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2Harvard University Herbaria, 22 Divinity Avenue, Cambridge, Massachusetts 02138; 3Department of Plant Biology, University of New Hampshire, Durham, New Hampshire 03824; and 4Department of Biochemistry and Molecular Biology, University of New Hampshire, Durham, New Hampshire 03824
Received for publication April 3, 1998. Accepted for publication March 26, 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Hamamelidaceae • ITS DNA sequences • homoplasy • phylogeny
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Zhang and Lu, 1995
). This family is known for its broad geographic distribution, high number of endemics, monotypic or oligotypic genera, and diverse morphology (Bogle, 1968
; Endress, 1989a,
b,
c,
1993
).
The geographic range includes eastern and southern Africa, Madagascar, northeastern Australia, western, central, and southeastern Asia, eastern North America, Central America, and northern South America (Gentry, 1993
; Ulloa and Jørgensen, 1993
; Zhang and Lu, 1995
; Lozano-Contreras, 1996
; Rakotobe, 1996
). Whereas most of the genera occur in the Northern Hemisphere, five genera are distributed only in the Southern Hemisphere, including Trichocladus Pers., Ostrearia Baill., Neostrearia Smith, Noahdendron Endress, Hyland et Tracey, and Dicoryphe Du Petit-Thouars. More than half of the genera in the Hamamelidaceae are endemic to very restricted areas. For instance, Ostrearia, Neostrearia, and Noahdendron are distributed only in the rainforests of northeastern Queensland, Australia; Maingaya Oliv. is endemic to northeastern Malaysia; Fortunearia Rehd. et Wils., Sinowilsonia Hemsl., Semiliguidambar Chang, and Shaniodendron (Chang) Deng, Wei et Wang can be found only in small areas of China. However, there are two genera in this family whose species are widely and disjunctly distributed in several continents. One of them is Liquidambar L., which can be found in western Asia, southeastern Asia, southeastern North America, and Central America (Bogle, 1968,
1986
); the other disjunct genus is Hamamelis L., which is composed of species distributed in southeastern Asia, eastern North America, and northern Mexico (Mione and Bogle, 1990
). In the Hamamelidaceae, while many genera are either monotypic or oligotypic, there are several genera that contain more than ten species, such as Corylopsis Sieb. et Zucc., Dicoryphe, and Distylium Sieb. et Zucc. (Chang, 1979
; Endress, 1993
; Rakotobe, 1996
).
Morphological characters in the Hamamelidaceae are highly diverse. For example, leaves are persistent or deciduous, simple and pinnately veined, or palmately lobed and veined. Most species are bisexual, but some are andromonoecious, and still others are monoecious. Flowers are complete and five-merous in most genera, four-merous in several genera, and variable in others; a few genera have an incomplete perianth, or are naked. Flowers are insect-, or bird-, or wind-pollinated (Bogle, 1970
; Endress, 1989a
; Li, 1997
).
Most of the traditional classification systems place the Hamamelidaceae in the "Lower" Hamamelidae, which includes Cercidiphyllaceae, Tetracentraceae, Trochodendraceae, Daphniphyllaceae, Platanaceae, Myrothamnaceae, and Eupteleaceae (Cronquist, 1981
; Takhtajan, 1997
). Endress (1977)
emphasized this family as a connecting taxon between the "Lower" and the "Higher" Hamamelidae (e.g., Betulaceae, Fagaceae, and Juglandaceae). Some members of the Hamamelidaceae have also been considered as linking taxa between the "lower" hamamelids and some basal elements of rosids and asterids (Hufford, 1992
; Chase et al., 1993
; Endress, 1993
; Morgan and Soltis, 1993
). A more comprehensive study (more taxa and more sources of data) is needed to further assess the systematic position of the Hamamelidaceae. Nevertheless, the Hamamelidaceae (including the Altingioideae) appears to be monophyletic based on both morphological (Hufford, 1992
) and DNA sequence data (Li, Bogle, and Klein, unpublished data).
The name Hamamelidaceae dates back to 1818 when Brown recognized it as a natural group with four genera, Hamamelis, Dicoryphe, Dahlia Thunb. (= Trichocladus Pers.), and Fothergilla. Since then, more than half a dozen classification systems have been proposed for the Hamamelidaceae (see review in Tong, 1930
; Bogle, 1968
; Chang, 1979
; Endress, 1989c
). However, the most comprehensive classification system for the Hamamelidaceae was put forward by Harms (1930)
. As shown in Table 1, based on morphological and anatomical characteristics, Harms recognized five subfamilies, the largest of which, the Hamamelidoideae, was further divided into five tribes. However, he did not classify the two then little-known genera Mytilaria Lecomte and Ostrearia. Schulze-Menz (1964)
transferred Sinowilsonia from the tribe Distylieae into the Corylopsideae, which had included Corylopsis and Fortunearia. Chang (1973
, 1979)
erected a new subfamily Mytilarioideae for Mytilaria and Chunia Chang.
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reviewed the previous classification systems, especially those of Harms and Chang, for the Hamamelidaceae, and recognized four subfamilies: Altingioideae, Exbucklandioideae, Rhodoleioideae, and Hamamelidoideae (Table 1). The Exbucklandioideae are a combination of the Exbucklandioideae Harms, Disanthoideae Harms, and the Mytilarioideae Chang. For the largest subfamily Hamamelidoideae, Endress (1989b
, c)
united the tribes Fothergilleae sensu Harms and Distylieae sensu Harms, forming the tribe Fothergilleae sensu Endress. Another major revision in Endress's system is that Fortunearia and Sinowilsonia were grouped with Eustigma Gardn. et Champ., thus establishing a more inclusive Eustigmateae. Furthermore, Endress (1989c)
treated the five Southern Hemisphere genera (Dicoryphe, Neostrearia, Noahdendron, Ostrearia, Trichocladus) as one of the three subtribes in the tribe Hamamelideae. As can be seen from the comparison of the major classification systems, fundamental questions concerning the systematics of the Hamamelidaceae still remain. That is, are the subfamilies, tribes, and subtribes monophyletic? In other words, do the classification systems reflect natural relationships in the Hamamelidaceae?
Nucleotide sequences of a chloroplast gene, rbcL, have been extensively used to examine plant phylogenies at higher taxonomic levels (Chase et al., 1993
; Qiu et al., 1998
). However, to resolve phylogenetic relationships among closely related genera, a fast-evolving DNA fragment, the nrDNA ITS region, has proven to be more useful (Baldwin, 1992
; Baldwin et al., 1995
; Bogler and Simpson, 1996
; Downie and Katz-Downie, 1996
; Kron and King, 1996
; Schilling and Panero, 1996
; Soltis, Johnson, and Looney, 1996
). A phylogenetic analysis of the Hamamelidaceae using nrDNA ITS data has shown that this region is informative in resolving subfamilial and tribal relationships (Shi et al., 1998
). However, more than half of the recognized genera were missing in Shi et al.'s data set, and a study with a much broader sampling is needed to address the intergeneric relationships in the Hamamelidaceae.
Therefore, the objectives of this study were as follows: (1) to reconstruct phylogenetic relationships of the Hamamelidaceae using ITS sequence data, and (2) to evaluate previous classification systems of the family in terms of the monophyly of the subfamilies, tribes, and subtribes of the Hamamelidaceae.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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. Polymerase chain reactionTM (PCR) was conducted in 0.2-mL thin-walled microcentrifuge tubes following the procedures described in Li et al. (1997)
and Li, Bogle, and Klein (1998)
. The PCR primers were universal ITS4 and ITS5 of White et al. (1990)
.
The PCR products were purified following Li et al. (1997)
. The resulting PCR product was used directly as a sequencing template. Sequencing reactions were carried out using Cycle Sequencing Kits and following the manufacturer's protocols (Applied Biosystems, Foster City, California).
The sequencing primers were ITS2, ITS3, ITS4 and ITS5 of White et al. (1990)
. The cycle sequencing products were then separated on 6% polyacrylamide gel using an Automated Sequencer 373A (Applied Biosystems, Foster City, California) in the Sequencing Facility Center of the University of New Hampshire (UNH).
For Liquidambar, Tetrathyrium, and Maingaya, 0.8% DMSO (dimethylsulfoxide) was added to both the PCR and cycle sequencing reactions.
The chromatograms were analyzed using the SEQED program (Applied Biosystems, Foster City, California). Also, in order to assure correct base-calling, we overlapped sequences generated from adjacent primers of either the same or opposite directions. The boundaries of ITS-1 and ITS-2 were determined by comparing sequences of the 3' 18S and 5.8S and the 5' end of the 26S ribosomal genes of Canella winterana (GenBank accession number GBAN-L03844; the prefix GBAN- has been added for linking online version of American Journal of Botany to GenBank but is not part of the actual accession number).
Sequence alignment
The ITS sequences within a genus and among closely related genera were easily aligned by sight. However, ITS sequences among genera of different subfamilies were not readily alignable, thus resulting in some ambiguous regions. These ambiguous sites, as identified by alignability by eye, can be eliminated from the data matrix before a phylogenetic analysis is conducted (Downie and Katz-Downie, 1996
). This "culled" method tends to create clades where internal relationships are not well resolved (Wheeler, Gatesy, and Desalle, 1995
; Soltis, Johnson, and Looney, 1996
).
Another way of dealing with alignments with ambiguous sites is to select a so-called optimal alignment. This approach involves consistency indices of the aligned sequences and the phylogenetic trees produced based on the data. Bogler and Simpson (1996)
used this "optimality" method to analyze the phylogenetic relationships of the Agavaceae. Many indices can be used to assess the optimality of sequence alignment, including the number of trees generated, the Consistency Index (CI), Retention Index (RI), and Rescaled Consistency Index (RC). Bogler and Simpson (1996)
, however, implied that the higher the RC was, the better the alignment. This seems to be reasonable because the RC index excludes characters that do little to the "fit" of the tree but inflate the CI (Wiley et al., 1991
).
In this study, the optimality method was employed to generate a data matrix of the ITS sequences of the Hamamelidaceae. The alignment that created trees with the highest RC index was considered as optimal for both ITS-1 and ITS-2. Individual alignments were conducted using the CLUSTAL option of the MEGALIGN program of DNA* software package (DNA* Inc., Madison, Wisconsin).
Phylogenetic analysis
The resulting data matrices from the optimality alignments were imported into the beta-test version of PAUP* 4.0d62 computer program for phylogenetic analyses, written by David L. Swofford (1997) at the Smithsonian Institution, with permission.
Indels were treated as missing data because this coding strategy retains information about substitutions that occur in other taxa in the indel region. However, it does not convey the information regarding the evolutionary event involved in the insertion or deletion (Platnick, Griswold, and Coddington, 1991
; Wojciechowski et al., 1993
). Thus, a parsimony analysis was also conducted treating gaps as the fifth character state.
All characters and their states were equally weighted in the parsimony analyses. Sequence divergence was analyzed using the pairwise difference obtained from PAUP*. Due to the size of the data set and the limitation of computer memory, the heuristic search option was used to find the shortest trees with TBR (Tree Bisection and Reconnection) branch swapping, MULPARS on, and STEEPEST DESCENT off.
It became impossible to produce reasonable sequence alignments when we tried to use taxa outside the Hamamelidaceae as outgroups. Therefore, in the parsimony analysis, Altingia and Liquidambar were used as outgroups because: (1) phylogenetic analyses using ITS data (Shi et al., 1998
) and evidence from morphology and matK gene sequences (Li, 1997
) have revealed that these two genera form a clade sister to the clade containing the rest of the Hamamelidaceae, and (2) the fossil record has shown that these genera are the most ancient members in the Hamamelidaceae (Zhang and Lu, 1995
). As a result, we focus our analysis and discussion on the Hamamelidaceae s.s. (Hamamelidaceae minus Altingioideae).
Both bootstrap and decay analyses were conducted using the PAUP* program to test the relative strength of putative clades (Felsenstein, 1985
; Bremer, 1988
; Donoghue et al., 1992
).
MacClade 3.03 (Maddison and Maddison, 1992
) was used to trace unambiguous changes along branches and to compare competing hypotheses concerning the relationships.
Both the skewness test (Huelsenbeck, 1991
) and the permutation test (Faith and Cranston, 1991
) were conducted to evaluate the phylogenetic information contained in the ITS data matrix. The skewness test was implemented using the Random tree option of PAUP*, and 10 000 random trees were examined. The permutation test, as used in Plunkett, Soltis, and Soltis (1997)
, was performed using the Permutation option of PAUP* with 100 replicates and heuristic searches.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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60% of the indels were a single base in length. There were three indels of ten or more bases in the ITS region: two indels (12 and 26 bases) were in ITS-1, and one (ten bases) in ITS-2. Pairwise sequence divergence in ITS-1 was generally higher than that in ITS-2, with averages of 18.5 and 16.6%, respectively. Pairwise divergence between the two genera of Altingioideae and the Hamamelidaceae s.s. was 30% for both spacers (Table 5).
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In the Trichocladus clade, four branches were recognized: Dicoryphe, Trichocladus, the Eustigmateae sensu Endress (1989b)
Plus Molinadendron, and the three Australian genera. Among the three Australian genera, Neostrearia was basally sister to the latter two genera. In the clade of the Eustigmateae sensu Endress (1989b)
plus Molinadendron, Molinadendron and Sinowilsonia were bound with a bootstrap value of 77% and a decay index of three steps (Fig. 1).
The Hamamelis clade was essentially the Fothergilleae sensu Endress (1989c)
, plus Hamamelis. There were four clades whose relationships were not well resolved in the phylogeny, including Hamamelis, Fothergilla, Parrotiopsis, and the well-supported Distylium group consisting of Distylium, Distyliopsis, Parrotia, Shaniodendron, and Sycopsis (Fig. 1).
The phylogenetic analysis with gaps as the fifth character state generated 46 shortest trees of 1266 steps with a consistency index of 0.6. The tree topology was the same as the phylogeny in Fig. 1. with several exceptions (Fig. 2). In the Trichocladus clade, Trichocladus was the basal taxon, followed by Dicoryphe, the paraphyletic Australian genera, and the monophyletic Eustigmateae sensu Endress (plus Molinadendron). In the Hamamelis clade, the clade of Hamamelis species was sister to the Fothergilleae sensu Endress (minus Matudaea and Molinadendron), in which Fothergilla was the basal taxon.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Downie and Katz-Downie, 1996
; Padgett, 1997
). The length of the two spacers in the Hamamelidaceae fell within these ranges, but ITS-1 sequences in most of the species sampled were in the high end of the range, except for the four genera (Eustigma, Fortunearia, Molinadendron, and Sinowilsonia) that shared two unique deletions (12 and 26 bp). The ITS-2 in the Hamamelidaceae was relatively less variable in length, mostly in the range of 224–249 bp, which agrees with a generalization that ITS-2 is more conservative than ITS-1 (Hershkovitz and Lewis, 1996
; Liston et al., 1996
).
A permutation test for the data set from the optimality alignment resulted in a probability of 0.01, indicating that the ITS data contain significant phylogenetic signal (Faith and Cranston, 1991
). This is consistent with the skewness of tree length distribution (Table 4).
Polyphyletic Exbucklandioideae sensu Endress
The Exbucklandioideae sensu Endress (1989c)
includes four genera, Chunia, Disanthus, Exbucklandia, and Mytilaria. The morphological synapomorphies of this subfamily include large, persistent stipules, palmate venation, and 4–6 ovules per carpel. However, the phylogenetic analysis based on the ITS DNA sequences provided a different picture of this taxon (Chunia was not available for this study). Exbucklandia and Mytilaria were grouped with Rhodoleia, while Disanthus formed its own clade (Fig. 1). This indicates that the Exbucklandioideae sensu Endress (1989c)
is polyphyletic. Furthermore, when the three genera (Disanthus, Exbucklandia, and Mytilaria) were forced into a monophylectic group, 35 more steps were required.
Mytilaria, Exbucklandia, and Rhodoleia have been previously recognized as subfamilies Mytilarioideae, Exbucklandioideae, and Rhodoleioideae, respectively (Harms, 1930
; Chang, 1948
, 1973
, 1979
; Tahktajan, 1997
). In the ITS phylogeny, Mytilaria was allied with the clade of Exbucklandia and Rhodoleia, suggesting a close relationship among the three genera. Exbucklandia and Rhodoleia also shared 32 unambiguous base substitutions (Fig. 1). Interestingly, this pattern agrees with an earlier taxonomic treatment (Reinsch, 1889
) and a rbcL phylogeny (Chase et al., 1993
; Qiu et al., 1998
). Nevertheless, these three genera differ greatly in morphology. Mytilaria and Exbucklandia share palmate venation (vs. pinnate venation in Rhodoleia), but differ in nodal anatomy (multilacunar vs. trilacunar; Bogle, 1990
), inflorescence type (spadix vs. head), and chromosome base number (x = 13 vs. x = 8; Pan and Yang, 1994
). Rhodoleia is distinct from Mytilaria and Exbucklandia in a suite of characters, including bird-pollinated, asymmetric flowers, and a chromosome base number of x = 12. In the ITS region, these three genera diverged greatly from their common ancestor (Table 5, Fig. 1). It therefore seems reasonable to continue to treat them as belonging to individual subfamilies (Harms, 1930
; Chang, 1973
, 1979
; Bogle, 1989
; Endress, 1989b
, c
).
Disanthus was the immediate sister taxon to the Hamamelidoideae in the phylogenetic tree (Fig. 1), reminiscent of the conclusions from previous morphological analyses (Hufford and Crane, 1989
; Pan, Lu, and Wen, 1991
). The intermediate systematic position of Disanthus between the Exbucklandia-Rhodoleia-Mytilaria clade and the Hamamelidoideae in the ITS-based tree does not provide evidence for the hypothesis that this genus is most primitive in the Hamamelidaceae, as has been suggested by some authors (Reinsch, 1889
; Harms, 1930
; Tong, 1930
; Cronquist, 1981
; Pan, Lu, and Wen, 1991
; Takhtajan, 1997
).
In the previous nrDNA ITS phylogeny (Shi et al., 1998
), Exbucklandia is sister to the Hamamelidoideae, whereas Disanthus and Rhodoleia form a clade. This result does not agree with morphological analysis (Hufford and Crane, 1989
), or the ITS analysis of this study, or the chloroplast gene phylogenies (rbcL—Chase et al., 1993
; matK—Li, 1997
; trn noncoding regions—Li et al., unpublished data). The difference is probably due to long-branch attractions resulting from the absence of Mytilaria or from the use of Corylus (Betulaceae, higher Hamamelidae) as the outgroup in Shi et al.'s analysis. In addition, we found DNA sequence differences for the same species sampled in both this study and Shi et al.'s (1998)
.
Monophyly of the Hamamelidoideae
It has been widely recognized that the Hamamelidoideae is a monophyletic group, characterized by a ballistic seed dispersal mechanism and one mature seed per carpel (Bogle, 1968
; Endress, 1989a
, b
, c
; Hufford and Crane, 1989
). The present analysis adds strong evidence to this hypothesis because the clade of this subfamily received a 100% bootstrap value and a decay index of more than five steps, and was further supported by 36 unambiguous base substitutions (Fig. 1). This result is consistent with the previous ITS phylogeny (Shi et al., 1998
).
The intergeneric relationships within the Hamamelidoideae, however, have been contentious (Harms, 1930
; Schulze-Menz, 1964
; Endress, 1989b
, c
). The relationships among the five tribes recognized by Harms (1930)
and more recently revised by Endress (1989c)
and others are discussed below.
Corylopsideae
The concept of the tribe Corylopsideae has been revised several times in the past several decades. Harms (1930)
delimited Corylopsideae as including Corylopsis and Fortunearia based on their similarity of leaf morphology, while Schulze-Menz (1964)
added Sinowilsonia to this tribe considering similar floral structures of the latter to Fortunearia. However, Endress (1989b
, c)
considered Corylopsideae as containing a single genus, Corylopsis, characterized by the orbicular petal.
In the ITS-based phylogenies (Figs. 1, 2), the three species of Corylopsis sampled formed a well-supported clade and were sister to the branch comprising Loropetalum, Tetrathyrium, Maingaya, and Matudaea, whereas Fortunearia and Sinowilsonia were phylogenetically distant from Corylopsis. Therefore, Corylopsis is not closely related to either Fortunearia or Sinowilsonia, as has already been shown in previous ITS analyses (Li, Bogle, and Klein, 1998
; Shi et al., 1998
). Floral ontogeny and embryological study also support the separation of Corylopsis from Fortunearia and Sinowilsonia (Li and Bogle, 1998
).
Hamamelideae
In Harms's system (1930)
, all of the genera in the Hamamelidoideae that have strap-shaped petals were placed in the tribe Hamamelideae and no further subdivisions were proposed. Endress (1989c)
, however, recognized three subtribes in the Hamamelideae, including the Hamamelidinae, Loropetalinae, and the Dicoryphinae. The Hamamelidinae contained a single genus, Hamamelis, characterized by the four-merous flower; the Dicoryphinae included the five Southern Hemisphere genera (Dicoryphe, Trichocladus, Ostrearia, Neostrearia, and Noahdendron) and was defined by the distinct anther dehiscence pattern; the Loropetalinae contained the remaining four genera, Loropetalum, Embolanthera, Maingaya, and Tetrathyrium.
The analysis of the ITS data placed the genera of the Hamamelideae into three different clades (Fig. 1), suggesting that the tribe is polyphyletic (as shown by Shi et al., 1998
). Maingaya, Tetrathyrium, and Embolanthera have been suggested to be the ancestral stock of the Australian hamamelids (Raven and Axelrod, 1974
). However, this study does not support that proposition because in the phylogeny (Fig. 1) the monophyletic Australian genera were distant from the lineage containing Maingaya and Tetrathyrium (Embolanthera not available for this study). The exclusive Southern Hemisphere distribution and the unique pattern of anther dehiscence suggest a close relationship of the three Australian and two African genera (Endress, 1989a
, b
, c
). However, in the strict consensus trees (Figs. 1, 2), the relationships of the Australian and African genera were not well resolved, even though these genera formed a clade in the 50% majority consensus tree (tree not shown). More evidence is needed to resolve relationships of the Southern Hemisphere genera and thus to elucidate their biogeography.
Eustigmateae
The delimitation of the Eustigmateae has expanded from monogeneric (Harms, 1930
) to trigeneric (Endress, 1989c
). Eustigma is distinct in its small, auriculate petals and greatly enlarged stigmatic surfaces (Harms, 1930
). The similarities of Eustigma with Fortunearia in other morphological characters such as pedicellate, lenticellate fruits, and covering sepals led Endress (1989c)
to the conclusion that Eustigmateae should include Fortunearia and Sinowilsonia.
The ITS-based tree (Fig. 1) offers strong support for Endress's hypothesis and further corroborates the implication (Endress, 1967
) that Molinadendron and Sinowilsonia are closely related. Interestingly, these four genera shared nine unambiguous base substitutions (Fig. 1) and two unique deletions totaling 38 bp (Li, Bogle, and Klein, 1998
).
Combining the Distylieae and Fothergilleae
In the phylogeny (Fig. 1), the clade of two Hamamelis species was sister to a branch containing the Distylieae (Distylium, Distyliopsis, and Sycopsis) and Fothergilleae sensu Harms (1930)
(Fothergilla, Parrotia, and Parrotiopsis). Neither the Distylieae nor the Fothergilleae formed a monophyletic clade. Instead, a close but unresolved relationship was shown among Sycopsis, Parrotia, and Shaniodendron. This result agrees with the finding that Sycopsis and Parrotia are interfertile, giving rise to the hybrid taxon, Sycoparrotia (Endress and Anliker, 1968
). Thus, the Fothergilleae sensu Endress (1989c)
, a merger of Distylieae Harms and Fothergilleae Harms, is supported.
Fothergilla and Parrotiopsis each formed their own clades in the ITS phylogeny (Fig. 1). This is consistent with the showy specialized structures they have evolved for insect pollination: long, white, clavate stamen filaments in Fothergilla and large, white subfloral bracts in Parrotiopsis (Bogle, 1970
; Endress, 1989a
). These specializations do not occur in any other members of the Fothergilleae sensu Endress (1989c)
or in the Hamamelidaceae.
The apetalous genera of the Hamamelidoideae have long been considered as monophyletic (Harms, 1930
; Endress, 1989c
), but the ITS phylogeny (Fig. 1) suggested that loss of petals in this subfamily has evolved at least three times independently: Matudaea in the Corylopsis clade, Molinadendron in the Trichocladus clade, and the Fothergilleae in the Hamamelis clade. Therefore, the apetalous genera do not belong to a single monophyletic group, and apetaly is homoplasious in this subfamily.
It is a novel relationship that Hamamelis was grouped with Fothergilleae sensu Endress (excl. Matudaea and Molinadendron). Interestingly, this pattern finds support from leaf venation (Harms, 1930
; Chang, 1979
; Li and Hickey, 1988
). The systematic position of Hamamelis was not resolved in the ITS phylogeny using gaps as missing data (Fig. 1); however, in the phylogenetic tree using gaps as the fifth character state (Fig. 2), the clade of the two Hamamelis species was sister to the Fothergilleae sensu Endress. Also, Hamamelis differs greatly from the Fothergilleae in a group of floral characters, including showy, strap-shaped petals, bisexuality, and nectariferous phyllomes (Endress, 1989a
). Therefore, Hamamelis should be isolated from the Fothergilleae in taxonomic treatments.
The evolutionary relationships shown in the phylogenetic trees (Figs. 1, 2) have significant implications for character evolution and biogeography. For example, apetaly and wind-pollination have evolved independently more than three times in the Hamamelidaceae. The American Matudaea (Central and South America) and Molinadendron (Central America) were suggested to be closely related to Asian Maingaya and Sinowilsonia, respectively. The Southern Hemisphere genera were shown to be a potentially monophyletic group by the 50% majority consensus tree. However, we believe that a well-resolved phylogeny based on multiple sources of data and detailed studies of the fossil record are needed to reveal a complete picture of character evolution and biogeography of the Hamamelidaceae.
In conclusion, at the subfamily level, this study recognized the monophyly of the Exbucklandioideae Harms, Mytilarioideae Harms, Rhodoleioideae Harms, Disanthoideae Harms, and the Hamamelidoideae. Furthermore, it suggested close relationships of Exbucklandia, Rhodoleia, and Mytilaria and the paraphyly of Exbucklandioideae sensu Endress (1989c)
. At the tribal and subtribal levels, the monophyletic groups were the corylopsideae sensu Endress (1989c)
; Eustigmateae sensu Endress (1989c)
, but expanded to include Molinadendron; Fothergilleae sensu Endress (1989c)
, expanded to include Hamamelis; Dicoryphinae; and Loropetalinae, expanded to include Matudaea. The Hamamelideae, however, were polyphyletic. The ITS phylogeny also revealed that some morphological characteristics commonly used to classify the Hamamelidoideae have evolved several times independently. These characteristics included strap-shaped petals, apetaly, and wind pollination. Thus homoplasy needs to be taken into account in future classifications of the Hamamelidaceae so that natural relationships can be reflected.
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FOOTNOTES |
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This is a portion of the doctoral thesis of the first author presented to the Graduate School of the University of New Hampshire, Durham. 
5 Author for correspondence, current address: Arnold Arboretum of Harvard University, 125 Arborway, Jamaica Plain, MA 02130.
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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