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Systematics |
2Bolus Herbarium, Department of Botany, University of Cape Town, 7701 Rondebosch, South Africa; 3Leslie Hill Molecular Systematics Laboratory, Kirstenbosch Research Centre, National Botanical Institute, Private Bag X7, 7735 Claremont, South Africa
Received for publication February 6, 2003. Accepted for publication May 1, 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Aizoaceae • atpB-rbcL • Caryophyllales • phylogeny • psbA-trnH • rps16 • trnL-F
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; APG, 1998
; Cuénoud et al., 2002
). Bittrich and Hartmann (1988)
reviewed the taxonomic history of the Aizoaceae and its various circumscriptions, which also incorporated the Mollugo group (e.g., Pax, 1889
; Ihlenfeldt and Straka, 1962
). Arguments based on nonmolecular characters have been put forward which suggest that, after separation of the Mollugo group (as done by Hutchinson [1926]
by establishing the Molluginaceae), the Aizoaceae form a monophyletic group (Bittrich and Hartmann, 1988
). That the Molluginaceae is not closely related to the Aizoaceae sensu stricto was later confirmed by rbcL, 18S, atpB, and matK sequences (Rettig et al., 1992
; Chase et al., 1993
; Soltis et al., 1997
, 2000
; Savolainen et al., 2000
; Cuénoud et al., 2002
) as well as variation in the structure and inverted repeat restriction sites of chloroplast DNA (Downie and Palmer, 1994
) and partial chloroplast DNA ORF2280 homolog sequences (Downie et al., 1997
). The presence of bladder cells in the epidermis, the hygrochastic capsule, and the perianth stamen tube may be synapomorphies for the Aizoaceae sensu stricto (Bittrich and Hartmann, 1988
), so that this restricted concept of the family is thought to be monophyletic.
Several molecular studies explore the phylogenetic position of the Aizoaceae within the order Caryophyllales (Rettig et al., 1992
; Chase et al., 1993
; Downie and Palmer, 1994
; Downie et al., 1997
; Soltis et al., 1997
, 2000
; APG, 1998
; Savolainen et al., 2000
). In all the studies the Aizoaceae is represented by a single species only, from one of the genera Trianthema (Sesuvioideae), Tetragonia (Tetragonioideae), Delosperma (Ruschioideae), except for the study by Cuénoud et al. (2002)
based on matK sequences, which incorporated six species across three subfamilies of Aizoaceae. The studies are largely congruent and place the Aizoaceae as sister to a clade comprising the Nyctaginaceae and some members of the polyphyletic Phytolaccaceae. Only a single study exists so far that addresses phylogenetic relationships within the Ruschioideae and was based on both chloroplast and nuclear data sets (Klak et al., in press
).
Clearly, the molecular studies published so far have not adequately addressed the question of the relationships within the Aizoaceae. The currently accepted classification of the Aizoaceae, based on nonmolecular characters (Bittrich and Hartmann, 1988
; Hartmann, 1993
, 2001a, b), was followed in this study.
In the most recent classification of the family (Hartmann, 2001) five subfamilies are recognized: Aizooideae, Tetragonioideae, Sesuvioideae, Ruschioideae, and Mesembryanthemoideae (Table 1). The Aizooideae, Tetragonioideae, and Sesuvioideae are only slightly succulent shrubs and include 145 species spread over 12 genera, which are distributed worldwide in tropical and temperate regions. The Ruschioideae and Mesembryanthemoideae, made up of 123 genera and about 1685 species, are all succulents and their center of distribution lies in the arid parts of southern Africa. Whereas the Mesembryanthemoideae form a relatively small group, of about 100 species in 11 genera, the Ruschioideae make up the largest group of the five subfamilies. Schwantes (1947
, 1957
) was the first to set up a tribal classification for the Ruschioideae, which he eventually subdivided into five tribes and 22 subtribes (Schwantes, 1971
). Later, Hartmann (1988
, 1991
, 1998
) replaced Schwantes' classification and arranged the genera into 12 groups but did not propose a formal classification. Recently, a formal tribal classification for the Ruschioideae was erected based on floral nectaries (Chesselet et al., 2002
) and in which four tribes are recognized (Apatesieae, Dorotheantheae, Delospermeae and Ruschieae). Of these, the first two are identical to Hartmann's Apatesia and Cleretum groups, respectively.
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; Bittrich and Hartmann, 1988
), other authors disagree and favor a division of the group into several small families (e.g., Friedrich, 1955
; Ihlenfeldt and Straka, 1962
; Chesselet et al., 2002
). Most frequently used and best established is the name Mesembryanthemaceae Fenzl. Within this family the subfamilies Mesembryanthemoideae and Ruschioideae are included, as both groups share the synapomorphy of petaloid staminodes. The three remaining subfamilies share a basic chromosome number of n = 8 and a perianth that is petaloid inside and sepaloid outside; these are considered to be synapomorphies for these three groups.
Bittrich (1990)
proposed two hypotheses of possible phylogenetic relationships among the subfamilies of the Aizoaceae. In the first hypothesis the Aizooideae, Tetragonioidae, and Sesuvioideae form a monophyletic group, which is sister to the Ruschioideae + Mesembryanthemoideae. In the second hypothesis the Ruschioideae + Mesembryanthemoideae are sister to the Aizooideae + Tetragonioideae. According to the latter hypothesis the Sesuvioideae would form an earlier branch within the Aizoaceae and constitute the sister group to the rest of the family. Only four of the subfamilies (Tetragonioideae, Sesuvioideae, Ruschioideae, Mesembryanthemoideae) are considered to be monophyletic, whereas the Aizooideae is considered to be paraphyletic as a result of the exclusion of the Tetragonioideae, which may be derived from members of the Aizooideae (Hofmann, 1973
; Bittrich, 1990
).
The aims of this study were to investigate the monophyly of the five subfamilies of the Aizoaceae and to test the hypotheses of intrafamiliar relationships proposed by Bittrich (1990)
. We intended to clarify whether Mesembryanthemaceae should be upheld as a separate family. In addition, we aimed to resolve relationships within the subfamilies, with particular attention given to the most species-rich subfamilies, namely the Ruschioideae and Mesembryanthemoideae.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, which may, potentially, be representative of maximally divergent evolutionary units within the subfamily. Several of the genera accepted by Hartmann (2001a, b) may not be monophyletic so that in some cases more than one representative per genus was included. Four outgroups were employed in the phylogenetic analyses. Phylogenetic trees based on DNA sequence data have shown the Phytolaccaceae and the Nyctaginaceae to be most closely related to the Aizoaceae. Therefore, Phytolacca dioica (Phytolaccaceae), Mirabilis jalapa, and Bougainvillea spectabilis (Nyctaginaceae) were chosen as outgroups. In addition, Limeum africanum (Molluginaceae) was included to root the tree.
In total, 95 taxa were included in the trnL-trnF and the rps16 intron data sets and 56 taxa in the combined four-gene-region analysis (trnL-trnF region, rps16 intron, atpB-rbcL intergenic spacer, and psbA-trnH intergenic spacer data sets; these data are available as Supplementary Data accompanying the online version of this article).
DNA extraction and amplification of template DNA
Total DNA was isolated from fresh leaf material of the 95 sampled species by the method of Saghai-Maroof et al. (1984)
as modified by Doyle and Doyle (1987)
. In some cases, where initial polymerase chain reaction (PCR) amplification did not yield a product, DNA was further purified by using the QIAquick PCR purification kit (Qiagen, Hilden, Germany).
The four DNA regions were amplified from total DNA by PCR. The trnL-F region (consisting of the adjacent trnL intron and trnL-F intergenic spacer) was amplified using primers c and f (Taberlet et al., 1991
). Primers used for amplification of rps16 were rpsF and rpsR2 (Oxelman et al., 1997
). The intergene spacer between the atpB and rbcL genes was amplified using primers 2 and 5 (Manen et al., 1994
). The psbA-trnH intergenic spacer was amplified using primers psbAF and trnHR (Sang et al., 1997
). Twenty-five microliter reactions were prepared, which contained 19 µL of sterile water, 2.5 µL of 10x PCR buffer, 1 µL of 10 mmol/L dNTPs in equimolar ratio, 0.75 µL of each 10 µmol/L primer, 0.5 µL of 25 mmol/L MgCl2, 0.125 µL of Taq DNA polymerase (5 units µL), and 0.5 µL of genomic DNA. In general, a 10x dilution of the extraction product was used as template DNA. The thermal reactions were carried out as follows: first 2 min at 97°C to ensure denaturation of double-stranded template DNA, 1 cycle; denaturing step of 95°C for 1 min, annealing step of 52°C for 45 sec and extension step of 72°C for 2 min; the three cycle steps were repeated 30 times and were finally followed by one extension step for 8 min at 72°C to complete unfinished DNA strands. The reactions were cleaned using the QIAquick PCR purification kit from Qiagen, and the purified products were eluted in 60 µL of Tris-EDTA buffer.
Sequencing and alignments
Both strands of the PCR products were cycle sequenced, as per manufacturer's instructions, using the ABI PRISM Dye Terminator Cycle Sequencing Ready Reaction Kit (Applied Biosystems, Foster City, California, USA). The primers used for amplification were also used for the sequencing reactions. In addition, for some samples the internal trnL-F region primers d and e were used (Taberlet et al., 1991
). The samples were run on an Applied Biosystems 377 automated DNA sequencer.
Data files were assembled and edited using GeneDoc version 2.6.002 (Nicholas and Nicholas, 1997
) and chromas version 1.43 (McCarthy, 1996–1997
). Sequences were aligned by eye. Ambiguous positions were coded using appropriate IUPAC (International Union of Pure and Applied Chemistry) ambiguity symbols so as to maximize retention of information. Gaps were coded as suggested by Simmons and Ochoterena (2000)
. They propose two methods for coding gaps, simple indel coding and complex indel coding. Their method of simple indel coding is followed in this study.
Cladistic analyses
Two matrices were analyzed, one consisting of combined trnL-F and rps16 intron sequences for 95 taxa representative of all five subfamilies of Aizoaceae and outgroups, and one consisting of combined rps16 intron, trnL-F, atpB-rbcL spacer and psbA-trnH spacer sequences for 56 taxa from the subfamily Ruschioideae. Due to the uniparental mode of inheritance of the plastid genome we would not expect incongruent patterns of relationships to be reflected by data sources from the different regions; we therefore analyzed combined matrices only for each taxon set.
All cladistic analyses were performed using the parsimony algorithm of the software package PAUP* version 4.0b4 (Swofford, 2000
). Each data matrix was analyzed using 1000 replicates of random taxon-addition to find islands of equally parsimonious trees, tree bisection-reconnection (TBR) branch swapping with MULPARS on, and all character transformations treated as equally likely (Fitch, 1971
). A limit of two trees saved on each replicate was set to minimize time spent swapping on islands of equally parsimonious trees. All trees found in the initial 1000 replicates were then used as starting trees for a second round of TBR swapping with a tree limit of 5000. Internal support was assessed using 1000 boostrap replicates (Felsenstein, 1985
) with simple taxon addition and a tree limit of 10 trees per replicate. Only those groups receiving greater than 50% support were reported. The number of steps contributed by each of the individual DNA regions was calculated for each analysis. For the 95 taxon matrix the contribution of transitions and tranversions and their relative performance (consistency and retention indices) was also calculated.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The monophyly of Aizoaceae receives 98% bootstrap support (BS). The two subfamilies Mesembryanthemoideae and Ruschioideae are each supported by 100% BS. Subfamily Tetragonioideae is polyphyletic: Tribulocarpus is placed with 100% BS as sister to subfamily Sesuvioideae, whereas Tetragonia fruticosa is sister to Gunniopsis (subfamily Aizooideae) (100% BS). Tetragonia and Gunniopsis are in turn placed with 98% BS as sister to the other five genera of the Aizooideae.
The relationships among the subfamilies are similarly well supported: the Sesuvioideae + Tribulocarpus are sister to the remainder of the Aizoaceae (98% BS). The Aizooideae + Tetragonia are retrieved as sister to the two succulent subfamilies Mesembryanthemoideae + Ruschioideae (98% BS). The Ruschioideae fall into four major clades (A–D; Fig. 1). Clade C incorporates the vast majority of members of the Ruschioideae, but few relationships are resolved and supported within this clade.
Four-gene-region analysis
The combined matrix (trnL-F, rps16 intron, atpB-rbcL spacer, and psbA-trnH spacer) contains 3824 characters (including four additional indels coded for the atpB-rbcL spacer data set), of which 303 characters were excluded due to dubious homology. Analysis of these four plastid regions for 56 taxa included 3521 characters of which 345 (10%) were variable and 67 (2%) were potentially parsimony informative. One thousand replicates gave 1928 equally parsimonious trees of length 414 with CI = 0.88 and RI = 0.78. Using these 1928 trees as starting trees in a second heuristic search gave 5000 equally parsimonious trees with identical tree length, CI and RI as in the initial search. The strict consensus of 5000 equally parsimonious trees is shown in Fig. 3. Bootstrap percentages are indicated below the branches.
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The addition of two further gene regions to the rps16 intron and trnL-F data set was intended to improve the resolution of the large polytomy (clade C) within the Ruschioideae. However, the relationships obtained for clade C in rps16/trnL-F analysis are very similar to those of the four-gene analysis (Fig. 3). The main difference is that one major additional (but unsupported) clade was retrieved in the four-gene-region analysis. This clade included eight genera (Faucaria, Mossia, Neohenricia, Bijlia, Orthopterum, Carruanthus, Cerochlamys, Machairophyllum) that form part of the Bergeranthus and Stomatium groups of Hartmann (1991)
.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). This is supported in this study, although Zaleya and Cypselea were not included here. Important synapomorphies for the genera traditionally included in the Sesuvioideae are bracteate inflorescences or bracteolate flowers (Hofmann, 1973
), circumscissile capsules, and arillate seeds (Bittrich and Hartmann, 1988
).
In the present classification Tribulocarpus dimorphanthus is part of the Tetragonioideae. This species is unusual for its heteromorphic flowers, and it was originally described as a species of Tetragonia (Pax, 1889
). It is also remarkable for its very disjunct geographical distribution, since it occurs in parts of Namibia and in Somalia (e.g., Thulin, 1993
; Hartmann, 2001b
). Due to the unusual floral morphology it was later placed in a genus on its own (Moore, 1921
), Tribulocarpus, which was considered to be closely allied to Tetragonia (e.g., Bittrich and Hartmann, 1988
). On account of the divergent morphology of the flowers and the fruits of Tetragonia and Tribulocarpus, some authors have favored their placement in a separate family (Tetragoniaceae, e.g., Friedrich, 1955
). This study shows, however, that Tribulocarpus is sister to the two species of Sesuvioideae and therefore forms part of the Sesuvioideae. The bracteate inflorescences, which have been listed as a synapomorphy for the Sesuvioideae, are shared with Tribulocarpus and may be used to delimit this subfamily.
Tetragonioideae
Only two genera are currently placed in the Tetragonioideae, namely Tetragonia and Tribulocarpus. Tetragonia is a fairly large genus consisting of 85 species, which are found in tropical and temperate regions of the Southern Hemisphere with a center of distribution in southern Africa. The members of this subfamily have been characterized by strongly lignified indehiscent, often horned or winged fruits, a semi- or completely inferior ovary and a short funicle. Despite these similarities, the fruits show marked differences between these two genera. In Tetragonia the fruit is simple and free from the bracts, whereas in Tribulocarpus the fruit is compound and fused to spinose bracts (Friedrich, 1955
). Whereas some authors have included Tribulocarpus in Tetragonia (Adamson, 1955
; Thulin, 1993
), others have retained it as a distinct genus (Bittrich and Hartmann, 1988
; Hartmann, 2001b
). Tetragonia retusa Thulin from Somalia displays a very similar floral morphology to Tribulocarpus such as the leaf-opposed flowers with a distinct, about 4 mm long perianth tube and a single two-lobed style (Thulin, 1993
). In these characters it differs from all other species of Tetragonia and is most similar to Tribulocarpus. On the other hand, Tribulocarpus has a capitulate inflorescence and a nonwinged, spiny compound fruit. On the basis of this character combination, Thulin (1993)
suggested that T. retusa may represent a link between Tetragonia and Tribulocarpus and that these two species should be recognized as marginal members of Tetragonia. However, as Tribulocarpus is shown here not to be closely related to Tetragonia, it appears worthwhile to reinvestigate the generic limits of the latter genus.
Aizooideae
The Aizooideae consist of six genera, which were all sampled in this study. The subfamily consists of annual to perennial herbs, subshrubs, or shrubs, with only slightly succulent leaves. The plants are found mainly in southern Africa and Australia, East Africa, western Arabia, and around the Mediterranean. Within the Aizooideae, all those genera for which more than one species were sampled (Galenia, Gunniopsis) were found to be monophyletic. Aizoon proves to be the most closely related genus within the Aizooideae to Galenia. The two species of Galenia sampled here (representing the two currently recognized subgenera) are retrieved as monophyletic, although members of Galenia subgenus Kolleria show similar features to those found in Aizoon (Bittrich, 1990
). The small genus Aizoanthemum, incorporating only five species, which was treated by Adamson (1959
, p. 44) as a subgenus of Aizoon, is shown here to be clearly distinct from the latter genus. Diagnostic features that separate the two genera are the basally flat filaments and the long expanding keels found in Aizoanthemum, as opposed to filiform filaments and short expanding keels in Aizoon.
The Australian endemic Gunniopsis is shown here to be most closely related to Tetragonia. Both genera differ remarkably in their fruit morphology from the other genera placed in the Aizooideae. In Tetragonia the fruits are strongly lignified and indehiscent and often winged, whereas they are hygrochastic in the remainder of the Aizooideae. Although the fruits of Gunniopsis are also hygrochastic, the valves are septicidal, whereas they are purely loculicidal in the other taxa of the Aizooideae (Acrosanthes, Aizoon, Galenia, Plinthus, Aizoanthemum).
A close association of Tetragonia to the members of the Aizooideae has been pointed out previously (Hofmann, 1973
; Bittrich, 1990
). Hofmann (1973)
found that in terms of the floral morphology, Tetragonia showed close links to Galenia and Plinthus. Bittrich (1990)
therefore suggested that both subfamilies together must be considered as a monophyletic group. Characters supporting the monophyly are the presence of epidermal bladder hairs in both subfamilies. These bladder hairs consist of a large terminal cell and a multicellular socle or stalk (Bittrich, 1990
). The only species investigated for this character, however, appear to have been members of Gunniopsis and Tetragonia. It is therefore possible that the presence of epidermal bladder hairs constitute a synapomorphy only for the clade consisting of Gunniopsis and Tetragonia. A further character that is very common in both subfamilies is the development of accessory lateral branches (Hofmann, 1973
), which in the other subfamilies is only recorded in Aptenia cordifolia (Troll and Weberling, 1981
). However, the most striking character that links Tetragonia with Galenia and Plinthus is the upright position of the seeds in the ripe fruit (Hofmann, 1973
; Bittrich, 1990
). Unfortunately, the above-mentioned morphological characters have so far been studied only for some of the members in the Tetragonia + Aizooideae clade. Therefore, more extensive morphological studies are required to establish which characters represent synapomorphies for the clades retrieved for the Aizooideae.
Mesembryanthemoideae
All genera of the Mesembryanthemoideae were sampled in this study, except for the monotypic Synaptophyllum. The subfamily includes about 100 species, which have evolved a wide range of morphological features and life-forms: true annual or biennial herbs, small to large shrubs or geophytes, and more rarely highly succulent compact forms, which are decumbent to erect with either woody or succulent stems. Most of the members are restricted to the winter rainfall region of southern Africa, with few occurring outside this area.
On the basis of several morphological characters this subfamily has been considered to form a monophyletic group, which is here supported by the molecular data. Characters that support the monophyly include the shell-shaped (koilomorphic) nectaries, the stamens and petals that (often) form a tube, and the presence of cortical bundles (Bittrich, 1986
). Taxonomic revisions and recircumscriptions for several of the genera of the Mesembryanthemoideae have been prepared in recent years (Ihlenfeldt and Bittrich, 1985
; Bittrich, 1986
; Gerbaulet, 1995
, 1996a
, b
, c
, 1997
; Klak and Linder, 1998
). In this study, some of the genera are shown not to be monophyletic. The genus Phyllobolus as constituted by Gerbaulet (1997)
is clearly polyphyletic. Phyllobolus digitatus, a highly succulent species with a dwarf growth form, is found here to be most closely related to Aspazoma, which has a shrubby habit. The former species has been recognized by many authors as a monotypic genus, Dactylopsis (e.g., Bittrich, 1986
; Chesselet et al., 2000
). It was thought by Bittrich (1986)
to be closely related to Phyllobolus, to which it was later moved on account of several shared derived characters with members of the Phyllobolus resurgens group (Gerbaulet, 1995
, 1997
). On the other hand, Phyllobolus digitatus shares with Aspazoma and Brownanthus a heteromorphic epidermis (i.e., the shape of the idioblasts on the stems differ from those found on the leaves) and neotenic seeds. A heteromorphic epidermis is nevertheless also found in species of Aptenia, so that this characteristic has evolved more than once in the Mesembryanthemoideae. However, a character that is unique to Aspazoma and Phyllobolus digitatus is that towards their bases the free parts of the leaves envelop each other to form a sheath around the stem. The remainder of the species of Phyllobolus sampled here are scattered among species of Aridaria and Prenia. Although the clade incorporating these species is very well supported, relationships among the three genera are both poorly resolved and poorly supported. In the past considerable controversy surrounded the level at which these genera should be recognized. Bittrich (1986)
proposed to include numerous genera into a single genus Phyllobolus, which he subdivided into five subgenera (i.e., Phyllobolus incl. Amoebophyllum, Sphalmanthus, Prenia, Aridaria, Sceletium) because he found that they were all morphologically interlinked. Later, Gerbaulet (1995
, 1996a
, b
, c
, 1997
) resurrected and recircumscribed most of these genera but incorporated Sphalmanthus and Amoebophyllum (= Phyllobolus roseus) in Phyllobolus. On account of a single shared character found in the seeds, Gerbaulet (1995)
thought Sceletium to be most closely related to Phyllobolus but provided no evidence as to which characters may link Aridaria and Prenia to Phyllobolus. In the present study Sceletium is placed as sister to Aptenia, which shows the former genus to be less closely related to the Phyllobolus alliance than previously suspected. On account of the low sample size, low level of resolution, and low support, it is premature to draw conclusions about the generic relationships of Prenia, Phyllobolus, and Aridaria. Nevertheless, the results suggest that the generic limits of these three genera should be reexamined.
This study shows that Mesembryanthemum is not monophyletic in its current circumscription either. In the latest synopsis of the genus, 16 species were recognized in three subgenera (Gerbaulet, 2001
). The three subgenera were represented each by one species in this study. Species placed in Mesembryanthemum and the monotypic Synaptophyllum are the only genera that are annuals (or short-lived), with the remainder of the species of Mesembryanthemoideae being perennials. Whereas until now Mesembryanthemum was thought to form the most basal group within the Mesembryanthemoideae (Bittrich, 1986
), it is shown here that only two of the subgenera (subg. Mesembryanthemum and subg. Opophytum) are placed as sister to the remainder of the Mesembryanthemoideae with M. barklyi (subg. Cryophytum) resolved as sister to the Phyllobolus alliance. This study suggests that each subgenus may represent a distinct evolutionary lineage. However, in the absence of a detailed taxonomic or cladistic treatment of Mesembryanthemum, more sampling is needed to establish whether the currently recognized subgenera form monophyletic groups and how they are related to each other. It is also noteworthy that an annual life form has evolved at least twice within this subfamily.
Whereas the majority of species of Aizoaceae have developed some degree of leaf succulence, some members of the Mesembryanthemoideae are remarkable for having a persistent succulent green cortex on the stems (and usually ephemeral leaves). On account of this single, though rather rare character, it was thought that Aspazoma, Psilocaulon, Aptenia, and Brownanthus were to be likely close relatives (e.g., Gerbaulet, 1995
). This study shows that Aptenia is far more closely related to members without a succulent green cortex than to those which have one, which supports earlier findings by Klak and Linder (1998)
. A reinterpretation of the morphological characters supports the close relationship between A. geniculiflora and Sceletium that is retrieved here. Aptenia geniculiflora shares a similar habit with several species of Sceletium, in that it is mostly found scrambling inside other bushes. The other three species of Aptenia (not sampled here) differ in several morphological characters from A. geniculiflora, such as four-angled stems (only indistinctly four-angled in A. geniculiflora) and the much broader and often ovate leaves. The latter character is found in most species of Sceletium and is absent in any other members of the subfamily. It may therefore represent a synapomorphy for this clade.
The monotypic Caulipsolon, which was originally part of Psilocaulon, is placed in this study as sister to the latter genus. Morphologically, it shares numerous similarities but none of the synapomorphies of Psilcaulon and has evolved several characters not found in any species of Psilocaulon, such as a tuberous rootstock and annual vegetative parts (Klak and Linder, 1998
). Although a tuberous rootstock with annual vegetative parts is typical for numerous species of Phyllobolus, Caulipsolon differs in floral and leaf epidermal features considerably from the latter genus.
The above examples show that the reticulate distribution of morphological characters and general scarcity of characters have made it difficult in the past to establish monophyletic groups within the Mesembryanthemoideae. The relationships retrieved in this study should therefore form the basis for a much broader study of the Mesembryanthemoideae and a reevaluation of the characters used to circumscribe genera.
Ruschioideae
The Ruschioideae, which consists of the majority of species of Aizoaceae (Table 1), falls into four major clades (A–D; Fig. 1): Clade A is identical with the Apatesia group of Hartmann (1991)
, which was formally recognized as a tribe, the Apatesieae, by Chesselet et al. (2002)
. All genera of this group except Skiatophytum had been included in this study. This is a very small clade of only 11 species, which consists of annual or perennial plants with mostly flat leaves (rarely trigonous), flowers with flat broad nectariferous rings, and fruits with reduced expanding tissue. Most of the members of the Apatesieae are restricted to the flats of the southwestern Cape. Their position within the Ruschioideae has been assumed for some time to be clearly distinct from the remainder of the Ruschioideae on account of their different floral and fruit morphology (Ihlenfeldt, 1960
). Similarly, Clade B incorporates a small group of about 11 species that have evolved several unique morphological characters. All members of this clade are annuals with flat leaves and prominent bladder cells, flowers with a broad, flat, segmented nectarial ring, and fruits with prominent expanding sheets. On the basis of these characters they were placed by Hartmann (1991)
into a separate group, the Cleretum group, which was recently recognized as the tribe Dorotheantheae by Chesselet et al. (2002)
. The wealth of morphological characters found in both of these groups is corroborated by the number of DNA sequence changes (proportional to the length of the branches) in this study (Fig. 2). Bittrich and Struck (1989)
suggested that the Dorotheantheae probably formed an early evolutionary branch within the Ruschioideae. In this study the Apatesieae (clade A) are sister to the Dorotheantheae (clade B) + the remainder of the Ruschioideae (clades C + D). Although the Dorotheantheae do form an early branch within the Ruschioideae, they are shown here to be more closely related to the remainder of the Ruschioideae than to the Apatesieae, as was recently hypothesized by Chesselet et al. (2002)
based on a survey of characters of the fruits and nectaries. The remainder of the Ruschioideae (clades C + D) forms a highly supported clade. Numerous morphological characters change at the base of this clade including modifications in leaf shape, leaf epidermal characters, and leaf anatomical characters (e.g., wide band tracheids; Landrum, 2001
) and the innovation of a crested (lophomorphic) nectary. Again the numerous molecular changes at the base of clade B (Fig. 2) correspond to the amount of DNA sequence change observed.
On the other hand there were relatively few DNA sequence changes at the bases of clades C and D, with even fewer changes found within the two clades (Fig. 2). The two clades are remarkably unequal in size: clade D incorporates all six species of Drosanthemum + one of the four species of Delosperma included in this study, which is sister to a large polytomy (clade D). There are currently about 100 species placed in Drosanthemum, which are characterized by crystalline-papillate leaves, rough to hispid internodes, and complete covering membranes. Drosanthemum was separated from the very similar genus Trichodiadema by the lack of a diadem at the tip of the leaf and from Delosperma by the presence of covering membranes (Schwantes, 1927
, p. 29; Hartmann, 2001a
, p. 228). In a study of the fruits of Drosanthemum a certain type of differentiated pedicel was identified as a further synapomorphy (Hartmann and Bruckmann, 2000
). On account of the lack of these characters, Drosanthemum asperulum (Salm-Dyck) Schwantes (reinstated as Delosperma asperulum) and D. zygophylloides had been excluded from the genus (Hartmann and Bruckmann, 2000
). This study shows that both species form part of Drosanthemum (Figs. 1–3). Despite numerous morphological similarities, neither Trichodiadema nor the other species of Delosperma appear to be very closely related to Drosanthemum and it appears that Drosanthemum forms a distinct evolutionary lineage. The clade is possibly characterized by the presence of roughened stems at least on young growth, which was found also in those species excluded by Hartmann and Bruckmann (2000)
. The results emphasize again that both a broader molecular survey of species of Drosanthemum as well as a detailed morphological study is required to gain a better understanding of the evolution of morphological characters and their possible use in the circumscription of genera.
Trichodiadema and Delosperma were retrieved in a clade (BS < 50%) with Meyerophytum, Disphyma, and Malephora (Figs. 1 and 3). All five of these genera are currently placed in the Mitrophyllum or Delosperma groups (Hartmann, 1991
). Other members of these two groups, such as Diplosoma, Monilaria, and Gibbaeum remain unresolved within the large polytomy.
A further clade is retrieved only in the four-gene-region analysis (restricted to members of the Ruschioideae), which incorporates all eight genera sampled from the Stomatium and Bergeranthus groups (Fig. 3). Members of these groups exhibit mostly a highly compact and dwarfed habit, flowers with yellow petals (rarely white or pink), and five separate nectaries. These characters distinguish them to a large extent from the other compact, dwarfed species, which have mostly purple flowers, with a nectarial ring, and which are placed in the Titanopsis and Dracophilus groups. These two clades therefore render some support (although with very low BS support) for the informal groups proposed by Hartmann (1988
, 1991
). However, the present study does not support the monophyly of the tribe Delospermeae (consisting of Hartmann's Bergeranthus, Stomatium, and Delosperma groups) (Chesselet et al., 2002
), since Drosanthemum (Delosperma group) is sister to a well-supported clade (95% BS) incorporating the other members of the Delospermeae as well as the Ruschieae.
Despite the use of four plastid regions, which are frequently employed to resolve generic and species level relationships in other angiosperm groups (Gielly et al., 1996
; Kim et al., 1996
; Lidén et al., 1997
; Mes et al., 1997
; Oxelman et al., 1997
), there is a surprising lack of resolution among the taxa of clade C of the Ruschioideae. This clade is representative of a large group of about 1563 species in 101 genera and thus constitutes about 85% of the total number of species included in the Aizoaceae (Table 1). The diverse range of morphology, in particular growth forms and leaf surfaces, found among genera and species in this group has been pointed out by various authors (e.g., Ihlenfeldt, 1994
; Hartmann, 2001a
, p. 15), and much of this diversity was sampled in this study. The very short and many zero length branches at the base of clade C (Fig. 2) indicate that there are very few DNA sequence changes that separate the taxa. Therefore scarcity of characters may explain the pattern observed in our phylogenetic tree. The study by Klak et al. (2003)
of the Lampranthus group (Ruschioideae) in which two nuclear and one chloroplast data sets had been analyzed had also yielded relatively few informative characters. Such short branch lengths at a base of a clade have already in other plant groups been associated with a rapid and recent diversification (e.g., Bakker et al., 1999
; Richardson et al., 2001
), although the number of species involved in the radiation of the Ruschioideae is as yet unmatched. The possible onset of this large radiation and morphological innovations that may have facilitated this diversification will be discussed in a forthcoming paper.
Relationships among the five subfamilies
The Sesuvioideae are shown here to be sister to the remainder of the Aizoaceae, which lends support to Bittrich's (1990)
second hypothesis (see above). Morphologically the Aizooideae, Mesembryanthemoideae, and Ruschioideae share several characters that are not found in the Sesuvioideae. These are hygrochastic, loculicidal capsules and characteristics in the floral ontogeny and morphology (Bittrich, 1990
). The similarity in the morphology and anatomy of the hygrochastic capsules in all of the three subfamilies supports a unique origin of this structure (Bittrich, 1990
). Therefore, the alternative hypothesis (see above), that the only slighly succulent subfamilies (i.e., Sesuvioideae, Aizooideae, Tetragonioideae) form a monophyletic group, can be rejected.
With respect to the two highly succulent subfamilies Ruschioideae and Mesembryanthemoideae, this study confirms earlier hypotheses (e.g., Bittrich and Hartmann, 1988
) that they form a monophyletic group. There are numerous morphological characters that have been considered as synapomorphies for these two subfamilies (Ihlenfeldt and Straka, 1962
; Bittrich and Hartmann, 1988
; Bittrich and Struck, 1989
), e.g., the petals are of staminodial origin and the basic chromosome number is n = 9.
On account of the phylogenetic tree retrieved in this study the subfamilies could be recognized in two ways. In the first instance the Sesuvioideae (including Tribulocarpus), the Aizooideae + Tetragonioideae and the Ruschioideae + Mesembryanthemoideae could each be recognized as a separate family. The Sesuvioideae and the Aizooideae + Tetragonioideae share numerous morphological characters such as the little succulent leaves, tepals that are colored on the inside but are green and leaf-like outside, and a basic chromosome number of n = 8 (Bittrich, 1990
). The presence of these shared characters in both clades and the relatively small number of species involved (Table 1) speak against recognizing the Sesuvioideae (including Tribulocarpus) and the Aizooideae + Tetragonioideae each at family rank. Alternatively, the widley used concept of the Aizoaceae comprising all subfamilies could be upheld. The latter classification is preferred here, as it would conserve an already well-established family concept. The family as a whole is well defined, as all members of the Aizoaceae share the synapomorphy of an epidermis with thin-walled, water-storing bladder cells that is unique within the order Caryophyllales (Bittrich, 1986
; Bittrich and Hartmann, 1988
; Hartmann, 2001a
).
Biogeography of Aizoaceae
The main center of distribution is clearly the arid regions of southern Africa. Minor centers can be found in arid Australia, in Central America, and on the western coast of South America. Members of the earliest diverging clade, the Sesuvioideae + Tribulocarpus, are distributed mainly in regions of summer rainfall or in tropical, often coastal areas worldwide. However, the distribution centers of the remaining subfamilies are located in winter rainfall areas or winter/summer rainfall transitional areas. Thus, the distribution of the subfamilies is in part influenced by climatic factors (Bittrich, 1990
). Few of the genera are widespread. The most widespread genus is probably Tetragonia, with endemic species found in Australia and South America but with most of its species restricted to southern Africa. The presence of species of Aizoaceae in Australia or South America has in the past been attributed to long-distance dispersal, a system in which widespread species became starting points for a radiation, leading to new endemic species (e.g., Shmida, 1985
, Bittrich, 1990
). This hypothesis is supported by the rather short branch length between Tetragonia fruticosa (restricted to South Africa) and the two species of Gunniopsis (endemics to Australia), both of which suggest a more recent dispersal event as opposed to an old Gondwanan connection. Some fruits of Tetragonia have been documented to be dispersed by birds in Australia (Forde, 1986
), which makes long-distance dispersal a more likely explanation for the observed pattern than vicariance.
With few exceptions the members of the Mesembryanthemoideae and Ruschioideae are endemic to southern Africa, with few species occurring only outside this area (e.g., Delosperma harazianum (Deflers) Poppendieck & Ihlenf., Disphyma australe (Aiton) J.M. Black, Carpobrotus chilensis (Molina) N.E.Br.). Within southern Africa the greatest number of species are found in the Succulent Karoo (Bittrich, 1986
; Jürgens, 1986
), which is characterized by the dominance of leaf succulents (Jürgens, 1986
). Within this area the number and coverage of members of the subfamilies Ruschioideae and Mesembryanthemoideae exceeds that of any other plant group (Jürgens, 1986
). The distribution area of the two subfamilies largely coincides, and members often share similar habitats. However, the two earliest diverging clades (A + B) within the Ruschioideae, the Apatesia and Cleretum groups, are largely restricted to the southwestern Cape. Within this region they form part of the fynbos or rhenosterveld vegetation. Although genera from clades C + D are also found in these two vegetation types (e.g., Lampranthus, Erepsia, Oscularia) and also in the summer-rainfall areas (e.g., Dinteranthus, Mossia, Neohenricia), the major radiation of species has occurred within the Succulent Karroo region.
Taxonomy
The classification and circumscription of the subfamilies proposed below differ little from the formal treatment by Bittrich and Hartmann (1988)
, but recognize four instead of five subfamilies. In addition, for future ease of reference, the three most divergent clades (i.e., clades A, B, and C + D) that were retrieved for the Ruschioideae are recognized each as a formal tribe. The tribal classification proposed here accepts only two of the four tribes (i.e., Apatesieae, Dorotheantheae) as circumscribed by Chesselet et al. (2002)
. Our third tribe, Ruschieae, has been enlarged and incorporates the other two tribes of Chesselet et al. (2002)
(Ruschieae and Delospermeae).
Aizoaceae Martynov
Type
Aizoon L.
Subfamily 1. Aizooideae
Type
Aizoon L.
Tetragonioideae Lindley, The Vegetable Kingdom, 3rd ed.: 527 (1853).
Type
Tetragonia L.
Diagnostic features
Annuals to perennials, with herbaceous or woody branches; leaves slightly succulent, mostly alternate, flat or more rarly cylindrical; inflorescence leafy, in Tetragonia usually andromonoecious; perianth internally petaloid, externally sepaloid; flowers perigynous, epigynous, or rarely hypogynous, with a holonectary; capsules loculicidal or septicidal, often hygrochastic or a winged nut or horn-shaped; chromosome number x = 8.
Genera
Acrosanthes Eckl. & Zeyh., Aizoanthemum Dinter ex Friedrich, Aizoon L., Galenia L., Gunniopsis Pax, Plinthus Fenzl., Tetragonia L.
Subfamily 2. Sesuvioideae
Lindley, The Vegetable Kingdom, 3rd ed.: 527 (1853).
Type
Sesuvium L.
Diagnostic features
Prostrate to erect perennials or annuals; leaves slightly succulent, petiolate, often stipulate, flat or more rarely cylindrical; inflorescence bracteate; perianth internally petaloid, externally sepaloid; flower perigynous, with a holonectary; fruit a circumscissile capsule or compound and fused to spinous bracts; chromosome number x = 8.
Genera
Cypselea Turp., Sesuvium L., Trianthema L., Tribulocarpus S. Moore, Zaleya N.L. Burman.
Subfamily 3. Mesembryanthemoideae
Ihlenf., Schwantes & Straka, Taxon 11: 52–56 (1962).
Type
Mesembryanthemum L.
Aptenioideae Schwantes, Sukkulentenkunde 2: 39 (1947), nomen inval. Aptenioideae Schwantes ex Bittrich & H.E.K. Hartmann, Botanical Journal of the Linnean Society 97: 250 (1988), nomen illeg.
Type
Aptenia N.E.Br.
Coilomorphioideae Rappa & Camarrone, Lavori dell'Istituto Botanico e del Giardino Coloniale di Palermo 14: 30 (1953).
Type
Not given.
Diagnostic features
Annual to short-lived or perennial herbs or shrubs, cortex with vascular bundles; leaves succulent, usually flat to almost cylindrical and channeled, bladder cells often large and conspicuous; flowers with petals of staminodial origin, with a central placenta, ovary half-inferior or inferior, nectaries koilomorphic, i.e., always separated and grooved; fruit a hygrochastic capsule with purely septal expanding keels reaching from the central columella to the tip of the valve or very rarely a woody nut; chromosome number x = 9.
Genera
Aptenia N.E.Br., Aridaria N.E.Br., Aspazoma N.E.Br., Brownanthus Schwantes, Caulipsolon Klak, Mesembryanthemum L., Phyllobolus N.E.Br., Prenia N.E.Br., Psilocaulon N.E.Br., Sceletium N.E.Br., Synaptophyllum N.E.Br.
Subfamily 4. Ruschioideae
Schwantes ex Ihlenfeldt, Schwantes & Straka, Taxon 11: 52–56 (1962).
Type
Ruschia Schwantes.
Diagnostic features
Perennial shrubs, rarely annual; leaves succulent, usually cylindrical or trigonous, rarely flat, epidermis rarely with conspicuous bladder cells, usually xeromorphic; flowers with petals of staminodial origin, with a basal or parietal placenta, ovary inferior, nectaries lophomorphic, i.e., crested, either separated or in a ring or rarely glands flattened; fruit a hygrochastic capsule with expanding keels of mainly valvar origin with only small septal portion near the outer rim of the locule, never reaching to the center of the fruit, mostly with covering membranes and additional closing devices; chromosome number x = 9.
Tribus 1. Apatesieae
Schwantes ex Ihlenfeldt, Schwantes & Straka, Taxon 11: 55 (1962).
Type
Apatesia N.E.Br.
Diagnostic features
Plants annual to perennial; leaves mostly flat, with conspicuous bladder cells only along the leaf margins; flowers with a broad flat nectariferous ring; fruits with reduced expanding tissue, breaking into mericarps.
Genera
Apatesia, Carpanthea, Caryotophora, Conicosia, Hymenogyne, Saphesia, Skiatophytum; 11 species.
Tribus 2. Dorotheantheae
(Schwantes ex Ihlenf. & Struck) Chesselet G.F.Sm. & A.E. van Wyk, Taxon 51: 306 (2002).
Type
Dorotheanthus Schwantes.
Diagnostic features
Plants annual; leaves flat, with conspicuous bladder cells over the entire leaf surface; flowers with a broad flat, segmented nectariferous ring; fruits with reduced expanding tissue, breaking into mericarps.
Genera
Aethephyllum N.E.Br., Cleretum, Dorotheanthus; 11 species.
Tribus 3. Ruschiae
Schwantes ex Ihlenfeldt, Schwantes & Straka, Taxon 11: 54 (1962).
Type
Ruschia Schwantes.
Delospermeae Chesselet, G.F.Sm. & A.E. van Wyk, Taxon 51: 306 (2002).
Type
Delosperma N.E.Br.
Diagnostic features—Plants perennial, stems woody; leaves cylindrical or trigonous, often basally fused into a sheath, usually with a xeromorphic epidermis, rarely with prominent bladder cells; flowers with crested nectaries, glands either in a ring or separated; capsules hygrochastic (very rarely xerochastic).
Genera
About 101 genera, approximately 1563 species.
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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