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1 School of Environmental and Evolutionary Biology, University of St Andrews, St Andrews, Fife KY16 9TH, UK; and 2 Royal Botanic Garden, Inverleith Row, Edinburgh EH20 3LR, UK
Received for publication December 3, 1998. Accepted for publication March 25, 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: diploid hybrid speciation • ecological isolation • hybridization • introgression • Rhododendron • RFLP
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Abbott, 1992
; Arnold, 1992, 1997
; Rieseberg and Wendel, 1993
; Rieseberg, 1997
; Rieseberg and Carney, 1998
), spontaneous hybrid formation is not evenly distributed among plant taxa. Ellstrand, Whitkus, and Rieseberg (1996)
have shown that the frequency of hybridization varies strongly among families, and whereas some plant genera contain large numbers of hybrids, the majority contain none. Genera prone to hybridization may sometimes contain many species occurring in sympatry without breakdown of species barriers (e.g., certain Quercus spp.—Whittemore and Schaal, 1991
; Nason, Ellstrand, and Arnold, 1992
; Penstemon—Wolfe and Elisens, 1994
; Wolfe, Xiang, and Kephart, 1998
). In such cases, the potential exists for the production of fertile hybrids, yet hybrid swarms rarely or never occur naturally, presumably because ecological factors limit hybrid formation or establishment. Possible mechanisms that limit hybridization in such genera may be those through which reproductive isolation evolved between some species pairs, and thus contributed to speciation and diversification within the genus as a whole. In this context, information regarding the frequency and nature of hybridization within a large genus is fundamental to understanding its history and how large numbers of potentially interfertile species might arise and be maintained.
With respect to woody plants, molecular markers have been used to investigate hybridization in wind-pollinated genera, notably Quercus (e.g., Whittemore and Schaal, 1991
; Nason, Ellstrand, and Arnold, 1992
; Jensen et al., 1993
; Howard et al., 1997
), and Populus (e.g., Paige and Capman, 1993
; Rajora and Dancik, 1995
), but less frequently among insect-pollinated woody species. That said, it has been shown that germplasm of one species may invade the range of another through long-distance pollen transfer in insect-pollinated Aesculus (dePamphilis and Wyatt, 1990
) and Eucalyptus (Potts and Reid, 1988
). Also, hybrids are frequent in island endemic groups such as the Hawaiian silversword alliance (Carr and Kyhos, 1986
) and the Macaronesian genus Argyranthemum (Brochmann, 1987
, and references therein). However, there is not as yet a large and widely distributed insect-pollinated woody genus in which the role of hybridization has been investigated in more than a few species.
Rhododendron (Ericaceae) is an example of a large woody genus in which hybridization may have played an important role in evolution and speciation. The very large number of horticultural hybrids in existence (over 1000; Bean, 1976
) testifies to the weakness of genetic barriers towards hybridization in this genus, yet natural hybridization of rhododendrons has been little studied (Kron, Gawen, and Chase, 1993
). Rhododendron subgenus Hymenanthes contains 225 species, which often occur in close sympatry; for example, 67 species occur in a small area of ~100 x 150 km in the eastern Himalayas (Chamberlain, 1982
). Only 14 natural hybrids have been identified within subgenus Hymenanthes (Chamberlain, 1982
), however the true extent of hybridization is almost certainly much greater in parts of the Himalayas where species boundaries appear incomplete. Actively speciating species complexes occur within this area (Argent et al., 1998
) and in many cases clear morphological boundaries among species have not been determined. Partly because the taxonomy is so complex, it is not known to what extent hybridization has contributed to species diversity or intergradation of species in this region.
Smaller clusters of sympatric Rhododendron species occur elsewhere, which provide an opportunity to investigate the extent of natural hybridization within the genus. For example, in northeast Turkey and the adjacent Caucasus four species of subsection Pontica, subgenus Hymenanthes occur in sympatry, and although one hybrid (R. ponticum x R. caucasicum) occurs wherever the parents are sympatric, and two others are suspected (Chamberlain, 1982
), these hybrids have not been well studied. An examination of the extent of hybridization among these four species would provide an indication of how frequently hybridization occurs among sympatric Rhododendron species throughout the range of the genus and would be a step towards understanding how species integrity is maintained.
The four species of Rhododendron subsection Pontica in northeast Turkey have different ecological preferences and altitude ranges. Rhododendron ponticum L. occurs from sea level to 1800 m (rarely to 2100 m) in forests (normally of Fagus orientalis; Stevens, 1978
) or Rhododendron thickets (Chamberlain, 1982
); R. ungernii Trautvetter occurs in forests from 1200 to 1850 m (Chamberlain, 1982
), and appears to show the strongest requirement for shade (R. Milne, personal observations); R. smirnovii Trautvetter occurs in forests or scrub from 1500 to 2300 m, occasionally descending to 500 m (Chamberlain, 1982
) with a preference for growing on rocky outcrops (R. Milne, personal observations). These three species may occur together between 1200 and 1500 m, as at Tiryal Daga, near Murgul, northeast Turkey (R. Milne, personal observations). The fourth species, R. caucasicum, is found between 2000 and 3000 m in the open alpine zone of this area (Stevens, 1978
), thus overlapping the range of R. smirnovii and to a much lesser extent R. ponticum; it also occasionally descends to altitudes as low as 1700 m, such as where late-lying snow patches indicate locally cold conditions (R. Milne, personal observations). Although hybrids are known to form between certain species pairs of this group, the four species are easily distinguished by four morphological characteristics, i.e., flower color, lower leaf surface indumentum, calyx lobe length, and ovary indumentum (see Table 2).
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; Chamberlain, 1982
; Güner and Duman, 1998
). This hybrid forms large colonies, and sometimes monocultures, between 1900 and 2100 m. Curiously, hybrid individuals are consistently intermediate between the parents in morphology (Stevens, 1978
; Güner and Duman, 1998
; R. Milne, personal observations), indicating that backcrosses probably are rare. The apparent absence of backcrosses has contributed to some uncertainty about whether R. x sochadzeae is indeed R. ponticum x R. caucasicum (Stevens, 1978
). However, according to a cpDNA phylogeny of Rhododendron subsect. Pontica (Milne, 1997
), R. ponticum and R. caucasicum are not sister species, and therefore R. x sochadzeae cannot be the progenitor of both species and, if a hybrid, must be the result of secondary contact.
Specimens of a putative hybrid between R. smirnovii and R. caucasicum have occasionally been observed, but their identity has not been confirmed (Chamberlain, 1982
). Hybridization between R. smirnovii and R. ungernii also appears to occur (Stevens, 1978
; Chamberlain, 1982
), and introgression resulting from this is a possible cause of a polymorphism for flower color within R. ungernii, with individuals producing either white or pale-pink flowers, but again there is no confirmation of this. No hybrids have been recorded between R. ponticum and R. smirnovii, or between R. ungernii and either R. ponticum or R. caucasicum.
Kron, Gawen, and Chase (1993)
demonstrated using morphological and cpDNA restriction fragment length polymorphism (RFLP) markers that hybridization and introgression had occurred between two species of Rhododendron (sect. Pentanthera) from Georgia, USA. Nuclear and cpDNA RFLP markers have been used by others to investigate possible instances of hybridization and/or introgression, for example among species of Senecio (Harris and Ingram, 1992
; Comes and Abbott, 1999
), Orchis (Caputo et al., 1997
), Stebbinocarpus (Wallace and Jansen, 1995
), and Helianthus (Rieseberg, Soltis, and Palmer, 1988
; Rieseberg, Carter, and Zona, 1990
). Chloroplast DNA markers are cytoplasmic and are thus not altered by recombination during backcrossing, and in many cases have provided evidence of introgression where nuclear molecular or morphological evidence of such has been lacking (Rieseberg and Wendel, 1993
). In the current study, morphological, cpDNA, and nuclear rDNA markers have been used to identify Rhododendron individuals in northeast Turkey that contain germplasm of more than one species, allowing investigation of instances of hybridization and introgression among the four species of Rhododendron subsection Pontica that occur in this region.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, modified as follows: ground material in hexacyltrimethylammonium bromide (CTAB) buffer was warmed to 65°C and washed with 24:1 chloroform/isoamyl in place of methylene chloride; the extracts were treated with RNAse (1%, 20 µL/extract) for 1 h before precipitation; DNA was precipitated with two volumes of ice cold 96% ethanol. The sample was purified as follows: half a volume of 7.5 mol/L sodium acetate was added, the mixture cooled for 20 min and centrifuged; the supernatant was precipitated with ethanol as above and rinsed with 76% alcohol/0.2 mol/L sodium acetate (twice) and 76% alcohol/10 mmol/L ammonium acetate (once), then resuspended in tris(hydroxymethyl)methylamine/ethylenediaminetetra-acetic acid (EDTA) buffer.
One accession of each species was selected for an initial RFLP survey to detect enzyme/probe combinations that might distinguish the cpDNA and rDNA of the four species. Material of R. ponticum was represented by a single accession from Istranca Daglari, northwest Turkey, while the other three species were represented by single accessions raised from wild seed collected in northeast Turkey. DNA extracts of these accessions were digested with 13 restriction enzymes to produce fragments that were separated by electrophoresis on 1% agarose gels. Following denaturation and neutralization, the fragments were transferred by Southern blotting to Electran (BDH) nylon membranes. Probe fragments were labeled with Digoxigenin (Boehringer Mannheim, Sussex, UK) according to the manufacturer's protocol. Membranes were hybridized with the labeled probes, washed and then detection was carried out using Anti-Digoxigenin and CSPD (disodium 3-(4-methoxyspiro{1,2-dioxetane-3,2'-(5'chloro)tricyclo[3.3.1.13,7]decan]-4-yl)phenyl phosphate) following the same protocol. Various combinations of the Lactuca sativa cpDNA probes (pLsC) described by Jansen and Palmer (1987)
were employed. All 13 enzymes (BamH1, Bcl1, Bgl2, Cla1, Dra1, EcoR1, Hae3, Hind3, Hpa2, Rsa1, Sal1, Sma1, and Stu1) were used in conjunction with the combined pLsC probes 7, 9, 14, and 10, which are arranged contiguously in the cpDNA molecule (Jansen and Palmer, 1987
). In addition, Bcl1, Bgl2, Cla1, EcoR1, Hpa2, Sma1, and Stu1 digests were probed with pLsC6; Bcl1, Bgl2, Hpa2, and Stu1 digests were probed with pLsC4; BamH1 and Hpa2 digests were probed with pLsC2; and Bcl1 and Bgl2 digests were probed with the probes pLsC 5, 11, 12, and 13 combined. Thus, in the initial screen a total of 26 enzyme/probe combinations were employed. Membranes containing fragments of the four species, produced after digestion with each of the 13 restriction enzymes, were also probed with the Triticum aestivum rDNA probe pTa71, which is 9.1 kb in size (Gerlach and Bedbrook, 1979
). After analyzing one accession of each species in this way, all of the remaining Rhododendron material was examined using only those enzyme/probe combinations that best distinguished the four species.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), and cpDNA haplotypes were therefore identified by the presence or absence of fragments (Table 3).
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Rhododendron ungernii x R. ponticum
Two accessions from Tiryal Daga possessed the cpDNA of R. ponticum and an additive rDNA profile of R. ponticum and R. ungernii and appear to represent the first records of a hybrid between these two species. These had corollas a lighter shade of pink than R. ponticum, sparsely white-hairy ovaries, long calyx lobes similar in size to typical R. ungernii, and very small crisped hairs on the leaf underside (Table 2). They occurred at ~1600 and 1750 m, respectively, in Rhododendron scrub where R. ungernii and R. ponticum were common and R. smirnovii occasional. A third accession from this area also had an additive rDNA profile of the two species, but was closer to R. ponticum in morphology (specifically, the corolla color was similar to pure R. ponticum and the calyx lobes were less prominent). Six other accessions from the vicinity possessed sparse ovary hair and/or long calyx lobes, but matched pure R. ponticum in other morphological and molecular characteristics; many other accessions were observed with similar characteristics but were not subjected to molecular examination. One accession of R. ungernii was found in this area that had white flowers and showed no morphological evidence of introgression, but had the cpDNA of R. ponticum and an additive rDNA profile of both species. Thus it appears that bidirectional introgression occurs following F1 production between these two species and that backcrosses towards R. ponticum are considerably more numerous than F1s. These results do not suggest that introgression from R. ponticum has contributed to the flower color polymorphism in R. ungernii. However, as only one putative backcross to R. ungernii was detected, the results do not provide strong evidence against the possibility.
Rhododendron ponticum x R. smirnovii
One accession, present at ~1400 m in the Tiryal Daga area, appeared to represent a hybrid derivative of R. ponticum and R. smirnovii (Table 5). It had short calyx lobes, a pubescent ovary, and sparsely pubescent ventral leaf surface, but all corollas had fallen. The accession had the cpDNA of R. smirnovii and expressed four rDNA bands, of which two were those unique to R. ponticum and two (4.71 and 5.49 kb) were common to R. smirnovii and R. caucasicum. As the involvement of R. smirnovii is proved by the cpDNA profile and the accession was collected 600 m below the normal range of R. caucasicum and 300 m below that of R. x sochadzeae, the accession must be a derivative involving R. ponticum and R. smirnovii, and the additional involvement of R. caucasicum is unlikely. Therefore, the rDNA profile observed is likely to be an additive profile of R. ponticum and R. smirnovii minus the distinctive 2.50-kb fragment of the latter (Table 4).
Rhododendron caucasicum x R. smirnovii
Rhododendron smirnovii and R. caucasicum occur together on the hill above Artvin, and one small group of putative hybrids, intermediate in morphology between the two species, was present at this site. All five individuals examined had an rDNA profile that could be R. smirnovii, or R. smirnovii plus R. caucasicum; however three accessions had the cpDNA of R. caucasicum and are thus shown to be hybrids by the molecular data (Table 5). The other two accessions had the cpDNA of R. smirnovii, but their morphological similarity to the other two accessions strongly indicates that these had a similar hybrid origin. Therefore it appears that either one of these two species can act as the cpDNA donor in this hybrid derivative. No firm evidence of backcrossing in either direction was detected, although two accessions of R. caucasicum with pale-pink flowers may have been backcrosses from R. smirnovii, but no cpDNA or rDNA evidence of such was detected (Table 5).
Rhododendron ponticum x R. caucasicum (= R. x sochadzeae)
The hybrid between R. ponticum and R. caucasicum, R. x sochadzeae, was plentiful on the hill above Artvin, mixed with similar numbers of R. caucasicum and R. smirnovii. It was also common at Tiryal Daga where it occurred in virtual monoculture on slopes between 1900 and 2100 m, although not on the steeper or rockier slopes, where it was replaced by R. smirnovii. Of 13 accessions sampled from these locations, all had the cpDNA of R. caucasicum and 11 had an additive rDNA profile of R. caucasicum and R. ponticum; the remaining two expressed only the rDNA bands of R. caucasicum (Table 5). Three accessions of R. x sochadzeae were collected from lower altitudes, among populations of R. ponticum, and these were more variable in their molecular characteristics. One had the cpDNA of R. ponticum and an additive rDNA profile of R. ponticum and R. caucasicum, a second had the same additive rDNA profile and the cpDNA of R. caucasicum, and the third had the molecular characteristics of R. caucasicum alone. In addition, two accessions of morphologically typical R. ponticum at Artvin, and one at Camlihemsin, all in close proximity to accessions of R. x sochadzeae, showed evidence of nuclear introgression in that they expressed the rDNA bands of R. caucasicum. Two accessions were found at Artvin that matched R. caucasicum in molecular and morphological characterization, except for having very pale-pink flowers. These accessions may have been backcrosses towards R. caucasicum from R. x sochadzeae, or from R. smirnovii as suggested above.
Six hybrid accessions from the hybrid zone at Camlihemsin were examined, of which five had the cpDNA of R. caucasicum and one had the cpDNA of R. ponticum. Five accessions possessed the additive rDNA profile of the two species, but one, which resembled R. ponticum more closely in morphology, expressed only the rDNA bands of R. caucasicum.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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for Louisiana irises in which F1 formation was rare although later generation hybrid derivatives were common. In the fourth case (R. smirnovii x R. caucasicum), a single small group of putative F1 individuals was detected, whereas in the final case (R. smirnovii x R. ponticum) only a single individual hybrid derivative was found. In these last two cases it was not certain whether backcrosses might be formed but were not detected, or whether the F1s do not, or only rarely, generate progeny.
The present study has also documented examples of nuclear without cytoplasmic introgression (R. caucasicum into R. ponticum; R. smirnovii into R. ungernii) and of both nuclear introgression and plastid transfer without apparent morphological introgression (R. ponticum into R. ungernii). An apparent example also occurred of the loss of part of one parent's rDNA profile in a hybrid derivative: the putative R. ponticum x R. smirnovii individual had both rDNA fragments of R. ponticum but just two of the three fragments characteristic of R. smirnovii. The loss of all rDNA fragments from one species from the profile of an F1 has been observed in Zea (Zimmer, Jupe, and Walbot, 1988
), Avena (Fabijanski et al., 1990
), and Senecio cambrensis (Harris and Ingram, 1992
), and could result from concerted evolution. However, the loss of part of a profile would appear to require either recombination within a hybrid or rDNA polymorphism within R. smirnovii.
The four Rhododendron species investigated occur together in the Tiryal Daga (northeast Turkey) area, where all of the hybrid combinations mentioned except R. smirnovii x R. caucasicum were observed. All four species are abundant at this site and despite the evidence of gene flow between them, in the field the great majority of plants could easily be referred to one species. The site appears to have been subject to human disturbance, and much of the Rhododendron scrub here may result from tree felling. This may have reduced the effect of habitat preferences as barriers to contact and hybridization between species. In contrast, R. ponticum and R. ungernii occur side by side in an undisturbed woodland at Savval Tepe and here no hybrids were found.
In general, the morphology of R. x sochadzeae was observed to be remarkably consistent at Artvin and Tiryal Daga, which concurs with the observations of Stevens (1978)
and Güner and Duman (1998)
. Accessions whose morphology indicated a backcross from R. x sochadzeae to either parent were very rare compared to accessions with the intermediate morphology typical of large populations of R. x sochadzeae. The consistent morphology of this hybrid would suggest that segregation of morphological characteristics is not occurring. In contrast, at Camlihemsin a very different situation existed. Here a small number of individuals of R. caucasicum occurred at ~1600 m in a northeast-facing valley, which was both very steeply sloping and steep-sided and in which snow patches persisted until at least late June; there was no sign of recent human habitat disturbance in this valley. Rhododendron ponticum grew abundantly on the sides of the valley, and hybrid derivatives of the two species were more common than R. caucasicum with which they occurred in the valley bottom. In this case, the intermediate phenotype did not predominate among the hybrids and a gradation of colors from creamy white to magenta was observed. Also there was no altitudinal zonation of the two species and their hybrids as there was at Tiryal Daga.
Clearly the limited molecular results presented here do not answer the question of why the morphology of the R. x sochadzeae hybrid in some populations appears constant. Clonal reproduction has been reported in some Rhododendron species, for example R. ferrugineum, a distantly related species that occurs at similar altitudes in the European Alps (Escaravage et al., 1998
), and could account therefore for some of the phenotypic uniformity observed in R. x sochadzeae. However, it is unlikely to be the sole explanation, because even if reproduction is predominately clonal at sites like Tiryal Daga, there must be some recruitment from seed, and as the presence of backcrosses at Camlihemsin indicates that the F1 is fertile, the problem of why only F1s or phenotypically intermediate individuals are recruited is not circumvented.
Another possible explanation is that the large populations are polyploid and behave as a species while the hybrid zone at Camlihemsin is homoploid. However, an accession grown from seed collected by R. Milne from the center of a large R. x sochadzeae population at Tiryal Daga was found to have the same chromosome number, 2n = 26, as both parents (Dr. H. McAllister, University of Liverpool, personal communication). Furthermore, no other polyploids are known within subgenus Hymenanthes, and R. x sochadzeae has never been recorded outside of the ranges of its two parents, which one might expect were it an independent polyploid species. Alternatively, some factor may make backcrosses rare in the presence of large numbers of F1s; one possibility is that flower-constant pollinators may be unlikely to transfer pollen between the hybrid and its parent species (Rieseberg and Wendel, 1993
; Wolfe, Xiang, and Kephart, 1998
). Also, selection against backcrosses has occasionally been observed in other plant species (Keim et al., 1989
; Bert and Arnold, 1995
; Allan, Clark, and Rieseberg, 1997
), and this may occur in R. x sochadzeae. Such ecological selection may have led to speciation in the putative diploid hybrid species Encelia virginensis (Allan, Clark, and Rieseberg, 1997
), which differs from R. x sochadzeae in that it now occurs allopatrically from its parents. A possible hypothesis is that R. x sochadzeae benefits from having a set of coadaptive genes from each parent, which confer hardiness to higher altitudes (R. caucasicum) and competitiveness at lower altitudes (R. ponticum) and only plants that are genetically intermediate contain both complete sets of these genes. If backcrossing were rare and most hybrid derivative individuals arose from crosses between intermediates rather than recruitment of new F1s, then the effects of segregation would disappear through several generations, as is the case in stabilized hybrid derivatives (e.g., Arnold, 1993
; Urbanska et al., 1997
). Whatever mechanism limits backcross formation at Tiryal Daga and Artvin, it has clearly broken down at Camlihemsin, possibly because R. caucasicum and R. x sochadzeae are present in relatively small numbers there. If R. x sochadzeae is preferentially pollinated by R. x sochadzeae pollen, then this might limit backcrossing where it is abundant but not where it is greatly outnumbered by R. ponticum, as at Camlihemsin. A comparable situation exists between two salamander races, which do not normally breed where their ranges meet but formed a hybrid swarm where an outlier of one race was surrounded by greater numbers of the other (Wake, Yanev, and Frelow, 1989
). There may be some parallels between R. x sochadzeae and Rhododendron x intermedium (R. ferrugineum x R. hirsutum), which is rare at some sites where parents co-occur, but abundant at others (Grant, 1981
); however this hybrid does not appear to have been observed or studied in detail.
The nature of R. x sochadzeae as a taxon remains open to question. Although the molecular results here confirm that it is the hybrid between R. ponticum and R. caucasicum, the morphological consistency of R. x sochadzeae suggests that it is a stabilized hybrid derivative. However, it occurs in the vicinity of both parents, and accessions with more variable molecular characteristics were observed outside of the main R. x sochadzeae population. This indicates that hybridization continues to occur between the parent species, and there is no reason to assume these hybrids are not interfertile with the other R. x sochadzeae plants. Rhododendron x sochadzeae may be an entity that combines the beneficial traits of both parents, maintains a degree of phenotypic consistency through selection against backcrosses and extreme segregants, and retains an unusually high genetic diversity through periodic recruitment of F1s. Further investigation of the genetics of R. x sochadzeae could be highly informative in regard to studies of interactions between fertile hybrid populations and their parents, and hence the mechanisms underlying hybrid speciation.
The evidence of this study indicates that hybrid formation between sympatric species of Rhododendron is likely to be common, and for closely related species may be the rule rather than the exception. As the four species in this study belong to the same subsection (Pontica, subgenus Hymenanthes), the results do not necessarily indicate whether less closely related species of Rhododendron form hybrids as frequently as these species. From these results, however, it is reasonable to assume that hybridization is probably fairly frequent between sympatric species of subgenus Hymenanthes, particularly in the Himalaya region where such species are most concentrated and, for example, many species of the large subsection Taliensa have been recorded within one small area (Chamberlain, 1982
). It would be of interest, therefore, to determine how such species are maintained in sympatry despite interspecific gene flow and whether hybridization has been a significant factor in the evolution of the large number of species within the genus Rhododendron.
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FOOTNOTES |
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3 Current address: Department of Agricultural and Environmental Science, University of Newcastle, Newcastle upon Tyne, NE1 7RU, UK.
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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