses with random subsets of 26 Q. lobata individuals, and each time two similar genetic clusters were identified. We thus continued our analyses to explore how well this structure corresponded to our assignment of individuals to species and to identify hybrid individuals, using prior information on species assignments (USEPOPINFO = 1). We ran the analysis at three values of the intergroup "immigration" rate v (in this context, "immigrant" means "hybrid"), as recommended by Pritchard, Stephens, and Donnelly (2000)
to see whether results were robust to choice of v. Values used were v = 0.10, 0.05, and 0.01, which we considered to span the range of reasonable frequencies of Q. lobata and Q. douglasii hybridization. The structure program then estimates the posterior probabilities that an individual is purely from the other population (in this case mis-assigned to species) or has a given amount of ancestry in the other species.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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12 alleles per locus and a mean expected heterozygosity of 0.833 across all loci (Table 1). Quercus lobata and Q. douglasii shared alleles at all loci but each harbored private alleles not found in the other species. Tests for homogeneity of allele distributions were highly significant (P < 0.0001) for all four loci. Aside from the general pattern of heterogeneity, the patterns varied extensively among loci. For QpZAG9 (Fig. 1), allele sizes ranged from 237 to 274 base pairs (bp) for Q. lobata and from 250 to 276 bp for Q. douglasii. The most common alleles for Q. lobata were 250 (19%) and 262 (31%). These two alleles were common in Q. douglasii but were not the most frequent. For QpZAG110 (Fig. 2), the most common allele in both species was 209, occurring at similar frequencies of 33%. There were other common alleles at this locus, however, that were unique to each species, including 207 in Q. lobata and 220 in Q. douglasii.
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Weir and Cockerham's (1984)
estimator of population subdivision, , was 0.049, 0.040, 0.035, and 0.298 for QpZAG9, QpZAG110, MSQ13, and MSQ4, respectively, significant over all loci ( = 0.106, P < 0.05). The estimator of RST, , was 0.004, 0.0135, 0.133, and 0.667 for QpZAG9, QpZAG110, MSQ13, and MSQ4, respectively, and was significant over all loci ( = 0.216, P < 0.05). Estimates of the number of migrants (Nm) based on = 2.11, 0.91 for , and 1.19 using the private allele method (Slatkin, 1985
; Barton and Slatkin, 1986
).
For the Bayesian analysis, we first used structure to cluster our data without using information regarding species assignment of individual trees. The two genetically distinct clusters found in the analysis correspond well to our assignment of individuals to Q. lobata and Q. douglasii. Of 109 Q. lobata genotyped, 98 (90%) had inferred ancestry in a "lobata" cluster with probability >0.90, and 22 of 26 Q. douglasii (85%) had >0.90 inferred ancestry in a "douglasii" cluster (Fig. 5). Of the five putative hybrid trees, two (1102H and 1050H) had >0.95 probability of ancestry in the "douglasii" cluster, whereas the other three, 1055H, 1123H, and 167H, had probabilities of ancestry in the "lobata" cluster of 0.954, 0.891, and 0.687, respectively.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Holstein, 1984
). Occasional individuals with intermediate morphologies, at Hastings and elsewhere, support the possibility of hybridization. At our study site, the species show similar flowering phenologies (W. D. Koenig, unpublished data) and patterns of annual acorn production that are both strongly correlated with each other (Koenig et al., 1994
) and with conditions during the spring flowering period (Koenig et al., 1996
). Our goal was to characterize microsatellite variability in these species and to use microsatellite data to gain accurate estimates of hybridization frequency.
We applied both standard genetic differentiation approaches as well as Bayesian clustering methods to characterize hybridization. Recently, the appropriateness of different measures of genetic differentiation for microsatellite loci (e.g., FST and RST) has come under scrutiny (Gaggiotti et al., 1999
; Hedrick, 1999
; Balloux and Lugon-Moulin, 2002
). In our case, both estimates of genetic differentiation were significant between Q. lobata and Q. douglasii, although values of both estimators ranged widely across loci. Over all loci, the estimate of RST was more than twice the value of FST, indicating that the two species do not just differ in distributions of allele frequencies, but also differ in allele sizes. Such shifts likely occur over longer divergence times than changes in frequencies (Slatkin, 1995
), suggesting historically low levels of introgression. The existence of many private alleles further indicates little gene flow between the two species (Slatkin, 1985
). Quercus douglasii had private alleles at all four loci, even though the number of individuals sampled was relatively small. Quercus lobata had private alleles at three loci, although some of these alleles may have been found at low frequency in Q. douglasii but not sampled.
Previous work on hybridization in plants has relied upon a priori assignment of individual trees to groups (for example, species "A," species "B," or "hybrid") based on phenotype. Hybridization in oaks is commonly inferred on the basis of morphologically intermediate trees. The classification by the researcher, however, may not reflect the underlying genetic structure of the population and may not present an accurate picture regarding introgression and hybridization. In our initial Bayesian analysis, we used a purely genetical analysis, using no external information, to infer population structure. The correspondence between genetic structure and phenotypic classification to species was extremely close, although the few exceptions (Table 2) are informative. The Bayesian clustering approach has the further advantage of assigning individuals to populations according to likelihoods based on allele frequencies and to identify individuals whose genetic makeup may be drawn from two populations (hybrids). This allowed us to rule out hybrid ancestry for nearly all sampled individuals. Four of five phenotypically intermediate trees (1050H, 1055H, 1102H, and 1123H, Table 2) had very low probabilities of hybrid ancestry. Three trees assigned to Q. lobata had modest probabilities of hybrid ancestry (1083L, 1117L, and 1156L, Table 2); one of these (1117L) was one of the two saplings sampled. Even the three trees that had the highest probability of hybrid ancestry (167H, 1100L, and 1122L, Table 2) had probabilities of pure Q. lobata ancestry that were twice as great. Our results suggests that the frequency of hybridization across all trees of these species is no higher than 4% (6/141), but could be much closer to zero.
Our results caution against the assumption that phenotypically intermediate trees are necessarily hybrids. Four phenotypically intermediate trees at our site showed little evidence of mixed ancestry; two were assigned to Q. lobata (1055H and 1123H, Table 2) and two to Q. douglasii (1050H and 1102H). Of the four trees with the highest probability of hybrid ancestry, only one was identified as intermediate in appearance. These findings suggest that apparently intermediate phenotypes between these two species are not necessarily hybrids and that true hybrids are not necessarily intermediate in phenotype.
The high level of differentiation between Q. lobata and Q. douglasii for microsatellite loci suggests that these markers may provide improved resolution for studying hybridization in oaks. Other molecular markers have often proven unsatisfactory. For example, chloroplast DNA may be commonly exchanged between species that are distantly related and show only limited ability to hybridize (Whittemore and Schaal, 1991
; Belahbib et al., 2001
). Other markers, such as allozymes, cannot distinguish among closely related oak species. Manos and Fairbrothers (1987)
found that five species of red oaks had a high degree of allozymic similarity, with a mean genetic identity of 0.958 between species, and concluded that isozymes "were of little value in identifying species since marker alleles were not found" (p. 365). Nason, Ellstrand, and Arnold (1992)
had better success using allozymes to study hybridization between two black oaks, Q. kelloggi and Q. wislizenii, and found these species differed in numbers and frequencies of alleles at allozyme loci. In contrast to our results, the putative hybrid trees in their study did correspond genetically to F1 hybrids, bearing alleles unique to alternative parental species at different loci. Howard et al. (1997)
were successful in finding 14 species-specific RAPD markers for the closely related white oaks Q. grisea and Q. gambelii, but this was only through screening 700 primers.
The best studied oak system thus far, and the only other system where microsatellite markers have been applied to the question of hybridization, is that of the European Q. robur-Q. petraea-Q. pubescens complex. These species are highly interfertile (Bacilieri et al., 1996
) and lack diagnostic chloroplast markers (Ferris et al., 1993
; Dumolin-Lapegue, Kremer, and Petit, 1999
), allozymes (Zanetto, Roussel, and Kremer, 1994
), and ITS sequences (Muir, Fleming, and Schlötterer, 2001
). Although the species show small but significant differences in allele frequencies at microsatellite loci (Muir, Fleming, and Schlötterer, 2000
), they are clearly not as well differentiated as Q. lobata and Q. douglasii. For example, assignment tests using data from 20 microsatellite loci could assign only 78% of individuals to species (Muir, Fleming, and Schlötterer, 2000
). In our study, data from only four microsatellite loci were sufficient to assign nearly all individuals to one species or another. Bruschi et al. (2000)
reports no significant differences for Q. petraea and Q. pubescens at two of three nuclear microsatellite loci and genetic differentiation (RST) between the species was only 0.048, compared to 0.216 for Q. lobata and Q. douglasii.
Hybridization and species boundaries among oak species remain complicated and compelling issues. Here we show that genetic introgression may be rare, even between closely related species occurring in a mixed stand. Because we primarily genotyped adult oaks, we do not know whether there are strong fertility barriers between Q. lobata and Q. douglasii or whether hybrid seedlings or saplings do not survive to adulthood. Indeed, the result that one of the two saplings we were able to sample was a potential hybrid raises the possibility that hybrids among acorns and saplings might be more common than among adults. Genotyping of Q. lobata acorns, planned as part of a pollination study, will allow us to determine if Q. douglasii pollen fertilizes Q. lobata acorns and whether the proportion of hybrid individuals declines between seed and adult stages.
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FOOTNOTES |
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4 Author for reprint requests (ashley{at}uic.edu
)
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LITERATURE CITED |
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