AOBPreview originally published online on August 23, 2008
Annals of Botany 2008 102(5):685-697; doi:10.1093/aob/mcn151
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Morphological and AFLP-based Differentiation within the Taxonomical Complex Section Caninae (subgenus Rosa)
1 Research Institute for Nature and Forest (INBO), Scientific Institute of the Flemish Government, Kliniekstraat 25, B-1070 Brussels, Belgium
2 Institute for Agricultural and Fisheries Research (ILVO), Scientific Institute of the Flemish Government, Burg. Van Gansbergelaan 96 bus 1,B-9820 Merelbeke, Belgium
* For correspondence. E-mail peter.breyne{at}inbo.be
Received: 16 April 2008 Returned for revision: 9 June 2008 Accepted: 10 July 2008 Published electronically: 23 August 2008
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ABSTRACT |
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Background and Aims: The taxonomical structure of the polymorphic subgenus Rosa section Caninae is highly complex due to the combination of some unusual features: the unique polyploid chromosomal constitution, the heterogamic canina meiosis, the ability to hybridize interspecifically, and the predominantly matroclinal inheritance. Although most taxonomists agree on the subdivision of the section into three morphologically well-defined groups (Rubigineae, Vestitae, and Caninae), they disagree on the existence of smaller groups such as Tomentellae. The aim was to gain insight in the taxonomical structure and investigate the interpopulation differentiation of the polymorphic section Caninae by analysing morphological and AFLP-based characters of the seven most common Belgian dog-rose taxa.
Methods: The intersubsectional and -specific relationships within the dog-roses were examined using morphological and molecular-genetic markers. AFLP data were analysed with basic descriptive genetic statistics because of the lack of Hardy–Weinberg equilibrium due to the polyploid genetic structure and heterogamic meiosis.
Key Results: Both the morphological and AFLP-based analyses supported the subdivision of the dog-roses in three well-defined though partly overlapping groups, Rubigineae, Vestitae and Caninae. However, it was not possible to distinguish between the morphologically well-defined taxa within the same subsection using AFLP-based data. In addition, the results suggested a high similarity of Rosa balsamica with subsection Caninae taxa. Small-scale geographical AFLP-based differentiation was observed within several dog-rose taxa. Surprisingly, individuals sampled at one locality and belonging to morphologically distinct dog-rose taxa displayed higher genetic similarities in comparison to their congeners sampled at different localities.
Conclusions: The hybridogenic character of the dog-roses was reflected in the vague boundaries between the subsections and on the species level within the subsections. Indications were found for current or historical hybridization on the genetic structure of the population. No morphological or AFLP-based evidence was obtained to support the existence of the separate subsection Tomentellae.
Key words: Subgenus Rosa, Caninae, Rubigineae, Vestitae, Tomentellae, Rosa balsamica, dog-rose, polyploidy, interspecific hybridization, intraspecific morphological variation, AFLP-based diversity, taxonomy
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INTRODUCTION |
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The genus Rosa L. (Rosaceae) is naturally distributed throughout the temperate and subtropical regions of the northern hemisphere (Rehder, 1940). Worldwide, the genus comprises between 100 and 250 botanical species, while about 30–60 endemic species are located in Europe (Henker, 2000). The genus Rosa consists of four subgenera of which the largest subgenus Rosa L. is subdivided into ten sections. The most numerous and complex section in Europe is the section Caninae (DC.) Ser. 1825, from this point on referred to as dog-roses.
Wild roses have a base chromosome set that consists of seven chromosomes (Täckholm, 1920, 1922; Blackburn and Heslop-Harrison, 1921) and the ploidy levels range from diploid (2x) to octoploid (8x). The pentaploid (5x) chromosomal constitution observed in the dog-roses is unique and reflects the original genomes of the allopolypoid hybridogenic origin. Two of the five chromosome sets, the so-called bivalent-forming chromosomes, are highly homologous and exchangeable among all section Caninae taxa (Nybom et al., 2006). Probably, they originate from a common Protocanina ancestor (Wissemann, 1999). The remaining three chromosome sets, the so-called univalent-forming chromosomes, are inherited apomictically through the seed parent (Nybom et al., 2006) and originate from different non-Caninae species through multiple hybridizations (Wissemann, 1999). These non-recombining haploid genomes can be assumed to act as different and independent gene pools and are proposed to reflect the taxonomical distance among the taxa (Nybom et al., 2006). In contrast to the large polymorphisms observed within the dog-roses, all species share the atypical chromosomal constitution and the heterogamous canina meiosis in which the progeny receives one of the bivalent- and all the univalent-forming chromosome sets from the seed parent and only one of the bivalent-forming chromosome sets of the pollen parent (Täckholm, 1920, 1922; Blackburn and Heslop-Harrison, 1921). This uneven allocation of maternal and paternal chromosomes to the progeny, also called hemisexuality, has a significant impact on the species. First, there is a tendency to a skewed maternal inheritance (Ritz et al., 2005; Wissemann, 2005; Wissemann and Ritz, 2005). Secondly, genetic recombination is restricted to the highly homologous bivalent-forming chromosomes (Nybom et al., 2004). In addition, dog-roses have the ability to hybridize among sections and subsections, to produce both sterile and fertile hybrids, and to reproduce through sexual and asexual strategies. These features all lead to a hybridogenic and highly polymorphic species-complex in which spontaneous hybrids are disguised and well-defined species groups are delimited (Ritz and Wissemann, 2003; Wissemann and Hellwig, 1997). The apparent morphological similarities allow the taxa to be merged into fewer but more diverse species-groups according to the preferences of the taxonomists. Nilsson (1999) divided the dog-rose species into three groups (Rosa rubiginosa, Rosa villosa and Rosa canina). Graham and Primavesi (1993) described four subsections (Rubiginosae, Villosae, Caninae and Stylosae), and both Henker (2000) and Wissemann (2003) agreed on six subsections (Rubigineae, Vestitae, Tomentellae, Caninae, Rubrifoliae and Trachyphyllae). Previous morphometrical and molecular-genetic (RAPD, STMS) research on wild dog-rose parents and their interspecific progeny (Nybom et al., 1996, 1997, 2006; Werlemark et al., 1999; Olsson et al., 2000; Werlemark and Nybom, 2001; Nybom et al., 2004) supported the subdivision of the analysed dog-rose species as was proposed by Nilsson (1999), and Graham and Primavesi (1993) excluding the Stylosae. Unless mentioned otherwise, the groups or subsections within the dog-roses are referred to using the nomenclature of Henker (2000).
A few distinct morphological characters delimit the three major groups within the section Caninae (Table 1). The first subsection Rubigineae is characterized by numerous, sticky glands on the leaflets spreading a typical strong scent of apples or vines. The taxa of the second subsection Vestitae display tomentose leaflets, and carry persistent stipitate glands on hips and pedicels spreading a turpentine odour. The taxa of the third group show a variation in pubescence and presence of odourless glands on the leaflets. According to Graham and Primavesi (1993) and Nilsson (1999), these taxa belong to the subsection Caninae, whereas both Henker (2000) and Wissemann (2003) split this group into two subsections: Caninae and Tomentellae. According to these latter authors, Rosa balsamica belongs to the subsection Tomentellae (Table 2).
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The present study reports on the morphological and AFLP-based variation within and among dog-rose populations in Belgium. We assessed (a) the differentiation of the dog-rose species in Belgium and correlate it to their taxonomical subdivision, and (b) the within- and between-population diversity in several Belgian dog-rose taxa.
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MATERIALS AND METHODS |
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Sampling wild rose shrubs
In total, 723 wild rose shrubs, belonging to seven dog-rose species – R. canina, Rosa corymbifera, R. balsamica, R. rubiginosa, Rosa agrestis, Rosa micrantha and Rosa tomentosa (Table 2) – were sampled in Belgium (Fig. 1). The shrubs were identified and classified according to the taxonomy of Henker (2000). Leaves were dried according to the standard herbarium protocols and hips were stored in ethanol (96 %). For the AFLP-based analyses, young and fresh leaflets were frozen in liquid nitrogen, lyophilized, and stored at –18 °C until DNA extraction.
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Morphological analysis
In a previous study, 17 diagnostic characters were determined with principal component analyses (PCA; De Cock et al., 2007; De Cock, 2008). The morphometric data, e.g. length and width of leaflets and hips, were explored in box and whisker plots, and the descriptive characters, such as frequency of glands on the leaflets' upper side, on hips or pedicels, were visualized in histograms. Additional principal components and canonical discriminating analyses were performed on these 17 factors in order to select the independent characters. All analyses were performed using S-Plus 6·2 Professional (Insightful Corporation). The detailed procedure is described in De Cock et al. (2007).
AFLP analysis
Three hundred nanograms of DNA were produced from 25 mg dried leaf material following the instructions of the Qiagen DNeasy Plant Mini Kit (Westburg, The Netherlands). The AFLP procedure was performed according to Vos et al. (1995). The restriction–ligation reaction was performed in one step. The amplification of the fragments was performed in two steps using the primer combinations EcoRI–AAG/MseI–CAT, EcoRI–AAG/MseI–CAG and EcoRI–ATC/MseI–CTA. The amplified fragments were separated on the Global Edition IR2 system of LI-COR (LI-COR) and visualized in automatically generated TIFF-files. Fragments were automatically scored using SAGA-MX version 3·0 (LI-COR). Additional manual controls and corrections were performed. In total, 150 fragments with a size range of 75–652 bp were evaluated and transformed into a binary matrix (presence, 1; absence, 0) that was used as an input file for several statistical programs.
AFLP-based data analysis
Distance matrices were computed with the Jaccard similarity coefficient, and visualized in biplots of principal co-ordinate analyses (PCO) using Splus 6·2 Professional. TREECON version 1·3b (Van de Peer and De Wachter, 1994) calculated pair-wise genetic distances by the simple matching algorithm (100 bootstraps). The dendrograms were drawn with UPGMA (unweighted pair group method with arithmetic mean) cluster analyses, repeated x100. The most probable number of gene pools was estimated and individuals were assigned to the inferred populations using the Bayesian approach (Structure; Pritchard et al., 2000), with the adaptations suggested by Evanno et al. (2005). RAPDDIV (Whitkus et al., 1998) determined the partitioning of the diversity within and among different populations of R. canina and R. corymbifera. The diversity was calculated with the Shannon–Weaver diversity index using the Brillouin formula to eliminate the bias of finite sample sizes. This approach is based on band phenotypes, and does not rely on the Hardy–Weinberg assumptions. Only one of the representative congruent results is shown.
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RESULTS |
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Morphological evaluation
Selection of independent diagnostic characters
The 17 morphometric and descriptive diagnostic characters explained at least 50 % of the variation in the three principal components. Nine independent characters were identified based on the loadings of the PCA (Table 3): the number of glands on the leaflet margin and pedicel, the length of the leaflet and pedicel, the serration of the leaflet margin, the pubescence on the upper and lower side of the leaflet, and the diameters of disc and orifice. They were analysed separately in box and whisker plots (Fig. 2) or histograms (Fig. 3) in order to assess inter- and intraspecific variation within the dog-roses. The impact of these characters on the hierarchical structure within the dog-roses was visualized in a PCA biplot (Table 3 and Fig. 4).
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Interspecific morphometrical variation
Based on the measured characters, several interspecific tendencies were observed (Fig. 2). The leaflet dimensions of R. tomentosa were highly variable in comparison to the other taxa examined. The taxa R. rubiginosa and R. micrantha were characterized by smaller and shorter leaflets, whereas the leaflets of R. canina, R. corymbifera and R. balsamica were clearly wider and longer. Rosa agrestis was characterized by intermediate leaflet dimensions. Concerning the hip characters, the diameter of the orifice did not display consistent differentiations among the taxa analysed except for R. rubiginosa where it was much larger. The diameter of the disc divided the taxa into two overlapping groups. Rosa canina, R. corymbifera and R. balsamica were the taxa with a larger disc, and R. agrestis, R. rubiginosa, R. micrantha and R. tomentosa displayed smaller disc diameters. The pedicels of R. tomentosa were longer compared with the other taxa.
Variation within descriptive characters
The pubescence and presence of the glands on the leaflets, hips and pedicels were highly variable within the dog-roses and formed the basis of the subdivision in subsections (Fig. 3). The leaflets of the subsection Rubigineae were densely glandular and mostly pubescent. Rosa tomentosa (subsection Vestitae) was characterized by densely pubescent and tomentose leaflets, and displayed persistent glandular hips and pedicels. Rosa canina, R. corymbifera (both subsection Caninae) and R. balsamica (subsection Tomentellae) all showed mainly eglandular pedicels and hips. Rosa corymbifera was characterized by eglandular rachides, leaflet margins and lower sides of the leaflet. For R. canina, they could be both eglandular or sparsely glandular. Glabrous and (irregular) uni- or biserrated (occasionally multiserrated) leaflets were typical for R. canina, whereas R. corymbifera had glabrous upper sides of the leaflet but the veins on the lower side were pubescent. The leaflets were (irregular) uniserrated. The rachides and leaflet margins of R. balsamica varied from sparsely to densely glandular and the veins at the lower side of the leaflet were moderately glandular. The upper sides of the leaflet were glabrous or sparsely pubescent, whereas the veins on the lower side were sparsely to moderately pubescent. The leaflet margins were mostly bi- to multiserrated or multiserrated.
Integration of diagnostic characters
In the PCA biplot that combined the four morphometric and five descriptive independent diagnostic characters, the taxa analysed grouped in three partly overlapping clusters (Fig. 4). The grouping reflected the taxonomical subsections. The subsection Rubigineae appeared as the most distinct group based on the pubescence on the leaflets, multiserrated and densely glandular leaflet margins, and the densely glandular rachides. Rosa rubiginosa displayed smaller leaflets and larger diameters of orifice compared with the other taxa analysed. The taxa of the subsection Rubigineae overlapped partly with R. balsamica (subsection Tomentellae) based on similar pubescence on the leaflets, presence of glands and serration of the leaflet margins (Fig. 4A). Rosa tomentosa of the subsection Vestitae displayed longer pedicels compared with the other dog-rose taxa and was characterized by densely pubescent or tomentose leaflets, strikingly glandular pedicels and hips (Fig. 4B). The taxa of the subsections Caninae and Tomentellae showed large overlap and formed a rather compact sphere. Yet, interspecific differentiation was present as each of these three taxa constituted the majority of the different parts of the sphere (Fig. 4C).
Intraspecific variation among pure and mixed populations
Tendencies towards intraspecific geographical differentiation were observed for several dog-rose taxa. A striking differentiation was observed between R. rubiginosa populations from the coastal region and the Maasvallei, situated about 250 km apart (Fig. 1). The coastal populations from the Westkust (WKU) consisted of over 60 R. rubiginosa shrubs and five R. canina or R. tomentosa shrubs. In contrast, the coastal population of Het Zwin (OKU) contained up to 100 R. canina and R. corymbifera individuals and about ten R. rubiginosa. Rosa micrantha was absent in the coastal region. At the Maasvallei, the population had a mixed presence with 19 R. rubiginosa, 11 R. micrantha, only four R. canina and one R. tomentosa. The R. rubiginosa of the Maasvallei population showed larger rachides and leaflets, and slightly smaller diameters of the orifice compared to those of the coastal populations (Fig. 5A, B). In addition, the R. micrantha individuals of the Maasvallei showed broader diameters of the orifice and disc (Fig. 5C, D), and the pedicels (data not shown) appeared to be shorter compared with their congeners from Brabants District Oost (BDO, with MV and BDO about 25 km apart) where R. rubiginosa is absent. The pedicels of R. rubiginosa Het Zwin (OKU) displayed a lower frequency in glands compared with their congeners at Maasvallei and Westkust (Fig. 6A). Similarly, the individuals at Het Zwin (OKU) that were morphologically defined as R. canina, R. corymbifera and R. balsamica, all showed a higher tendency to the presence of glands on the leaflets or pedicels compared with their congeners of populations lacking Rubigineae (Fig. 6B–F).
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AFLP-based interspecific variation
Differentiation within the dog-roses
None of the applied approaches used to analyse the AFLP markers was able to support the subdivision of the dog-rose species into a few distinct and well-defined groups. For instance, the similarity coefficients within section Caninae equalled 66 %, whereas the similarity among the subsections Caninae and Tomentellae was 68 % (Table 4). However, intersectional differentiation was observed. The subsection Rubigineae was the most differentiated, and formed a well-defined subcluster (Fig. 7A). When the subsection Rubigineae was excluded from the data set, the subsection Vestitae showed a tendency to form a separate cluster (Fig. 7B). Finally, PCO analyses performed on the two remaining subsections Caninae and Tomentellae could not detect any interspecific AFLP-based differentiation (Fig. 7C).
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AFLP-based variation in pure and mixed populations
The different approaches used to analyse the AFLP polymorphisms indicated a remarkable higher similarity among morphologically different species all originating from the mixed growth site compared with the similarity among congeners sampled at other localities (Fig. 7D, Table 5). For instance, the similarity coefficient among the R. canina, R. corymbifera and R. balsamica of Het Zwin (OKU) varied between 79 % and 100 %, whereas the similarity among different R. canina populations ranged between 69 % and 77 %. The partitioning of the diversity was assessed by comparing the within- and among-population variation for the two most common taxa: R. canina and R. corymbifera (Table 6). The genetic variation (HS) within R. canina was higher when more localities were taken into account (Table 6A, bold). Little to no difference was observed within (HS) or among (DST) R. canina or R. corymbifera sampled at the same locality. For instance, the within-differentiation of R. canina Het Zwin equalled that of R. corymbifera Het Zwin and R. corymbifera Heers (HS = 0·16 for all populations; Table 6A, underlined). In addition, the differentiation between the two Het Zwin populations (DST) was set on 0·18 (Table 6A). Comparing the partitioning of the differentiation among the two taxa sampled at five localities with the differentiation among the five localities, the genetic variation among the localities was clearly higher (DST = 0·34) than the variation among the two taxa sampled at these localities (DST = 0·16; Table 6A, B, italics).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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The observed inter- and intraspecific variation in the dog-rose taxa is influenced by large phenotypic and genetic plasticity, the ability to hybridize, the unique polyploid chromosomal constitution, the heterogamous canina meiosis, and the predominantly matroclinal inheritance. The combination of these factors leads to a complex and ambiguous taxonomical hierarchy which is subject to discussion. The hierarchical structure of the dog-roses into three groups as proposed by Graham and Primavesi (1993) and Nilsson (1999) and supported by an extensive study of the morphometrical and genetic characters of wild individuals and the interspecific progeny (Nybom et al., 1996, 1997, 2004, 2006; Werlemark et al., 1999; Olsson et al., 2000; Werlemark and Nybom, 2001) was confirmed by the present morphological and AFLP-based analyses. However, the boundaries among the observed groups were vague and indicated the presence of intermediate morphological states and the hybridogenic character of the dog-roses.
Within the dog-roses, the subsection Rubigineae was the most differentiated in both the present morphological and AFLP-based analyses. This confirmed the results of the morphometrical study (Nybom et al., 1996), the RAPD (Olsson et al., 2000) and STMS analyses (Nybom et al., 2004) in which R. rubiginosa was used to represent the subsection Rubigineae. Similarly, the AFLP analysis of Koopman et al. (2008) describes the subsection Rubigineae as a derived and genetically defined group within the dog-roses. The interspecific differentiation may be due to one or more distinct non-Caninae parent(s) in the historical hybridization event leading to the origin of the subsection Rubigineae taxa. Most likely, this putative historical parental species passed on some distinct univalent-forming chromosomes. Alternatively, the bivalent-forming chromosomes may be less homologous compared with the other Caninae subsections; however, this should impose a barrier for the reproducibility of interspecific hybrids (Nybom et al., 2006). This barrier is in conflict with the observations of successful controlled interspecific crossings (e.g. Werlemark et al., 1999) and of spontaneous interspecific progeny (Graham and Primavesi, 1993; Feuerhahn and Spethmann, 1995) including a subsection Rubigineae parent. The fertility of the interspecific progeny depends on the homology of the bivalent-forming chromosomes of the parents (Nybom et al., 2006). Therefore, the differentiation of the Rubigineae is most likely caused by distinct univalent-forming chromosome sets.
Excluding the most distinct subsection Rubigineae, a morphological and genetic differentiation of the subsection Vestitae with the subsections Tomentellae and Caninae was observed. The boundaries of this subdivision were more vague compared with the differentiation of the subsection Rubigineae. Previous cpDNA analyses have divided the dog-roses into the odorant glandular taxa (cf. Rubigineae and Vestitae) and the eglandular or non-odorant glandular taxa (cf. subsections Caninae, Tomentellae; Wissemann and Ritz, 2005) supporting the assignment of the subsection Vestitae to a separate cluster. Koopman et al. (2008) were not able to distinguish the subsection Vestitae from the subsections Caninae and Tomentellae in their phylogenetic analyses. Since they emphasize the phylogenetic relationships within the whole subgenus, their selected markers may not be sufficiently discriminatory at the lower taxonomical structures within the dog-roses.
In contrast to the classifications of Henker (2000) and Wissemann (2003), neither the present morphological nor the present AFLP-based approach was able to differentiate among the subsections Caninae and Tomentellae. In our morphological analyses, R. balsamica overlapped with the subsections Caninae and Rubigineae, which confirmed the morphological similarity of R. balsamica with both subsections as was mentioned by Wissemann (2000). The previously proven matroclinal inheritance of leaflet dimensions (Werlemark et al., 1999) and epicuticular wax structures (Wissemann, 2000) both indicate the historical influence of a subsection Caninae taxon in R. balsamica. Alternatively, the presence of glands on the leaflets may originate from a subsection Rubigineae ancestor. Additional PCA analyses restricted to the subsections Caninae and Tomentellae indicated that the pubescence and glands on the R. balsamica leaflets supplemented the observed variation in R. canina and R. corymbifera. In addition, it was not possible to observe any intersubsectional or -specific AFLP-based differentiation for the analysed taxa of these two subsections. Moreover, the observed similarity among R. canina, R. corymbifera and R. balsamica equalled the similarity within each of these three taxa. Consequently, it was assumed that these taxa share highly related univalent-forming chromosome sets. The strong similarity of R. balsamica with the subsection Caninae has already been indicated by independent research methods and tools such as the chemical composition of the epicuticular waxes (Wissemann, 2000), nrITS-sequences and cpDNA analyses (Wissemann and Ritz, 2005). Until now, no indications were found that support the subdivision of R. balsamica from the subsection Caninae taxa.
Even within the small geographical area of Belgium, intraspecific geographic variation was observed among populations that indicate past or present-day hybridization. The values of the well-defined morphometric species-specific characters of R. rubiginosa from the coastal populations are congruent with those described in literature. In the mixed R. rubiginosa–R. micrantha population of the Maasvallei, intermediate values between those of the parental species have been observed. The orifice diameter is described as >1 mm for R. rubiginosa, whereas it is <1 mm for R. micrantha (Henker, 2000). Rosa rubiginosa sampled at the mixed Maasvallei-population displayed smaller diameters compared with the literature and to the congeners of the putative pure populations; whereas for R. micrantha, larger diameters were observed. Also for the rachis length of R. rubiginosa and the disc diameter of R. micrantha intermediate values were measured. Within the taxa R. canina, R. corymbifera and R. balsamica, intraspecific geographical variations were observed at the morphological level. The individuals of the mixed population Het Zwin all displayed a higher frequency of glandular leaflets compared to their congeners sampled at the other localities. This may indicate the past hybridization influence of R. rubiginosa. In addition, R. rubiginosa in Het Zwin (OKU) displayed fewer glands on both hips and pedicels compared with their congeners in Maasvallei. Moreover, the morphological intraspecific variation observed in R. canina, R. corymbifera and R. balsamica was supported by the higher genetic similarity among morphologically different taxa that were sampled at the same locality, compared with the similarity among congeners sampled at localities with a different composition of taxa. In other words, the genetic structure of these individuals reflected the common growth site instead of the taxonomical position. It can be hypothesized that past introgression events (interspecific hybridizations and backcrossing) in a mixed population such as Het Zwin resulted in more similar genetic constitutions and that genes responsible for the morphological differentiation between the taxa are limited and not highlighted with the applied molecular techniques. This may indicate that the differentiation among these taxa is a relative young phenomenon and is still in progress.
In conclusion, the taxa and subsections of the dog-roses are distinguishable by a set of well-defined morphological characters. However, the large and consistent overlap of the morphologically defined groups indicates the occurrence of intersubsectional and -specific hybridization that results in a combination of intermediate, transgressive and species-specific characters. In addition, these morphologically separable taxa are only to a certain extent distinguishable using routinely applied molecular-marker techniques. The allopolyploid origin of the non-recombining univalent-forming chromosomes can be responsible for the variable genetic similarities among the taxa. Even more, when different closely related dog-rose species are present at the same growth site, the genetic structure may show more differentiation between localities than between taxa. From an evolutionary point of view, the canina meiotic system has probably developed fairly recently (Lim et al., 2005), supporting the idea that the dog-roses are rather young (Atienza et al., 2005). Consequently, the intersubsectional boundaries are still being created, or are disappearing. Possibly, the partly apomictic character of the canina genome hampers quick evolutionary species formations and prevents the large-scale species differentiation in the dog-roses.
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ACKNOWLEDGEMENTS |
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We are grateful to M. Vanloosveldt for his help with the morphological analyses, L. Verschaeve for assistance with the AFLP analyses, and P. Quataert and P. Verschelde for their statistical support. The research was funded by the Agency of Nature and Forest of the Flemish Government (B&G/19/2001).
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LITERATURE CITED |
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