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Systematics |
Department of Systematic Botany, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18D, SE-752 36 Uppsala, Sweden
Received for publication January 30, 2001. Accepted for publication May 22, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: 18S • Asterids • atpB • Cardiopteridaceae • DNA sequence data • Icacinaceae • morphology • ndhF • Pennantiaceae • phylogeny • rbcL • Stemonuraceae
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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54 genera. They comprise trees up to 40 m high, shrubs (sometimes scrambling), and lianas. Among these is one of the world's rarest species (Pennantia baylisiana, with only a single wild individual; e.g., Baylis, 1977
; Murray and de Lange, 1995
). In this family, there are also several commercially important timber trees (e.g., in Apodytes and Cantleya) and some ornamentals (Citronella, Pennantia). Many genera produce edible fruits and some are cultivated to obtain products such as starch (from the seeds and large fleshy tubers of Casimirella), oil (from the fruits of Poraqueiba), or maté (the leaves of Citronella may be used as a substitute for those of Ilex; Howard, 1942c
, and references therein).
Icacinaceae are badly in need of revision. The family as described in the works of Howard (1940, 1942a, b, c, d, 1943a, b, c, 1992)
and Sleumer (1942, 1969, 1971)
is clearly not a monophyletic unit. Molecular studies show convincingly that the family must be divided into at least two groups (Savolainen et al., 2000a, b
; Soltis et al., 2000
). In retrospect, this is hardly surprising. None of the characters used to define Icacinaceae was present in Icacinaceae alone, nor were the diagnostic characters rare among the angiosperms as a whole. In the following, I will use the name Icacinaceae sensu lato (s.l.) when referring to Icacinaceae as circumscribed by Sleumer and Howard (references cited above). Icacinaceae sensu stricto (s.s.) will be used when referring to a more restricted entity including genera related to Icacina.
This study, including both molecular and morphological data, deals with (a) where in the angiosperm system the members of Icacinaceae s.s. belong; (b) where the "orphan taxa" not related to Icacina belong; whether they will be placed in existing families and orders or arranged in new taxa; and (c) the support for the taxa under (a) and (b) as indicated by jackknife values from the present data as well as by general agreement of morphological characters.
To be able to place the members of Icacinaceae s.l. in the angiosperm phylogeny, a data matrix of DNA sequences with 129 taxa representing all major groups of angiosperms was compiled. The main focus is on the chloroplast gene ndhF, but for taxa with available rbcL, atpB, and 18S rDNA sequences, these were also included as a means of increasing support for the resulting phylogeny. The ndhF sequences were analyzed both separately and in combination with the other genes. Icacinaceae s.l. are represented by 26 ndhF sequences (25 of these obtained for this study), eight rbcL sequences, four sequences from the atpB, and three from the 18S rDNA gene. The sequenced taxa include members from all four tribes of Engler (1893)
and Sleumer (1942)
and from all main areas of the distribution (Africa, Asia, Australasia, and Central and South America). For some widespread genera, sequences from different parts of their distribution were included. Furthermore, morphology of the Icacinaceae s.l. (see MATERIALS AND METHODS) was studied and analyzed in combination with the sequence data in order to explore morphological support for those clades that include "icacinaceous taxa."
Icacinaceae were first recognized as a family by Miers (1851)
. He realized that their relationships were not with Olacaceae, as had been suggested by De Candolle (1824)
and was later accepted by Bentham (1841, 1862)
, who had placed them in a tribe Icacineae in his family Olacineae. Instead, Miers (1852, 1864)
argued for affinities with Celastraceae and Aquifoliaceae. The characters Miers (1852)
emphasized when discriminating Icacinaceae from Olacaceae include, among others, their commonly polygamous flowers with alternipetalous stamens and ovaries with generally two pendulous ovules in each locule.
Many subsequent authors (e.g., Baillon, 1862–63a, b, 1872, 1874
; Cronquist, 1981
) have followed Miers in placing Icacinaceae in Celastrales. Sleumer (1942)
considered both "Icacinineae" and "Celastrineae" to be in Sapindales. Following Reveal (1993)
, Takhtajan (1997)
chose Icacinaceae as the type family for the order Icacinales. Icacinales sensu Takhtajan included both Icacinaceae and Aquifoliaceae together with Phellinaceae and Sphenostemonaceae, and they were placed under the superorder Celastranae. However, Phellinaceae are a member of Asterales (e.g., Kårehed et al., 1999
) and Sphenostemonaceae might belong in Dipsacales (Savolainen et al., 2000b
).
Until recently, Icacinaceae have always been regarded as a rosid taxon, partly due to the misinterpretation of the affinities of Aquifoliaceae. In the APG system (APG, 1998
), based on several molecular studies, Aquifoliaceae are asterids, while Celastraceae are still placed among the rosids. Icacinaceae are unassigned to order, but listed under euasterids II. Characters supporting Icacinaceae as asterids are, for example, their unitegmic ovules, the presence of iridoids (Nandi, Chase, and Endress, 1998
), and their wood anatomy (Baas, Wheeler, and Chase, 2000
). Curiously, lepidopteran caterpillars feeding on various asterids also recognize Icacinaceae as asterids (Spichiger, Vuattoux, and Savolainen, 1997
).
The large-scale studies by Savolainen et al. (2000a, b)
and Soltis et al. (2000)
indicate that Icacinaceae should be subdivided. Icacina and related genera form a monophyletic group with a rather uncertain position among the euasterids; in the most parsimonious tree of Savolainen et al. (2000b)
it is even sister taxon to Aphloia, a rosid. Other genera group with Cardiopteridaceae and, together with that family, constitute the sister group of Aquifoliales.
Traditionally, Icacinaceae have been divided into various infrafamilial taxa, the most widely accepted were the tribes used by Engler (1893)
and Sleumer (1942)
: Icacineae (including the majority of the genera), Iodeae (Iodes, Hosiea, Mappianthus, Natsiatopsis, Natsiatum, and Polyporandra), Sarcostigmateae (Sarcostigma), and Phytocreneae (Chlamydocarya, Miquelia, Phytocrene, Polycephalium, Pyrenacantha, and Stachyanthus). The first two do not constitute natural groups. The characters used to define them do not hold; various sources of data (e.g., nodal and wood anatomy [Bailey and Howard, 1941a, b, c, d
] and palynological data [Dahl, 1952
; Lobreau, 1969
; Lobreau-Callen, 1972, 1973, 1980
]) show no clear distinction between the two taxa and they are consequently inseparable. The monogeneric Sarcostigmateae differ from the other tribes in lacking endosperm and having thick, fleshy cotyledons. Phytocreneae contain genera with long embryos and thin, broad cotyledons and may be a natural entity. All four tribes have been recognized as separate families, as have the genera Emmotum, Leptaulus, Pleurisanthes (Bennett and Brown, 1852
; van Tieghem, 1897
), and Pennantia (Agardh, 1858
). Their relationships with the rest of Icacinaceae have, however, not been questioned.
Metteniusa, on the other hand, has, since it was described in Florae Colombiae (Flora of Colombia; Karsten, 1860
), variously been included in Icacinaceae as a rather aberrant member (e.g., Sleumer, 1942
; Cronquist, 1981
) or regarded as a distinct family, possibly related to Alangiaceae (Willis, 1966
), Boraginaceae, or Convolvulaceae (Karsten, 1860
). Takhtajan (1997)
treated Metteniusa as the sole member of the order Metteniusales in the superorder Celastranae (Rosidae), together with his Icacinales and five other orders.
Other genera with suggested affinities to the Icacinaceae include Cardiopteris and Lophopyxis. They were both included in Icacinaceae as separate subfamilies by Engler (1893)
, but have mostly been regarded as families of their own. Lophopyxis most likely has no affinities with the Icacinaceae; Savolainen et al. (2000b)
suggest a placement in Malpighiales. Several molecular studies (Savolainen et al., 2000a, b
; Soltis et al., 2000
) show not a relation of Cardiopteris to all Icacinaceae but close affinities between certain members of the Icacinaceae s.l. and Cardiopteridaceae (see DISCUSSION). According to Savolainen et al. (2000b)
, the genus Pentaphylax is also allied to Cardiopteridaceae. That relationship is probably an artefact of their analysis (the 642-base-pair-long rbcL sequence belongs to an orchid; a BLAST search of GenBank retrieves only orchids as related sequences). Neither Lophopyxis nor Pentaphylax is further dealt with in this study, since there is presently no available data supporting a relationship to Icacinaceae.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) were included. Some taxa are represented by only a single sequence (e.g., Poales by Zea mays), while others are more densely sampled (some genera, such as Pennantia, are represented by more than one sequence).
The data matrix was initially aligned with Clustal X (Thompson et al., 1997
) and subsequently modified manually, taking the reading frame of the corresponding amino acid sequence into consideration. A total of 72 insertion/deletion events were included in the aligned matrix, 36 of which are potentially phylogenetically informative (information on alignment gaps has been archived on the American Journal of Botany Supplementary Data web site). The latter were coded as absent or present and included in the matrix as additional characters. In the analyses, nucleotide positions corresponding to positions 1–2110 of the unaligned sequence of Nicotiana tabacum were used.
Available sequences from the rbcL, atpB, and 18S rDNA genes for the same taxa were added to the ndhF matrix (sequences from the latter two genes are mainly from Soltis et al., 2000
, and their alignment is adopted). If different species had been sequenced for different genes, the congeneric sequences were pooled in the combined matrix. Those taxa with ndhF sequences only were coded with "missing data" in the positions corresponding to the other genes. Four Icacinaceae not sequenced for ndhF were added to the combined molecular matrix and, likewise, coded with missing data in the part of the combined matrix corresponding to the positions for the ndhF gene. The molecular data matrices are available from the author upon request.
Sequencing
DNA was extracted from dried material according to the protocol given by Oxelman, Backlund, and Bremer (1999)
. Their protocols for polymerase chain reactions (PCR) and sequencing reactions were also followed. The primers used in these reactions are described in Oxelman, Backlund, and Bremer (1999
; their primers 1, 1201, 1350R, 1427, 1947R, and +209R) and Kornhall, Heidari, and Bremer (in press; their primers 40, 1018R, and 2065R).
Morphological data
Fresh and herbarium material of 45 out of 54 genera of Icacinaceae s.l. were studied (voucher information has been archived on the American Journal of Botany Supplementary Data web site). These studies and an extensive literature survey resulted in a morphological data matrix (archived on the American Journal of Botany Supplementary Data web site) with 71 potentially phylogenetically informative characters from, for example, gross morphology, leaf and wood anatomy, and palynology (Table 1). Genera were used as terminal taxa, since most genera have few species and most of the variation is between genera. Naturally, using genera as terminal taxa leads to more polymorphisms than using exemplars. However, if I were to code, for example, only type species or those species available as herbarium material, more cells in the data matrix would have been coded with "missing data" because the species described in the literature regarding pollen, for example, often are other species than these; the resulting matrix would have been less informative and possibly misleading.
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), but they have not been merged. There are differences between the two taxa, which some authors (Lobreau-Callen, 1972, 1973
; van Staveren and Baas, 1973
) regard as distinct enough to keep them separated. In the morphological analysis, both Iodes and Mappianthus are included in order to investigate their supposed congenerity. Metteniusa is included in the morphological data matrix, even though it might not be related to the rest of the genera (see above). If Metteniusa, once sequenced, will show icacinaceous affinities, the morphologically based conclusions of its relationships will be valid; otherwise, they must be disregarded. Several attempts to amplify DNA from both leaves and flowers of the available Metteniusa material failed. Because Cardiopteris most likely is related to part of Icacinaceae s.l., it was also coded for the morphological characters.
The morphological data were first analyzed separately to investigate if groups within the Icacinaceae s.l. can be defined by morphological apomorphies alone. A subsequent "total evidence" analysis (the morphological data combined with the molecular data from the four genes; see, e.g., Kluge, 1998
) was performed to obtain a phylogeny to be used for exploring morphological support for groups including members of Icacinaceae s.l. In the total evidence analysis, those 28 taxa lacking sequence data were excluded.
Cladistic analysis
The ndhF, the combined molecular (ndhF, rbcL, atpB, and 18S rDNA), the morphological, and the total evidence (molecular and morphological data) matrices were analyzed with PAUP* (Swofford, 2000
). For each matrix a heuristic search with 1000 random addition sequence replicates and TBR (tree bisection-reconnection) branch swapping was conducted with the MULTREES option off. For each replicate, the shortest tree was saved regardless of its length. These trees were submitted to a second round of TBR branch swapping with MULTREES on. All matrices were also analyzed using the Ratchet (500 iterations, holding two trees per iteration and sampling 10% of the characters; Nixon, 1999
) as implemented in the computer program WinClada (Nixon, 2000
). These analyses were run with NONA (Goloboff, 1993
). No shorter trees were found and the resulting consensus trees were identical to the strict consensus trees of the heuristic analyses. During all analyses, gaps were treated as missing data and polymorphisms as uncertainties. Jackknifing with a deletion frequency of 37% was performed 1000 times for each matrix. Each replicate included five random addition sequence replicates and TBR branch swapping. Congruence between the ndhF data and the data from the other three genes was tested by the ILD test (incongruence length difference; Farris et al., 1995
) as implemented in PAUP* (the partition-homogeneity test with heuristic search; 1000 replicates, five random addition sequence replicates per replicate, TBR branch swapping, and uninformative characters excluded; Lee, 2001
).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Six genera (eight sequences) of Icacinaceae s.l. and Cardiopteris form a strongly supported clade (a jackknife value [JK] of 99%; see Cardiopteridaceae sensu Savolainen et al. [2000b]
) with two well-supported subgroups (JK = 92 and 100%, respectively). I will refer to these subgroups as Cardiopteridaceae and Stemonuraceae. The entire clade is strongly supported (JK = 98%) as sister to Aquifoliales (JK = 100%), and together these groups are sister to the other euasterids II.
The only member of Icacinaceae s.l. that does not group with Icacinaceae s.s., Cardiopteridaceae, or Stemonuraceae is Pennantia. It has a well-supported position in Apiales (JK = 100%) and is sister to the rest of the order.
The combined molecular analysis
Two (Chlamydocarya and Sarcostigma) of the four icacinaceous taxa not included in the ndhF analysis group with Icacinaceae s.s. and Garryales, a third (Gonocaryum) groups with Cardiopteridaceae, and the fourth (Gomphandra) with Stemonuraceae. The positions and jackknife values of these groupings in the consensus of the most parsimonious trees are nearly identical to the ndhF analysis. Pennantia still has high support for its inclusion in Apiales. The missing data in the combined molecular data matrix, mainly due to the narrower sampling of icacinaceous taxa in the rbcL-atpB-18S rDNA-part of the matrix, do not seem to affect tree topology. If the taxa only represented by a single sequence are removed from the analysis, the resulting tree is slightly more unresolved, but all remaining taxa still group in the same orders, except for Icacinaceae s.s. which have an unresolved position basal in euasterids I.
The morphological and total evidence analyses
The morphological data analyzed alone reveal synapomorphies for certain groupings within Icacinaceae s.l. (Fig. 3). However, no groups of more than two taxa are well supported, as judged by jackknife values (bootstrap and Bremer support analyses, not reported here, were likewise unable to support larger groupings). When morphological data were analyzed together with the molecular data in the total evidence analysis, the overall topology remained the same as for the combined molecular analysis, but the strict consensus tree was more resolved for the groups under study (Figs. 1–2). To make further inferences about those genera with no sequence data, the morphological data were optimized on one of the most parsimonious trees of the morphological analysis, even though there are a few differences between the topology of this analysis and that of the total evidence analysis (Fig. 3).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Bremer, Bremer, and Thulin, 2000
) do form a monophyletic sister group to the well-supported remainder of euasterids I, as in the most parsimonious trees (Figs. 1–2), Garryales should be expanded to include also Icacinaceae s.s. On the other hand, if the well-supported subgroups that constitute the supposed Garryales s.l. instead form a grade basal to euasterids I, reclassifications at both family and order levels are necessary. The taxa of such a grade (apart from Garryales s.s. and a taxon Icacinaceae s.s. comprising only the clade including Icacina) would not include any type species of current orders or families and might, moreover, be sister to more than one order, thereby necessitating the creation of new families and/or orders (cf. the recommendations for phylogenetic circumscriptions in Bremer, 2000
).
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; Aucuba, Garrya, Eucommia, and Oncotheca; note, however, that the analysis of Soltis et al. [2000]
does not support a position of Oncotheca within Garryales), what characters support such an expanded Garryales? Garryales in the expanded sense consist of woody genera, mainly trees or shrubs but also lianas. The leaves in Garryales s.s. differ from those of Icacinaceae s.s. in being opposite. There are, however, Icacinaceae with opposite leaves (Cassinopsis, Iodes, Mappianthus, and Polyporandra). Otherwise, the leaves of Garryales s.l. are simple and lack stipules, with a majority of the genera having penninerved leaves without hydathodes and serrations. Cyclocytic stomata dominate; most genera have only this kind, but sometimes they occur in combination with another kind. Notable exceptions are Apodytes and Eucommia, which have only anomocytic stomata, and Aucuba and Garrya, which have laterocytic stomata; the latter feature is not present in any of the icacinaceous genera. Among the genera of Icacinaceae s.s. pentamerous flowers predominate. In the morphological data matrix this is not so evident, since even the rare presence of flowers with a different number of floral parts were coded. The only genera that normally have lower merisms are Calatola, Chlamydocarya, Natsiatopsis (tetramerous), and Polycephalium (trimerous). Both Aucuba and Garrya have tetramerous flowers. Eucommia lacks perianth, but the number of stamens ranges from 4 to >12. Flowers of Garryales s.l. are generally small, with free, valvate petals (imbricate in Oncotheca). The inflexed apex of the petals, so common among Icacinaceae, is also present in Aucuba. All genera have isomerous (with the exception of Eucommia), alternipetalous, and free stamens. The anthers are generally introrse, but in Emmotum and five closely related genera (cf. Fig. 3), Garrya, and Oncotheca they might be latrorse or more or less extrorse.
Ovaries with one locule and two pendant ovules, only one of which generally matures, are present throughout the order. Aucuba is also one-locular, but has only one ovule. Emmotum and Oncotheca differ in being three- and five-locular, respectively. The ovules are anatropous and unitegmic; they are crassinucellate in Aucuba and Garrya, weakly so in Eucommia, and tenuinucellate in Oncotheca and Icacinaceae s.s. Garrya and Eucommia have two (to three) styles, while most other genera have only one. Casimirella, which most likely belongs in this order (cf. Fig. 3), rarely develops two or three styles. Oncotheca has five styles, each with three stigmas. The fruits of Icacinaceae s.s and Oncotheca are drupaceous, while those of Aucuba and Garrya are described as berries. Those of Eucommia are samaras.
Node anatomy, the vessel arrangement, and the type of perforations in the vessels have been used to group icacinaceous taxa (Bailey and Howard, 1941a, b, c, d
). These characters seem to fit rather well to describe the two subgroups of Garryales (in the consensus tree of Fig. 1). The first subgroup includes Aucuba, Garrya, Apodytes, Raphiostylis, Emmotum, Ottoschulzia, and most likely (according to the morphological analysis; Fig. 3) also Calatola, Oecopetalum, Platea, and Poraqueiba. This subgroup has trilacunar nodes, mainly solitary vessels, and scalariform perforation plates (for Garrya see Mosely and Beeks, 1955
). The other subgroup has unilacunar nodes, often aggregated vessels, and simple perforations. There is one exception to this pattern; Raphiostylis has the characters of the subgroup to which it does not belong. The pentalacunar nodes and scalariform perforations of Oncotheca suggest a placement in the first subgroup. Eucommia, with its unilacunar nodes and simple perforations (scalariform in vessels of the earliest secondary xylem), fits best in the second subgroup. Based on the morphological analysis, the position of Pittosporopsis is uncertain, but its petals overlap apically, much the same way as those of Garrya do.
As shown, many characters do support a monophyletic Garryales s.l., but there is also a great deal of variation among the included taxa. Further studies on the morphological support for Garryales and the basal relationships of euasterids I are needed. For the moment, I conclude that basal to euasterids I s.s. (Boraginaceae, Gentianales, Lamiales, and Solanales) are Garryales s.s. and at least four additional, well-supported taxa (cf. Fig. 1). These might be a monophyletic unit or they might constitute a grade basal to euasterids I s.s.
The "Icacina group" is the largest and most heterogeneous assemblage of genera. They include all the genera of the former tribes (Sleumer, 1942
) Iodeae, Sarcostigmateae, and Phytocreneae, together with several Icacineae. The total evidence analysis does not preclude monophyly of either Iodeae, Sarcostigmateae, or Phytocreneae. Morphology alone cannot support monophyly of each of these tribes, but with the inclusion of Rhyticaryum the three tribes are at least supported as a monophyletic unit, leaving a paraphyletic Icacineae behind (or polyphyletic considering that several former Icacineae are part of euasterids II). If Stachyanthus is excluded from Phytocreneae, the morphological analysis indicates that Phytocreneae form a group sharing characters such as verrucose or papillose interior of the endocarp and interxylary phloem. The results do not support the congenerity of Iodes and Mappianthus (Fig. 3; see Morphological data).
The two sequences of Cassinopsis, one African and one from Madagascar, have a weakly supported (JK < 50%) position as sister to the Icacina group (Fig. 1). Several morphological characters differ from those in the other taxa of Garryales s.l. In fact, the morphological analysis groups Cassinopsis with Cardiopteris (in euasterids II; see below), but in the light of molecular data, the characters supporting their relationship (e.g., imbricate petals, reticulate pollen) are evidently homoplastic.
A group of genera recognized on morphological grounds by Howard (1942b, c)
comprises Emmotum, Oecopetalum, Ottoschulzia, and Poraqueiba. They are all New World genera and share characters such as fleshy petals, broad connectives, fruit and seed type, and wood anatomical features (Bailey and Howard, 1941b
; Howard, 1942c
). My morphological analysis suggests an inclusion of Calatola and Platea in the "Emmotum group." They are similar to the other genera in having latrorse or more or less extrorse anthers. Calatola was regarded by Howard (1942c)
as anomalous in the family, especially due to its inflorescences. On the other hand, he noted similarities in the wood between Platea and Oecopetalum. The genus Emmotum was regarded as a separate family by van Tieghem (1897)
, mainly because of its three-locular ovaries. His Emmotaceae could be expanded to include also the other genera mentioned above, which were unknown to or not mentioned by him. (Note that Eucommia and Oncotheca, like some members of the "Emmotum group," have latrorse or extrorse anthers and prolonged connectives.)
The total evidence analysis finds a close relationship between Apodytes and Raphiostylis—the "Apodytes group." The morphological analysis fails to recognize this relationship, but the two genera have similar pollen. Based on her palynological studies, Lobreau-Callen (1973)
suggested Raphiostylis is derived from Apodytes.
Aquifoliales and Cardiopteridaceae
The circumscription of Aquifoliales and character evolution within that order will be dealt with in more detail in a forthcoming paper. In the following, I will mainly comment on those matters most relevant to the placement of icacinaceous taxa.
Savolainen et al. (2000b)
suggest an expansion of the monogeneric Cardiopteridaceae (Fig. 5) to include Pentaphylacaceae and at least the three former Icacinaceae genera Gomphandra, Gonocaryum, and Irvingbaileya. They do not place this expanded family, but according to Soltis et al. (2000)
, Gonocaryum and Irvingbaileya belong in Aquifoliales. My results confirm the placement of Cardiopteris together with several icacinaceous taxa in this order, but the inclusion of Pentaphylacaceae is in need of confirmation (see above).
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; Aquifoliaceae, Helwingiaceae, Phyllonomaceae) consisting of two well-supported monophyletic groups, Cardiopteridaceae (JK = 98%) and Stemonuraceae (JK = 100%). Cardiopteridaceae contain, besides Cardiopteris, (at least) Citronella, Gonocaryum, and Leptaulus and Stemonuraceae include Irvingbaileya among others (see next section). As suggested by Soltis et al. (2000)
, Aquifoliales should be more broadly circumscribed and include Cardiopteridaceae and Stemonuraceae. The expanded Aquifoliales have very high support (JK = 99%).
Cardiopteridaceae as understood here include Cardiopteris, Citronella, Gonocaryum, and Leptaulus. Miers (1864)
has already proposed that Citronella is more related to Aquifoliaceae than to Icacinaceae. Following the morphological analysis, Dendrobangia and Metteniusa might also belong here. Howard (1942c)
suggested Dendrobangia was related to Platea, mainly because of their shared presence of peltate-stellate hairs. Metteniusa groups together with Gonocaryum in the morphological analysis. They share characters such as comparatively large embryo, folded cotyledons, and furrowed endosperm. These characters are paralleled by some of the icacinaceous taxa of euasterids I. The inclusion of Metteniusa in Cardiopteridaceae is questionable, however. This conclusion is based on the assumption that the genus is indeed related to some icacinaceous genera. As initially mentioned, various authors have regarded Metteniusa as the sole member of either a separate family or an entire order (e.g., Takhtajan, 1997
). Characters unmatched in any Icacinaceae s.l. are moniliform anthers, with their free basal parts recurving, and uni-ovulate ovaries built up of only one carpel. The flowers are also much larger than the flowers of any other Icacinaceae s.l. (up to 4 cm long).
Cardiopteridaceae circumscribed as above are rather heterogeneous and hard to characterize. Apart from Citronella, the genera do, however, resemble one another in having sympetalous corollas with epipetalous stamens. Among Icacinaceae s.l. these characters are only found in this group and in Cassinopsis. The different genera of Cardiopteridaceae could be arranged in more easily recognizable taxa to be treated either at tribe, subfamily, or family level. Pending more data and considering the negative effect of creating redundant names, I hesitate to make any transfers here. However, two of the genera have been accepted as separate families in the past, Leptaulaceae (van Tieghem, 1897
) and Metteniusaceae (Karsten, 1860
).
Circumscription of Stemonuraceae–Stemonuraceae, stat. nov. 
Tribus Stemonureae M. Roem., Fam. Nat. Syn. Monogr. 1: 8 (1846). Type: Stemonurus Blume
Trees or shrubs. Leaves simple, alternate, entire, and penninerved, without stipules. Inflorescences axillary or terminal cymes or panicles, peduncles usually bracteate. Flowers bi- or unisexual, articulated with the pedicel. Calyx small, shortly and broadly (4–) 5 (–6)-lobed. Petals (4–) 5 (–7), free, sometimes united in Gomphandra, valvate, often keeled and with an inflexed apex, wanting in male flowers of Grisollea. Stamens isomerous, alternipetalous, filaments often short, flattened, dilated upwards, bearing "cylindrical," club-shaped hairs, sometimes with an adaxial appendage (Discophora, Lasianthera), rarely glabrous and/or filiform. Anthers ± ovate, introrse or extrorse (Grisollea), longitudinally dehiscent. Disc sometimes present, either slightly cup-shaped or as a unilateral, fleshy scale at the base of the ovary. Ovary cylindrical to conical, in male flowers abortive and sometimes immersed in a fleshy gibbosity or "disc," in female or bisexual flowers often with a fleshy unilateral appendage enlarging in fruit. Stigma sessile or on short style. Ovules two, anatropous, pendant from the apex of the locule. Fruit drupaceous, often laterally compressed, rarely fusiform, with mostly longitudinally ribbed endocarp. Seed one; embryo minute with copious endosperm. n = 22 (Stemonurus).
Included genera and number of species: Cantleya (1), Codiocarpus (2), Discophora (2), Gastrolepis (1), Gomphandra (>30), Grisollea (2), Hartleya (1), Irvingbaileya (1), Lasianthera (1), Medusanthera (4–5), Stemonurus (12), Whitmorea (1).
I prefer to recognize a family Stemonuraceae (JK = 100%; Figs. 2–3, 6–8) separate from Cardiopteridaceae, since Stemonuraceae are well-supported in the total evidence analysis and, in addition, by an array of morphological features. If Stemonuraceae were given a rank below family, I think that this well-characterized group would be hidden among the morphologically diverse Cardiopteridaceae. Recognizing both these groups under the name Cardiopteridaceae will create a very heterogeneous family with its type genus as the most aberrant member. While all other taxa are woody, Cardiopteris is a twining herb, with white milky juice and truly imbricate petals and samaras, characters not present in Stemonuraceae or any of the former Icacinaceae s.l. (Sleumer, 1942, 1971
). A Cardiopteridaceae with Stemonuraceae included would be a family well-supported by molecular characters, but a family difficult to describe and recognize. I argue against families with no easily recognized characters, that is, I submit to the "principle of ease of identification" (cf. Backlund and Bremer, 1998
). By creating a morphologically well-defined Stemonuraceae, the remaining Cardiopteridaceae are more easily recognized. Even though still rather heterogeneous, they do (except Citronella) share sympetalous corollas and epipetalous stamens. Also, segregating Stemonuraceae might be a more stable alternative. Since Stemonuraceae exhibit such easily recognized characters, probably no currently unplaced taxa will belong in the family; a species with these characters should already most likely have been correctly placed. Cardiopteridaceae, however, heterogeneous as they are, might well house additional taxa. Including these might render an even more diverse family. Chase, Fay, and Savolainen (2000)
argue for using DNA patterns as a measure of overall genetic divergence when delimiting families. Apart from having higher jackknife support than Cardiopteridaceae and jackknife support as high as for the two families together (Fig. 2), Stemonuraceae have the longest branch in all the analyses (Table 3), that is, they are the group supported by most characters. The two families do not "share so much evolutionary history that most of what is true for one also holds for the other" (Chase, Fay, and Savolainen, 2000
, p. 687). Therefore, Stemonuraceae should be recognized separately.
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). I do not think the risk of confusing the name Stemonuraceae with Stemonaceae is too high, since the latter are a monocot family in Pandanales. I prefer Stemonurus, the second oldest generic name of the group, as the type genus over Lasianthera, which is the oldest genus, since the monotypic Lasianthera is morphologically less representative. Lasianthera has, for example, fused petals and an African distribution. Moreover, Stemonurus is one of two genera with more than a handful species as well as a rather wide southeast Asian and Malesian distribution. The other, Gomphandra, has sometimes been regarded as congeneric with Stemonurus (see Howard, 1940
and Sleumer, 1969
for the taxonomic history of the names Stemonurus and Gomphandra).
Stemonurus itself has hermaphroditic flowers with free, although agglutinized, petals with a keel and inflexed apex (Figs. 6–7). Its stamens have flattened, fleshy filaments that widen upwards and bear characteristic hairs (Figs. 6–8). The hairs are normally club-shaped with a large lumen and thick walls (the cylindrical hairs of Heintzelman and Howard, 1948
). At the base of the pistil there is often a slightly cup-shaped disc. The drupes are ovoid to elliptic and the endocarp is fibrous. The somatic chromosome number of Stemonurus is 2n = 44 (Oginuma et al., 1998
). The monotypic Cantleya shares many characters with Stemonurus (Fig. 3), but has a sessile stigma and more fusiform fruits. Sleumer (1969)
described Whitmorea, another monotypic genus, as closely related to Stemonurus. It differs mainly in having linear filaments, linear anther cells, and an ovary with an apical cavity into which the stigma is turned. All these characters are unmatched in other icacinaceous taxa.
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), are found in the following closely related genera: Discophora, Gastrolepis, Lasianthera, Medusanthera, and its segregates Codiocarpus and Irvingbaileya. In contrast to the three genera already discussed, they all lack the keeled petals, have "a characteristically flattened drupe with a fleshy appendage borne laterally" (Howard, 1943a
, p. 47), and a longitudinally ribbed endocarp. All genera mentioned so far except Lasianthera have flowers with free petals. Lasianthera and Gastrolepis have hermaphroditic flowers as do Stemonurus, Cantleya, and Whitmorea, while all the other have unisexual flowers. The filaments of Codiocarpus differ from those in the others in being filiform and lacking the hairs. Lasianthera and Stemonurus are the only genera that actually have a style, even though it is very short.
Three more genera should be included in Stemonuraceae, i.e., Gomphandra, Hartleya, and Grisollea. Gomphandra belongs here with its unisexual flowers, stamens of the "Stemonurus type," and sessile stigma (see Fig. 3). Its drupes are not laterally compressed and lack the fleshy appendage, as, for example, in Stemonurus. Hartleya was originally suggested as most closely related to Gastrolepis (Sleumer, 1969, 1971
). Even though Hartleya differs from that genus in some characters (e.g., unisexual flowers and glabrous filaments), it clearly posseses the general characters of the family.
According to Villiers (1980)
, Grisollea resembles Discophora and Gastrolepis in flowers and fruits. Grisollea clearly belongs to Stemonuraceae (Figs. 2–3). Some characters are, however, only found in this genus. For example, the male flowers lack petals and their stamens have short, thick, and glabrous filaments and extrorse anthers, and the ovary is crowned by a swelling, which surrounds the short style.
As shown above, members of Stemonuraceae share several characteristic features. In addition, they all have a combination of scalariform and simple perforation plates (paralleled only in Gonocaryum and Leptaulus) and pollen with a polar/equatorial quota equal to or less than 0.9. Stemonuraceae include mainly Australasian genera. The only exceptions are Discophora from South America, Lasianthera from Tropical Africa, and Grisollea from Madagascar, the Comoros, and the Seychelles.
Circumscription of Pennantiaceae–Pennantiaceae J. Agardh, Theoria Syst. Pl.: 301 (1858). Type: Pennantia J. R. Forst. & G. Forst. Monogeneric
In our analyses, Pennantia was represented by two of the four species, one Australian and one from New Zealand. Its entire distribution is covered. The placement of Pennantia in Apiales (Fig. 2) has never been suggested before. I prefer to expand Apiales rather than creating a monogeneric order. Monogeneric orders should be avoided in order to minimize redundancy in the classification (APG, 1998
). Also, I agree with the view held by Bremer (2000)
that a new order should only be described if it is sister to two or more of the 40 orders recognized in the classification by APG (1998)
. However, the family Pennantiaceae of Agardh (1858
; his Pennantieae) need to be recognized, since it is not possible to include Pennantia in any other family without violating monophyly.
Considering the characters used to describe Pennantia in Flora of New Zealand (Allan, 1961
) and Flora of Australia (Guymer, 1984
; Green, 1994
), it is clear that all of them are matched by at least one of the families of Apiales. It is worth noting that paracytic stomata are common in Apiales, while Pennantia is the only genus of Icacinaceae s.l. with that type exclusively. Furthermore, the only multicellular hairs of Icacinaceae s.l. are the uniseriate hairs of Pennantia corymbosa. Similar hairs are found, for example, in Pittosporaceae (Wilkinson, 1992
). A more detailed discussion of the morphology of Pennantiaceae and their relationships will be presented elsewhere.
Conclusions and systematic implications
The data presented show that Icacinaceae s.l. are polyphyletic. The genera included belong to both euasterids I and II and should be rearranged into three different orders: Garryales, Aquifoliales, and Apiales. In Table 4, I suggest how to treat the icacinaceous genera at the family level, and in Table 5, a summary of characters useful in delimiting these taxa is given. For those who dislike this increase in the already large number of families, I reiterate the view put forward by Miers, that scientists should "detect in the various natural groups of plants, a few decisive characters [synapomorphies], by which they can be readily distinguished, and this should be accomplished, even at the risk of increasing the number of families"; otherwise "the most opposite characters often become blended in one group, and we thus lose sight of every useful and well-defined line of demarcation" (Miers, 1851
, p. 174).
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, as well as in accordance with the principle of monophyly, I recommend both Stemonuraceae and Pennantiaceae be accepted at family level. Stemonuraceae are a morphologically distinct group of genera that deserves to be treated at family level (see above). Pennantiaceae must be recognized, even though accepting monogeneric families creates redundant names and obscure phylogenetic information (see Backlund and Bremer, 1998
). The data presented here provide no support for the inclusion of Pennantia in any other family. As exemplified by this study on Icacinaceae, our preconceived assumptions about relationships among the less known angiosperm families might be inaccurate. If, as in Icacinaceae s.l., several distinct evolutionary lineages are hidden within a single polyphyletic taxon, we may have to recognize even larger biodiversity in tropical plant communities than is recognized today.
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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