Natural Hybridization Within the Genus Quercus L Bs Rushton

Natural hybridization within the genus Quercus L Bs Rushton

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Bs Rushton. Natural hybridization within the genus Quercus L. Annales des sciences forestières, INRA/EDP Sciences, 1993, 50 (Suppl1), pp.73s-90s. hal-00882878

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Natural hybridization within the genus Quercus L

BS Rushton

Department of Biological and Biomedical Sciences, University of Ulster, Coleraine, Northern Ireland, BT52 1SA, UK

Summary — Hybridization within the genus Quercus L appears to be extensive and reports vary from sightings of individual hybrid trees to small numbers of individual hybrid trees within populations to populations with characteristics of small-scale (eg Q robur and Q petraea in Hurepoix, France) and large-scale introgression (eg Q robur and Q petraea in Scotland) and, in some cases, the occurrence of hybrid swarms (eg Q douglasii and Q turbinelia subsp californica in California). This has persuaded some authorities to question the current formal species concept in the genus and to suggest alternatives. The evidence supporting these cases of hybridization is examined in detail. The majority of the reports of hybrids between species of Quercus are based on an analysis of morphological data alone using a variety of univariate, bivariate and, more effectively, multivariate statistics, while other forms of evidence, such as estimates of fertility in the putative hybrids, resynthesis of hybrids, habitat characteristics of the putative hybrids and F2 segregation of parental types, have only been used occa- sionally. Data from chemotaxonomic investigations of suspected Quercus hybrids (mainly isozymes and phenolic components) in some instances support the morphological evidence but in other instances are contradictory; chemical data are also shown to be variable and possibly related to environmental variation which will limit their usefulness. It is concluded that, before any radical revision of the genus is attempted in which the specific limits are redefined, a wider application of the possible techniques for the study of hybrids be applied in or- der to clarify the true extent of gene flow between Quercus species. natural hybridization / introgression / chemotaxonomy / morphology / Quercus L

Résumé — Hybridation à l’intérieur du genre Quercus L. L’hybridation à l’intérieur du genre Quercus L est très largement répandue. Les descriptions d’hybrides concernent soit des arbres iso- lés, soit un nombre limité d’arbres situés en peuplement (Q robur et Q petraea à Hurepoix, France), soit des zones d’introgression (Q robur et Q petraea en Écosse), soit de larges populations gré- gaires d’hybrides (Q douglasii et Q turbinella subsp californica en Californie). La notion même d’es- pèce à l’intérieur du genre a été mise en doute par les spécialistes, qui ont suggéré d’autres interpré- tations. Les différents cas d’hybridation sont examinés en détail dans cette contribution. La majorité d’entre eux se réfère à des données morphologiques interprétées sous forme univariée, bivariée ou multivariée. Par contre d’autres méthodes de mise en évidence telles que les estimations de fertilité des hybrides, les hybridations contrôlées, les ségrégations des types parentaux en F2, et la description de l’habitat des hybrides putatifs, ont été plus rarement utilisées. Les données chimiotaxonomi- ques relatives aux hybrides suspectés (essentiellement isozymes et composés phénoliques) corro- borent les observations morphologiques dans certains cas, mais les infirment dans d’autres cas. Les caractères biochimiques manifestent également des variations liées au milieu, qui limitent leur utilisa- tion. En conclusion, il est recommandé d’utiliser l’ensemble des techniques disponibles pour l’étude de l’hybridation et des flux géniques avant de remettre en cause de manière radicale le genre Quercus. hybridation naturelle / introgression / chimiotaxonomie / morphologie / Quercus L

INTRODUCTION THE DETECTION OF HYBRIDIZATION

It is estimated that Quercus L, one of the Hybridization manifests itself in a number largest genera of flowering plants, includes of ways, but the initial recognition of hy- about 450 species (Jones, 1974), although brids is by morphological intermediacy, the the literature contains considerably more putative hybrids showing evidence of inter- names and descriptions than this and vari- mediate character states or a combination able estimates for the total number of spe- of suspected parental character states cies. Recorded hybrids between these (Phipps, 1984). Indeed, as Gottlieb (1972) would appear to be both common and points out, in the absence of morphological widespread. The earliest record of a hybrid intermediacy, hybridity would not be sus- oak in America was the description of x pected. When the parental species are suf- Q hispanica by Michaux in 1812 (Palmer, ficiently distinct, morphology alone may be 1948). In Europe, there are many similar sufficient to establish a case for hybridity, early records (see Gardiner, 1974). The but where, as is often the case in Quercus, apparent abundance of hybrids in certain the parental species show a wide range of areas has caused taxonomic confusion natural variation and/or possesses few di- (and "complete frustration"; Tucker, 1961) agnostic characters, other criteria have to in the past and, in certain floras, has un- be used. These include (Gottlieb, 1972): 1) doubtedly led to misidentification. an additive biochemical profile for characters, such as flavonoids or proteins, which Population studies have indicated that are present in one or other parent but not the pattern of hybridization may follow 2 in both; 2) unusual amounts of interpopula- distinct the population shows evi- paths: 1) tional morphological variation (resulting dence of swarm formation, where hybrid from segregation of parental differences); the majority of the population appears the occurrence of the hybrid in intermediate between the 2 3) putative completely intermediate habitats and evidence that or the suspected parental species; 2) pop- the putative hybrid has intermediacy for ulation shows evidence of introgression physiological characters; 4) the occurrence (Anderson, 1953), where the population of the putative hybrid in areas where the 2 consists of one species and a series of F1 suspected parents are sympatric; 5) the and backcrossed (1974) hybrids. Wigston occurrence of the putative hybrid in geo- has reviewed the essential characteristics logical strata more recent than either of the of and how to introgression they apply 2 suspected parents; 6) the existence of at Quercus. least partial fertility in F1 hybrids between This paper reviews the evidence which the parents to permit the possible produc- has been utilized in the detection of hy- tion of segregant genotypes; and 7) experi- brids and provides an evaluation, so far as mental production of individuals that re- current knowledge allows, of the different semble the putative hybrid in segregants of types of evidence. hybrids between the parents. These criteria are broadly the same as species could be more easily discriminated those proposed by Stace (1980) and Craw- in one season than in another; the general- ford (1985) and build on those already es- ity of this result needs to be confirmed (see tablished in the earlier part of this century also Blue and Jensen, 1988). (see Stace, 1975). To this list may be add- In the early population studies, the stan- the of reduced shown ed possibility fertility dard approach was to construct hybrid indi- some and DNA by hybrids polymorphism. ces based on a limited range of morpho- Within Quercus, few examples exist in logical characters and display these data which a thorough investigation using all the in the form of bivariate scatter diagrams in above criteria has been completed. which the 2 axes of variation represented quantitative characters and each point on the scatter was usually a tree (Cousens, PATTERNS 1963, 1965). The points were annotated to OF MORPHOLOGICAL VARIATION show the variation in characters expressed in hybrid-index form to produce, for each a which encapsulated intermediacy is the major, point, metroglyph Morphological the variation and Par- and often only, criterion used in assessing pattern (eg Brophy nell, While this approach has much the status of putative oak hybrids. Charac- 1974). to commend it, since the full of the ters are restricted to leaf and fruit- pattern usually variation is the inter- structures, others buds: expressed together, ing though (eg, be because of Jensen, 1988; bark: Dupouey, 1983) have pretation may problematic the difficulties in been utilized. The comparative uniformity choosing appropriate characters for the axes (Rush- of floral structures within the genus (and quantitative possibly their ephemeral nature) has limit- ton, 1978). ed their use in population studies. Restric- Subsequently, with the advent of numer- tion of samples to only fruiting specimens ical taxonomic methods, multivariate meth- inevitably underestimates levels of hybridi- odologies were utilized and a wide range ty. In addition, differences in fruit produc- of these have now found application in tion from year to year similarly bias sam- analysis of morphological data from oak pling, if samples are restricted to only populations, including principal compo- fruiting individuals. nents analysis (Rushton, 1978, 1983; Du- and Le 1989, Leaf morphology has been the most im- pouey Bouler, 1989; Jensen, discriminant function portant discriminator for oak taxa, both at etc), analysis (Ledig the level of the subgenus and the species et al, 1969; Rushton, 1974; Wigston, 1975; and cluster (Muller, 1942), but clearly leaf morphology Jensen et al, 1984) analysis These is subject to environmental modification. In (Rushton, 1978; Jensen, 1988). a much more ob- the field, standardized collecting points methods have enabled to in mor- (Cousens, 1963) have been used to over- jective approach pattern-seeking data and come these effects. However, in a study of phological sophisticated shape- methods are now evaluat- the influence of crown position on leaf describing being characters of Q palustris and Q velutina, ed (Jensen, 1990; Jensen et al, 1991) as a Ludlam and Jensen (1989) concluded that means of collecting objective morphologi- "leaves should be collected from several cal data from oak leaves. positions on each tree and these collec- One major disadvantage of these ap- tions pooled for evaluating among-tree proaches (and earlier methods) is that of variation". One further result was that the 2 fixing known reference points to aid in interpretation but this has been overcome by generalize about whether morphological the use of reference populations .(com- data overestimate or underestimate levels posed of natural populations showing no of hybridity. signs of hybridity or artificial populations of herbarium specimens) which are used in all analyses (see fig 1; and Rushton, POLLEN VIABILITY 1978). In some oak taxa, different groups of re- Stace (1975) provides cautionary advice searchers have come to dif- substantially concerning the use of fertility of putative ferent conclusions the levels of regarding hybrids as an indicator of hybrid status, data. This is hybridity using morphological since it has been shown that hybrids may true of the 2 particularly wide-ranging, be completely sterile, or show no signifi- common Q robur and European species, cant reduction in fertility compared with the Q petraea and Gar- (see below) prompted parents, or be intermediate. However, diner (1970) to describe the discrepancies many hybrids have been shown to pos- as a "hybrid controversy". However, rarely sess reduced pollen viability and correla- are the data sets comparable with directly tion between morphological characteristics variation in sample sizes, numbers and and pollen viability is supportive evidence types of characters, methods of scoring for hybridity, eg Cercidium and Parkinsonia and use of reference material, analysis, 1974; Carter and Rem, De- etc. It must also be borne in mind that (Carter, 1974). spite the extensive investigations of mor- within the genus are ex- many species variation in Quercus de- tremely variable in morphological charac- phological spp, tailed studies of pollen viability are scant teristics and are also likely to show varia- and restricted to a very narrow range of tion in to cross, thus leading to ability in those studies in differential hybridization levels in different species. However, which extensive estimates have been areas. made, the general conclusion is that re- Consideration of the use of morphologi- duced pollen viability can frequently be ob- cal data to detect oak would indi- hybrids served in putative Quercus hybrids (see cate: that more attention 1) considerably also the discussion in Tucker, 1963; be to within-tree variation and possi- paid p 706-707). Of course, if substantive pol- bly between-season variation: and 2) that len sterility is a feature of Quercus hybrids, attempts should be made to standardize then this may limit gene flow between spe- methods of scoring and data analysis. Un- cies and promote the maintenance of spe- replicate samples from the doubtedly, cies identity. same trees, combined with population samples and analyzed using multivariate Surveys of Q robur and Q petraea in methodologies would enable levels of phe- England and Wales (see fig 2; and Rush- notypic plasticity to be assessed alongside ton, 1978) and in Northern Ireland (Rush- population variation, though the number of ton, 1988) have shown that morphological instances in which such intensive sam- intermediacy is accompanied by a tenden- pling has been coupled with extensive cy for reduced pollen viability and Olsson sampling is very small. Where morphologi- (1975a) has provided similar results for the cal data have been collected alongside same species. However, close examina- other data (see below), the correspon- tion of assumed F1 hybrids indicated that dence between the different types of evi- they had an "unexpectedly high percent- dence may be poor, and it is difficult to age of pollen stainability" (Olsson, 1975a),

similar to that recorded in some intermedi- also variation between individual trees, ate trees observed by Rushton (1978) and though detailed data on the extent of this Minihan and Rushton (1984), and this was were not provided. Guttman and Weigt tentatively ascribed to cryptic structural hy- (1989) examined leaf material from 10 spe- bridity. cies of subgenus Erythrobalanus and 8 species of subgenus Quercus and were able to resolve 18 loci which represented CHEMOTAXONOMIC STUDIES 12 different enzyme systems. Subgeneric differences were re-enforced by the allo- zymes and species relationships com- Electrophoretic evidence pared well with other data, though there were differences. For example, Q nigra and Q laurifolia were found to be closely Crawford has out that allo- (1985) pointed related using morphological data analyzed offer several over other zymes advantages by cladistic and phenetic means (Jensen, types of evidence when assessing hybrid 1983), but isozymic results (Guttman and since it is to examine the origin, possible Weigt, 1989) suggested they were more of a number of without the products genes distantly related and in different groups of character or addi- problem intermediacy within the subgenus. One interesting con- which is sometimes the case with tivity clusion of Guttman and Weigt (1989) was morphological characteristics; that is, the that the rather small genetic distances esti- allelic products of specific genes in the pu- mated between the oak taxa (especially tative are either the same or differ- hybrid within subgenus Eryfhrobalanus) may re- ent from those of the suspected parental flect the extensive interspecific hybridiza- species. Despite this considerable advan- tion and introgression that has taken place examination of tage, Quercus spp by within the genus. Manos and Fairbrothers chemotaxonomic methods is restricted to a (1987) studied 6 species of the subgenus small number of reports and often these Erythrobalanus, and obtained similar re- are not specifically concerned with the oc- sults and thus concluded that, within the currence or incidence of hybridization but subgenus, evolution may have taken place with variation between species (eg, Bella- by morphological divergence accompanied rosa et al, 1990) or genetic diversity within by little electrophoretically detectable ge- species (eg Yacine and Lumaret, 1988, netic differentiation. 1989). Several reports are mentioned here A similar conclusion was reached by to focus attention on their or be- potential Chechowitz et al (1990) who showed that cause their results relate to hybridization oak populations in South Dakota and Wyo- within the genus generally. ming could not be distinguished electro- Perhaps the most wide-ranging enzyme phoretically from Q macrocarpa, whilst study was that of Santamour (1983) who morphologically they showed extensive in- surveyed cambial peroxidase isoenzymes trogression between Q macrocarpa and Q in over 90 taxa. Major bands enabled sub- gambelii. They argued that such disparity generic differences to be highlighted, but reflected natural selection operating differ- there was variability within the subgenera ently on morphological and electrophoretic Quercus, Cyclobalanus and Erythrobala- characters. Some species (eg Q rubra; nus so that individual species could not be Houston, 1983) have been shown to pos- assigned to these subgenera on the basis sess extensive isoenzyme variation, which of isoenzyme patterns alone. There was would also preclude the use of isoenzymes in studies of their hybrids, whilst other mor- brids in the survey yielded somewhat dif- phologically very similar species can be re- ferent results. Q x bebbiana, thought to be solved electrophoretically (eg Q ilex, Q ro- a hybrid between Q alba and Q macrocar- tundifolia; Afzal-Rafii, 1988). Isozyme pa, was shown to possess a largely addi- variation has also been used to show con- tive phenolic profile. The parentage of Q siderable gene flow between island popu- comptonae was thought to be Q lyrata x Q lations of red oaks (Hokanson et al, 1991). virginiana, but chromatographically it was Discrepancy between morphological generally very similar to that of Q virginia- and chemical characters has been inter- na and lacked the most prominent spot of preted very differently by Cristofolini Q lyrata. (1985), who assessed seed and leaf pro- One of the most elegant studies of oak teins of a number of species. Whilst each hybridization using leaf phenols was that of species gave characteristic protein pat- Knops and Jensen (1980) involving 3 spe- terns, morphologically intermediate plants cies, Q ilicifolia, Q marilandica and Q velu- nearly always produced protein patterns tina; morphological data indicated that hy- corresponding to one or other of the sus- bridization was restricted to Q ilicifolia x Q pected parental species. The conclusion marilandica and Q marilandica x Q veluti- drawn was that morphological variation na. The 3 species had distinctive phenol may be due to phenotypic plasticity rather patterns which allowed detection and con- than to hybridization. An earlier investiga- firmation of the putative hybrid parentages tion of some of the same species (Olsson, and confirmed the lack of hybrids between 1975b) indicated that leaf peroxidase iso- Q ilicifolia and Q velutina. Cottam et al zymes showed high interspecific variation (1982) also used anthocyanidins and cate- in Q robur and Q petraea and that intro- chins to confirm the status of artificially gressed populations had more affinities raised hybrids. with Q petraea. Like isozymes, phenol can, however, be Because of the conflicting results al- variable within species and this variation ready shown by isoenzyme studies, it is may be related to the environment. unlikely that isoenzyme investigations will McDougal and Parks (1984) showed that generally provide accurate estimates of foliar phenols of Q rubra varied with eleva- the levels of natural hybridization, though tion (fig 3) and it was subsequently shown they may be useful in establishing individu- (McDougal and Parks, 1986) that the dif- al cases of hybridization. ferences in phenols between different ele- vations was largely under genetic control. As argued above for isoenzyme studies, Variation in phenolic compounds it is also unlikely that the use of phenolic compounds will prove particularly useful in An extensive study of phenols of American estimating levels of natural hybridization in oaks by Li and Hsaio 1973) provided (eg oak populations. the basis for our knowledge of phenolic variation in Quercus. Leaf phenols of 49 were studied and, the species generally, DNA phenolic pattern allowed differentiation of the subgenera Quercus, Protobalanus and Erythrobalanus, though the authors indi- Organellar DNAs show a high degree of cated that no one chromatographic spot potential for assessing levels of hybridity in was diagnostic for any subgenus. Two hy- natural populations (Whittemore and

Schaal, 1991), though their use in Quer- Tucker (1961) showed that Q turbinella cus has so far been very limited. Whitte- and Q gambelii are ecologically separated, more and Schaal (1991) used variation of the former living in semi-arid areas com- chloroplast DNA and nuclear ribosomal pared to the more mesic habitats at higher DNA extracted from winter buds and altitude of the latter, but where they are expanding leaves of 5 species of Ameri- sympatric, in certain forest types, they hy- can white oak which differed in many bridize. Neilson and Wullstein (1985) re- morphological characters but which had ported that the differential drought re- different but overlapping geographical sponse of the 2 species is primarily due to ranges and ecological tolerances. Using anatomical/morphological leaf differences obviously non-hybrid individuals (as- but, unfortunately, no hybrids were stud- sessed on morphological data), they were ied. Rushton (1979) demonstrated that able to conclude that there were "... sev- populations, which were composed largely eral clear cases of localized gene ex- of hybrids between Q robur and Q petraea change between species, showing that and which may have been hybrid swarms, there is appreciable gene flow between were found along coastal river valleys in sympatric species in this group." The rec- Wales where they occupied intermediate ognition that gene flow occurs in this habitats between the better drained, sili- group without apparent morphological in- ceous, nutrient-poor hill-tops and the wet- termediacy suggests that hybridization ter, more poorly drained nutrient-richer val- may be more common than other data ley floors. types indicate, and there is little doubt Disturbance may also be a factor in pro- that further investigations along these moting hybridization. For example, Silliman lines will assist in assessing levels of and Leisner (1958) showed that a mixed gene flow in Quercus. population of Q alba and Q montana on a stable, undisturbed site had no hybrids, whilst hybrids were common on a site sub- HYBRIDITY RELATED ject to successive disturbance by fire and TO THE HABITAT forestry. In an F2 generation, segregation and re- The importance of the habitat in controlling combination would suggest that the individ- natural hybridization has been examined uals should be more heterogeneous in by Anderson (1948). He argued that the F1 their habitat requirements compared to ei- hybrid should be uniform in its habitat re- ther the F1 generation or the original pa- quirements and that these are likely to be rental species. Conversely, backcrossed intermediate between those of the 2 pa- F2 trees might be expected to show habitat rental species (the ’hybrid habitat’). For ex- preferences similar to those of the back- ample, edaphic restriction of hybridization crossed parental species (Grant, 1971; is seen in Q harvardii, which is restricted Rushton, 1979). Benson et al (1967) have to deep, coarse sands, and Q mohriana, provided a clear example of such ecologi- which occurs on exposed limestone. cal segregation, though the method of data Where erosion creates a mixture of sand collection may be suspect. Hybrid popula- and limestone fragments, hybrids are com- tions between Q douglassii and Q turbinel- mon (Muller, 1952). In other species, it la subsp californica were examined and may be climate which restricts hybridiza- the composition of each population related tion, as is the case of Q harvardii and Q to the degree of site exposure; on south- stellata (Muller, 1952). west facing slopes, the populations were more like Q turbinella subsp californica, successful intersubgeneric crosses. Jova- while Q douglasii-like populations were novic et al (1973) also reported some suc- more prominent on north-east facing cess in attempted hybridization between Q slopes. Thus selection among the F2 gen- robur, Q alba, Q pubescens and Q pedun- eration for different recombinant types had culiflora. Whilst most interspecific crosses occurred as a result of exposure differen- gave very low success rates (usually less ces. Evolutionary sorting in this instance than ≈ 1.5%) compared with intraspecific must be very rapid (Benson et al, 1967). crosses, the Q pedunculiflora x Q robur Consequently, the successful outcome cross was highly successful (30.7%). How- Cottam et al have viewed of a hybridization event in Quercus de- ever, (1982) much of the work done in eastern pends crucially upon the habitat condi- Europe tions, and the level of hybridity reported as dubious: "Most American tree geneticists have tended to be about the under field conditions may be a reflection sceptical in more of the habitat restriction on establish- work done eastern Europe." Wright ment than other factors. (1976) stated that "... the authenticity of some is in doubt because the ’hybrids’ re- sembled the female parent only". This criti- cism is mild to some ARTIFICIAL HYBRIDIZATION compared opinions and comments made (not for publication) at geneticists’ gatherings. There have been 2 major research pro- The work of Cottam et al (1982) is well grammes aimed at producing artificial hy- documented and, in cases of doubt regard- brids, one led by Piatnitsky, started in 1937 ing the suspected hybrid, supplementary in Russia, and the other reported by Cot- data of F2 segregation, phenolic com- tam et al (1982). The work of Piatnitsky pounds and epidermal characters (as seen was summarized in Piatnitsky (1960). In under the scanning electron microscope) all, over 200 000 pollinations were made were all utilized. The only data not provid- representing 47 different interspecific ed are the absolute success rates for each crosses, and 24 of these from 9 species cross made - the number of acorns and were considered successful (it should be subsequent seedlings are reported from noted, however, that Q fastigiata was con- the number of pollination ’sacks’ but no in- sidered a separate species rather than a dication is given of the number of female variety of Q robur). Many of the successful flowers in each sack. Nevertheless, the crosses were between species in the sub- programme was successful (table I) and genus Quercus but there were a number of resulted in 43 hybrid combinations. Inter- estingly, data given by Cottam et al (1982) sembling the parental species. Two differ- for another programme (Schreiner, 1962) ent approaches have been used: 1) F2 show an almost complete absence of suc- segregation to determine the parental spe- cess (table I), resulting, according to Cot- cies of natural hybrids (eg Allard, 1949; tam et al (1982), from a different pollina- Tucker and Bogert, 1973); and 2) the ex- tion method that may have "overpollinated" amination of the inheritance patterns in ar- the stigmas. tificial hybrids (see fig 4; and Yarnell, In addition to these 2 major research 1933). Where F2 generations were raised programmes, there are numerous reports by Cottam et al (1982), there was a clear of more limited crossing experiments (eg, segregation of parental characters and, po- Dengler, 1941; Gegel’skii, 1975; Rushton, tentially, this would appear to be a most 1977). One general point to emerge from useful tool in establishing parentage (see some of these studies is that certain spe- also Burk, 1965). cies show a degree of self-incompatibility. Artificial resynthesis has therefore been achieved in a number of cases. However, LEVELS OF HYBRIDIZATION the lack of success in some instances IN NATURAL POPULATIONS where extensive natural hybridization has been reported (eg Q robur and Q petraea) remains for further investigation. It should It is not possible to generalize on the levels be recalled that the inability to resynthe- of hybridization in natural populations; in- size hybrids artificially does not in itself instances are recorded of individual hybrid in- validate the case for natural hybridization trees (Tucker and Boger, 1973), barely events. One other line of investigation trogressed (eg Dupouey, 1983) to highly would be to examine the frequency of oc- introgressed populations (eg Cousens, currence of hybrids in natural populations 1963) and hybrid swarms (Benson et al, of those species shown to have a high po- 1967). What is apparent is that, in some tential for successful artificial hybrid pro- species pairs that have been investigated duction. over a wide geographical range, the levels of hybridity vary considerably (see table II) though some of the differences could be KARYOTYPE ANALYSIS due to different methodologies of investigation. Karyotype analysis has yielded little infor- Cousens (1965) believed that there was mation that can be of value in hybridization an increasing cline of introgression be- studies; the chromosomes are very small tween Q robur and Q petraea northwards and, although differences between species in England and Scotland. Rushton (1979) have been shown (eg Rushton, 1974; has shown a similar cline of increasing in- Wang, 1986), the karyotype is very uni- trogression from east to west in England form in those species examined. and Wales. The presence of suitable habitats for hybrid and backcross establish- ment may be a factor here, and planting of F2 SEGREGATION important amenity and forestry species like these may have accelerated hybridization Theoretically, the F2 should show a range in some areas. In Scotland, the shorter of types including the recovery of forms re- growing season may also allow a greater overlap of flowering period which would CONCLUSION enhance hybrid formation. It should be clearly emphasized, howev- The extensive occurrence of hybrids with- er, that the view of widespread hybridiza- in the genus is now well documented; tion in Quercus is not shared by all re- Hardin (1975) has observed that gene ex- searchers (eg, Jones, 1959), who have change "occurs or at least has the poten- indicated that oaks are very plastic and tial for taking place among nearly all spe- that the great range of variation in (largely) cies of subgenus Quercus in eastern foliage characters with tree age, crown po- North America (albeit to a very limited ex- sition, growing conditions etc, results in tent in most cases), and the species can misinterpretations of patterns of variation. be thought of as comprising the most in- To some extent this view is supported by clusive breeding group or syngameon." the low percentage of success rates in This has led some authorities, such as many artificial hybridization studies com- Burger (1975), to question the traditional pared to intraspecific crosses (eg Rushton, species concept within Quercus and for 1977; Ostrolucka, personal communica- some to suggest alternatives, such as the tion); whilst it has been possible to pro- multispecies (Van Valen, 1976), a con- duce numerous artificial hybrids, the actual cept very like that of the syngameon percentage of success rates is usually ex- (Grant, 1971). It must be recalled, howev- tremely low. er, that a large proportion of recorded hybrids have been determined on morpho- Bellarosa R, Delre V, Schirone B, Maggini F RNA in Quercus logical grounds alone and that the per- (1990) Ribosomal genes spp (Fagaceae). Plant Syst Evol 172, 127-139 centage of success rates for artificially raised hybrids is usually quite low. Re- Benson L, Phillips EA, Wilder PA, et al (1967) evaluation of the systematic organization Evolutionary sorting of characters in a hybrid swarm I. Direction of Am J Bot 54, of the in terms of relation- slope. genus species 1017-1026 ships must await the more extensive application of alternative lines of evidence. Blue MP, Jensen RJ (1988) Positional and sea- sonal variation in oak As Whittemore and Schaal state: (Quercus; Fagaceae) (1991) leaf morphology. Am J Bot 75, 939-947 "Sympatric oak species are able to remain distinct despite considerable introgres- Brophy WB, Parnell DR (1974) Hybridization between Quercus agrifolia and Q wislizenii sion, so that that on species concepts rely (Fagaceae). Madroño 22, 290-302 total genetic isolation between species to WC The in Quer- explain their distinctness clearly are not Burger (1975) species concept cus. Taxon 24, 45-50 applicable in Quercus." It will only be by the application of a wide range of different Burk CJ (1965) Segregation in three generations of of the oak Quercus x techniques that the levels of gene flow be- progeny hybrid rudkini marilandica x Q phellos). J Elisha tween Quercus and the limits of (Q species Mitchell Sci Soc 81, 50-53 individual species will be accurately assessed. Carter AM (1974) Evidence for the hybrid origin of Cercidium sonorae (Leguminosae: Caesal- piniodeae) of northwestern Mexico. Madroño 22, 266-272 ACKNOWLEDGMENTS Carter AM, Rem NC (1974) Pollen studies in relation to hybridization in Cercidium and Parkinsonia Caesalpinioi- The author wishes to thank MC Lewis for first in- (Leguminosae: deae) of northwestern Mexico. Madroño 22, him to Quercus over 20 troducing hybrids years 303-311 ago and the staff of the Drawing and Photo- graphic Office, University of Ulster, for their help Chechowitz N, Chappell DM, Guttman SI, Weigt in preparing diagrams for this paper. LA (1990) Morphological, electrophoretic, and ecological analysis of Quercus macrocarpa populations in the Black Hills of South Dakota and Wyoming. Can J Bot 68, 2185-2194 REFERENCES Cottam WP, Tucker JM, Santamour FS (1982) Oak Hybridization at the University of Utah. State Arboretum of Utah Publ no Salt Afzal-Rafii Z (1988) Caractéristiques taxono- 1, Lake UT mique, morphologique et isoenzymatique du City, complexe "Chêne vert". 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