Phylogenetics of Dilleniaceae Using Sequence Data ...

Phylogenetics of Dilleniaceae Using Sequence Data from Four Plastid Loci ( rbcL , infA , rps4 , rpl16 Intron) Author(s): James W. Horn Reviewed work(s): Source: International Journal of Plant Sciences, Vol. 170, No. 6 (July/August 2009), pp. 794813 Published by: The University of Chicago Press Stable URL: http://www.jstor.org/stable/10.1086/599239 . Accessed: 03/12/2012 21:21 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp

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Int. J. Plant Sci. 170(6):794–813. 2009. Ó 2009 by The University of Chicago. All rights reserved. 1058-5893/2009/17006-0008$15.00 DOI: 10.1086/599239

PHYLOGENETICS OF DILLENIACEAE USING SEQUENCE DATA FROM FOUR PLASTID LOCI (rbcL, infA, rps4, rpl16 INTRON) James W. Horn1 Department of Biology, Duke University, Durham, North Carolina 27708, U.S.A., and Fairchild Tropical Botanic Garden, 11935 Old Cutler Road, Coral Gables, Florida 33156, U.S.A.

Dilleniaceae are an angiosperm family consisting of 10–14 genera and ;500 described species, with a pantropical distribution extending into temperate Australia. This study addresses the infrafamilial relationships of Dilleniaceae with nucleotide sequence data from the plastid loci rbcL, infA, rps4, and the rpl16 intron. Analyses of these data using maximum parsimony and Bayesian methods resolve Tetracera, the only pantropical genus in the family, as sister to all other Dilleniaceae. Within the clade of Dilleniaceae exclusive of Tetracera, the New World endemic genera form a clade that is sister to a clade composed of the Old World endemic genera. The latter contains two major subclades: (1) a clade containing Acrotrema, Dillenia, and Schumacheria and (2) a clade containing Hibbertia and its satellite genera, Adrastaea and Pachynema, which are embedded within Hibbertia. Ancestral-state reconstructions of six morphological characters of both biological and taxonomic significance within Dilleniaceae suggest hypotheses of polarity or lability for each that differ substantially from those based on evolutionary trends. Perforation plate–type evolution within Dilleniaceae is equivocal, but the large majority of most parsimonious reconstructions suggest that simple perforation plates are plesiomorphic. Poorly organized leaf venation architecture is synapomorphic for Hibbertia s.l. Floral morphological features classically regarded as primitive, such as exceptionally large numbers of stamens (200þ) and numerous carpels (more than isomerous with the corolla), are clearly derived within Dilleniaceae and are features of uncommon occurrence within the family as a whole. Both multicarpellate, synorganized gynoecia and monosymmetric androecia have multiple origins within the family. A new classification of Dilleniaceae is outlined, and nomenclatural changes necessitated by the phylogenetic results are provided. Keywords: Dilleniaceae, character evolution, molecular systematics, floral morphology. Online enhancement: appendix table.

Introduction

of Actinidiaceae by several early authors (e.g., Baillon 1865), has remained stable (de Candolle 1824; Gilg and Werdermann 1925; Hutchinson 1964; Dickison 1970b; Takhtajan 1997). Molecular systematic studies to date, in accordance with this perception, strongly suggest the monophyly of Dilleniaceae, but they sample a narrow range of diversity within the family (Hoot et al. 1999; Savolainen et al. 2000a, 2000b; Ingrouille et al. 2002; cf. Hilu et al. 2003; see ‘‘Discussion’’). The relationship of Dilleniaceae to other angiosperms remains poorly known, despite the long-standing view that they are a lineage important for understanding angiosperm phylogeny at deep hierarchical levels. Molecular phylogenetic studies addressing the relationship of Dilleniaceae within angiosperms have yet to reach a consensus regarding placement of the family beyond indicating it as an early-diverging lineage within the core group of eudicots (Stevens 2001–2009; APG 2003). A majority of these studies, however, resolve the family as sister to either Caryophyllales (Hoot et al. 1999; Soltis et al. 2000, 2003, 2005, 2007) or Vitaceae (Chase et al. 1993; Savolainen et al. 2000b; Hilu et al. 2003). Recent studies employing increasingly large data sets suggest that Dilleniaceae are a yet more deeply divergent lineage within core eudicots, potentially sister to a superclade of multiple ordinal-level clades (of various circumscriptions, depending on the study; Worberg et al. 2007; Moore et al. 2008).

Dilleniaceae are a family of trees, shrubs, and lianas containing 10–14 genera and ;500 species, with a pantropical distribution that extends into temperate Australia (fig. 1; Horn 2007). Although remarkably diverse, especially in habit and floral structure, the family is readily diagnosed by a unique suite of morphological features. Of these, vegetative characters are the most reliable means of identifying the family over much of its geographic range. The combination of scabrous leaves and primary stems; leaf venation with more or less straight, parallel secondaries and scalariform tertiaries; petioles with a broad insertion at the stem; and orangish inner or outer bark that exfoliates thin plates or strips is diagnostic. Floral characteristics that distinguish the family include uniformly persistent and typically accrescent calyces; apopetalous, caducous corollas; polymerous, marcescent, or tardily deciduous androecia; free stylodia; and arillate seeds. Thus identifiable, Dilleniaceae have been considered a natural grouping within angiosperms whose circumscription, apart from the inclusion 1 Current address: Department of Botany and Laboratories of Analytical Biology, Smithsonian Institution, P.O. Box 37012, NMNH MRC-0166, Washington, DC 20013-7012, U.S.A.; e-mail: [email protected].

Manuscript received July 2008; revised manuscript received March 2009.

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HORN—PHYLOGENETICS OF DILLENIACEAE

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Fig. 1 Distribution of Dilleniaceae. A, Distribution of Tetracera (Delimoideae; across whole shaded area) and Doliocarpoideae (Neotropical only). B, Distribution of Hibbertia (Hibbertioideae). C, Distribution of Dillenioideae. Dillenia occurs within the whole of the shaded area; Didesmandra, endemic to Borneo, is indicated by a white star; distributions of other genera are as indicated.

The inherent biological significance of Dilleniaceae, however, centers on its extensive structural diversity. Dilleniaceae are remarkable among angiosperm families because they vary with respect to many characters that formed the basis of the evolutionary trends that formerly objectified angiosperm systematics (Stebbins 1974; Stebbins and Hoogland 1976; Cronquist 1988; Takhtajan 1991). Illustrative of this, merosity within the androecium and gynoecium of dilleniaceous flowers ranges from 1 to 900 stamens and from 1 to 20 carpels, respectively (Gilg and Werdermann 1925; Hoogland 1952; Endress 1997). Carpels may be entirely free or show substantial synorganization. Floral symmetry varies from polysymmetric to monosymmetric. The unusual patterns of variation among the large constellation of ‘‘fundamental’’ trend-based characters within Dilleniaceae not only shaped the former view that the family provided a link between magnoliid dicots and more ‘‘advanced’’ dicot lineages (Cronquist 1981) but also were critical for establishing evolutionary hypotheses within the family. Dickison (1967a, 1968, 1970b) and others (Stebbins 1974; Stebbins and Hoogland

1976; Rury and Dickison 1977) made explicit use of evolutionary trends in their phylogenetic interpretations of structural data. Despite the family’s protean nature, the infrafamilial classification of Dilleniaceae has been rather stable, with just two major groups most often recognized. Tetracera, the only pantropical genus, along with the Neotropical endemics Curatella, Davilla, Doliocarpus, and Pinzona, constitute the tribe Delimeae (de Candolle 1824; ¼Tetracereae: Gilg & Werdermann 1925; Hutchinson 1964), or subfamily Delimoideae (¼‘‘Tetraceroideae’’ of Hoogland 1952 and Dickison 1970b). Except for Curatella, species of these genera are often lianas, a growth form otherwise rare within the family (Kubitzki 1970, 1971). Tribe Dilleniae (de Candolle 1817, 1824), or subfamily Dillenioideae (Hoogland 1952), contains Acrotrema, Adrastaea, Didesmandra, Dillenia, Hibbertia, Pachynema, and Schumacheria, which are restricted to the Old World. The largely Australian genera Hibbertia (which often includes the monotypic Adrastaea) and Pachynema and the nearly herbaceous Acrotrema are segregated as tribes in


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INTERNATIONAL JOURNAL OF PLANT SCIENCES

some classifications (Gilg and Werdermann 1925; Hutchinson 1964). Dillenioideae, as considered here, display a significantly greater amount of structural and ecological diversity than Delimoideae, and they range in habit from large rainforest trees with leaves more than 1 m long (Dillenia spp.; Hoogland 1952) to xeromorphic subshrubs possessing minute leaves 1 mm long borne on phyllocladous shoot systems (Pachynema spp.; Craven and Dunlop 1992). But because the states of most characters considered important for understanding relationships within Dilleniaceae have complex distributions suggestive of mosaic evolution, uncertainty regarding the potential phylogenetic and classificatory significance of all structural and chemical features within the family eventually leads to the complete abandonment of any system of classification above the genus level (Gurni and Kubitzki 1981; Aymard C 1997; but see Horn 2007). Here I present a phylogenetic hypothesis of Dilleniaceae based on sequence data from four plastid loci. Of the four regions chosen, three have been shown to be sufficiently variable to elucidate infrafamilial relationships (rbcL: Prince and Parks 2001; Chase et al. 2002; Gustafsson et al. 2002; Wurdack et al. 2004; rps4: Reeves et al. 2001; the rpl16 intron: Kelchner and Clark 1997; Zhang 2000; Clausing and Renner 2001; Downie et al. 2001). Data from the plastid gene infA (Millen et al. 2001) are here employed for the first time in a phylogenetic study. The first goal of this study is to test the monophyly of genera of Dilleniaceae and to discover the major clades within the family. The second goal is to examine character evolution in the context of a new phylogenetic hypothesis for the family, emphasizing characters that were important to previous hypotheses of phylogenetic trends in Dilleniaceae and angiosperms as a whole. Finally, a new classification of Dilleniaceae, based on the phylogenetic results, is presented.

Material and Methods Taxon Sampling Voucher information for the taxa included in the analyses are listed in table A1 in the online edition of the International Journal of Plant Sciences. Within Dilleniaceae, 57 species were sampled, representing 12 of the 14 genera (including major segregate genera) recognized in the primary specialist treatments of the family (Gilg and Werdermann 1925; Harden and Everett 1990; Aymard C 1997). Suitable material was not available for Didesmandra and Neodillenia. Twenty-two species of Hibbertia s.l., the largest and most taxonomically complex genus of the family, were included. Sampling within Hibbertia was guided by the classification of Gilg and Werdermann (1925) and by preliminary results of a separate molecular phylogenetic study of Hibbertia, which included a large majority of the species currently recognized within the genus (Horn 2005). Within the species-rich genera Davilla, Dillenia, Doliocarpus, and Tetracera, a minimum of five species each were included, chosen to represent subgeneric groups recognized in recent monographs (Davilla and Doliocarpus: Kubitzki 1971; Dillenia: Hoogland 1952; Tetracera: Kubitzki 1970) and to span the geographic range. Because many recent large-scale molecular phylogenetic analyses suggest that Dilleniaceae are sister to either Caryophyllales or Vitaceae (see ‘‘Introduction’’), exemplars from these taxa were chosen as outgroups (table A1). Within Caryophyllales, species

were chosen as exemplars of major clades (see Cueńoud et al. 2002).

DNA Extraction, PCR Amplification, and Sequencing Leaf material for DNA extraction was obtained from samples collected in the field and desiccated in silica gel and from herbarium specimens at MO, NCU, NY, and US. An area of dry leaf tissue measuring 0.5–1.0 cm2 for each sample was disrupted with a stainless-steel ball bearing or a porcelain bead in a Model 2000 Geno/Grinder (SPEX CertiPrep, Metuchen, NJ). Extractions of total genomic DNA were made by using the DNeasy Plant Mini Kit (Qiagen, Valencia, CA) according to the manufacturer’s protocols, except for the modification of lysis conditions by the addition of 570 mg of proteinase K (PCR grade; Roche Diagnostics, Indianapolis, IN) with subsequent agitation at 37°C for 24–48 h. Double-stranded DNA templates were amplified via PCR for four chloroplast loci: infA, rbcL, rps4, and the rpl16 intron. Amplifications and/or cycle sequencing reactions used the following primer combinations for PCR: infA, rpl36-f/rps8-r (rpl36-f: 59-CACAAATTTTACGAACGGAAG-39; rps8-r: 59-TAATGACAGAYCGAGARGCTCGAC-39; K. J. Wurdack, personal communication); rbcL, 1F/1460R (Fay et al. 1998) or rbcLDillR; rps4, TRNAS/rps5 (Nadot et al. 1995) or rps4DillF/ rps4DillR; rpl16 intron, F71/R1661 (Kelchner and Clark 1997). The infA primers are rooted in flanking plastid genes (i.e., rpl36 and rps8, respectively), which ensures that plastid copies are amplified, rather than nuclear copies originating from plastid-nuclear gene transfers (see Millen et al. 2001). Since the 1460R primer, typically used to amplify rbcL, primed poorly to its target sequence for a few ingroup taxa, a new reverse primer, rbcLDillR (59-TCCATACTTCACAAGCAGGAG-39), was designed for those problematic taxa. Likewise, new primers (rps4DillF: 59-GTGATCTYAGAAACCAATCKCG-39; rps4DillR: 59-ATTATTCCAACAGCAGGGCCT-39) were designed for the rps4 gene because the standard primers consistently amplified multiple fragments of varying length under a variety of PCR conditions for many taxa of Dilleniaceae. The newly designed rps4 primers consistently yielded single bands. Amplified products were cleaned with the QIAquick PCR Purification Kit (Qiagen) and directly cycle sequenced by using an ABI BigDye Terminator Cycle Sequencing Kit (Applied Biosystems, Foster City, CA). Sequences were resolved on an ABI Prism 3700 DNA Analyzer automated sequencer (96 capillaries).

Sequence Manipulation and Alignment Sequence assembly and editing were done with Sequencher, version 4.1.2 (Gene Codes, Ann Arbor, MI). Data matrices were aligned by eye in Se-Al, version 2.0a11 (Rambaut 1996). Within the rps4 gene, only the nucleotides within the region amplified by the rps4DillF/rps4DillR primers (excluding the priming regions themselves) were included in subsequent analyses. Gapped regions and regions of ambiguous alignment were identified and excluded from subsequent analyses. Gaps were interpreted as missing data and were not coded as separate characters.



Phylogenetic Analysis Because Dilleniaceae are distantly related to all potential outgroups, a preliminary analysis (analysis I) was conducted with the infA and rbcL genes for all 57 ingroup taxa plus the four outgroup taxa. Outgroup sequences of rps4 and the rpl16 intron have large regions that align poorly with those of Dilleniaceae. The purpose of analysis I was to test the monophyly of Dilleniaceae and determine the position of the root within the family. With the caveat that the two nodes just mentioned could be discovered with critical statistical support, analysis II was confined to the 57 ingroup taxa and used sequence data from all four of the loci amplified, with optimal trees rooted at the node specified by analysis I. Maximum parsimony (MP) analyses of separate and combined data partitions for analyses I and II were conducted with PAUP* 4.0b10 (Swofford 2002); only parsimony-informative characters were used. Characters in the MP analyses were all equally weighted and unordered (Fitch 1971). MP analyses employed heuristic searches with 1000 random addition sequence replicates (holding 20 trees at each step), tree-bisectionreconnection (TBR) branch swapping, and ACCTRAN character state optimization; all shortest trees were saved. Branches were collapsed if optimizations of their minimum length equaled 0 (amb). Because PAUP* under the amb option sometimes includes trees a step or two longer than those of optimal score, tree sets obtained from MP analyses were filtered to identify and discard all non-shortest trees. Relative support values for internal branches were estimated with nonparametric bootstrap resampling (Felsenstein 1985) by using 1000 pseudoreplicates with TBR branch swapping and saving all trees. Bootstrap percentages (BP) of 90–100 are here considered strong support, those of 70–89 moderate support, and those of 50–69 poor support. The calculation of decay indices employed AutoDecay, version 5.03 (Eriksson 2001), in conjunction with PAUP* (each constraint tree was evaluated by using the reverse constraint option, with 100 random addition sequence replicates using TBR, and holding 20 trees at each step). For Bayesian phylogenetic analysis, a model of evolution for each data partition was preselected by using the hierarchical likelihood ratio test in MrModeltest, version 2.0 (Nylander 2004). For infA, rps4, and the rpl16 intron, the GTRþG model was selected, and for rbcL, the GTRþIþG model was selected. The inclusion of outgroup sequences did not change the models selected for infA and rbcL. Bayesian posterior probability values were calculated with MRBAYES, version 3.0B4 (Huelsenbeck and Ronquist 2001). Final Bayesian analyses were each conducted with one run of 2 3 106 generations of the Markov chain Monte Carlo algorithm with four chains; chains were sampled every 50 cycles, and branch lengths were saved. Convergence of the chains was determined by plotting ln L scores against generation. Stationarity was assumed when ln L values had stabilized. On the basis of these results, burn-in trees were determined heuristically and discarded. Posterior probability percentages (BI) were determined via the construction of a majority-rule consensus tree in PAUP* by using all post-burn-in trees. Only BI scores 95 were considered significant (Erixon et al. 2003). Congruence between data partitions was assessed both by comparing the bootstrap topologies of individual data parti-

797

tions, searching for topological conflict supported with BP 70 (Lutzoni and Vilgalys 1995; Johnson and Soltis 1999), and through the use of the incongruence length difference (ILD) test (Farris et al. 1994, 1995; implemented in PAUP* as the partition homogeneity test: Mason-Gamer and Kellogg 1996). In analysis II, the ILD test was conducted across the four-way partitioned data set and with every pairwise combination of data partitions. In each instance, 999 random replicates were run to generate the distribution of tree lengths, with each randomized partition analyzed by using a heuristic search with 30 random addition sequence replicates and the MulTrees option not in effect.

Character Evolution Character state reconstructions were performed on the six characters in table 1, which were selected because of their biological importance and prominence in previous classifications of the family. Androecial and gynoecial merosity were scored as unordered, multistate characters. Although the coding disparity between states 1 and 2 for androecial merosity represents an arbitrary deconstruction of a continuum that is without reference to the merosity of other organ whorls in the flower, it is justifiable on the grounds that androecia with more than 200 members have a limited distribution within angiosperms, and certainly within Dilleniaceae. Evaluation of floral symmetry was restricted in scope to its expression in the androecium. Ancestral-state reconstructions used Tetracera as the outgroup because the character state variation of interest is located in the clade containing all other genera of the family. However, the optimization of perforation plate type was conducted by using a hypothetical outgroup with perforation plate type coded as simple. Although the interfamilial relationships of Dilleniaceae are uncertain, candidate sister taxa to Dilleniaceae all possess vessel elements with exclusively simple perforation plates (Caryophyllales: summarized by Stevens [2001–2009]; Vitaceae: Wheeler and Lapasha 1994). Reconstruction of ancestral states was conducted with Mesquite, version 2.5 (Maddison and Maddison 2008), on the topology of the tree with the most optimal likelihood score recovered from Bayesian analysis of combined data from analysis II. All characters were analyzed with parsimony optimization. Floral (androecial) symmetry, showing a complex distribution of states, was also examined by using likelihood optimization, with relative branch length information.

Results Analysis I: rbcL and infA (57 Ingroup Taxa, 4 Outgroup Taxa) Statistics pertaining to sequence characteristics and individual and combined analyses are summarized in table 2. The coding region of the infA gene is intact (i.e., without indels or premature stop codons), which suggests its functionality. Levels of sequence divergence exhibited by infA within Dilleniaceae were similar to those of the two other protein-coding genes (rbcL and rps4; table 2). Strict consensus topologies of the individual infA and rbcL analyses were completely congruent; there were no instances of ‘‘hard’’ topological incongruity (data not shown). Results from the ILD test indicate



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Table 1 Characters Analyzed for the Dilleniaceae Character, states

References

Vessel element perforation plate type 0, scalariform 1, simple Leaf venation architecture 0, tertiary venation strongly percurrent; areoles well developed 1, tertiary venation random to weakly percurrent; areoles not or imperfectly developed Androecial merosity 0, oligomerous to diplomerous relative to the merosity of corolla 1, polymerous relative to the merosity of corolla, to 200 members 2, polymerous in excess of 200 members Gynoecial merosity 0, oligomerous relative to merosity of corolla 1, isomerous relative to merosity of corolla 2, polymerous relative to merosity of corolla Gynoecial synorganization 0, gynoecium with solitary carpel or with multiple, free carpels; without an internal compitum 1, gynoecium of 2 or more fused carpels; apical paracarpous zone present that can function as an internal compitum Floral symmetry 0, polysymmetric 1, monosymmetric

that the infA and rbcL partitions have similar phylogenetic structure (P ¼ 0:829). Dilleniaceae are recovered in the strict consensus topology (fig. 2) as a well-supported (BP and BI both 100; decay index ¼ d18), monophyletic group. Within Dilleniaceae, a well-supported Tetracera clade is sister to a moderately to well-supported clade containing the remainder of the family (BP ¼ 74, BI ¼ 98, decay index ¼ d2). The clade of all other Dilleniaceae consists of a moderately to well-supported subclade of all Neotropical endemic genera sister to a poorly to moderately supported subclade congruent with prior concepts of Dillenioideae. The latter clade

Dickison 1967a, 1979; Baretta-Kuipers 1972; Dickison et al. 1978

Rury 1976; Rury and Dickison 1977; J. W. Horn, personal observations

Hoogland 1952; Kubitzki 1970, 1971; voucher specimens (table A1)

Hoogland 1952; Kubitzki 1970, 1971; voucher specimens (table A1)

Dickison 1968, 1971; Wilson 1974; Endress 1997; J. W. Horn, personal observations

Horn 2007; Hibbertia taxa scored from voucher specimens (table A1)

is resolved into two well-supported sister clades: a Hibbertia clade (in which Adrastaea and Pachynema are embedded) and a subclade containing Dillenia and related Indomalesian genera. Thus, Dilleniaceae consist of four major clades: the Tetracera clade (Tetracera only), the doliocarpoid clade (all Neotropical endemic genera), the hibbertioid clade (Hibbertia s.l.), and the dillenioid clade (Dillenia, Acrotrema, and Schumacheria). Because of the status of Tetracera as sister to other Dilleniaceae, subfamily Delimoideae is paraphyletic, because all prior concepts of this subfamily also include what is here contained in the doliocarpoid clade.

Table 2 Sequence and Analytical Statistics Pertaining to Analyses I and II of Dilleniaceae Phylogeny Analysis I

No. taxa Unaligned length variation (range) Aligned length No. excluded nucleotide positions Pairwise divergence range (%) MP-informative nucleotide positions No. MP trees Length (steps) Consistency index Retention index

Analysis II

infA

rbcL

Combined

infA

rps4

rbcL

rpl16 intron

Combined

61

61

61

57

56

57

57

57

503–555 630

1392 1392

... 2022

503–541 574

572–746 815

1390 1390

872–1257 1487

... 4266

119

0

119

55

183

0

452

690

0–15.27

0–10.21

0–11.13

0–6.52

0–6.04

0–3.74

0–8.71

.03–4.77

108 (21.1%) 36 228 .610 .847

169 (12.1%) 1860 415 .511 .811

277 (14.6%) 181 653 .538 .818

72 (13.9%) 36 136 .640 .901

77 (12.2%) 4 126 .770 .946

113 (8.1%) 72 245 .518 .866

161 (15.6%) 113 333 .634 .914

423 (11.8%) 396 867 .602 .896

Note. MP ¼ maximum parsimony.


Fig. 2 Analysis I: combined rbcL and infA sequence data, rooted with exemplars of Caryophyllales and Vitaceae. Schematic of the strict consensus of 181 maximum parsimony trees (length 653 steps, consistency index ¼ 0.538, retention index ¼ 0.818). Numbers above branches indicate bootstrap support first and posterior probability second; decay indices are placed below branches. Boldface indicates support statistics for the Dilleniaceae clade and the clade of Dilleniaceae exclusive of Tetracera.


800


Analysis II: rbcL, infA, rps4, rpl16 Intron (57 Ingroup Taxa) Statistics pertaining to sequence characteristics and individual and combined analyses are summarized in table 2. Because of the highly degraded nature of the DNA extracted from Schumacheria alnifolia, this species could not be amplified for the rps4 gene and represents the only instance of a taxon missing from a data partition. Results from the ILD test indicate that all four loci share similar phylogenetic signal. The test was conducted across all four data partitions (P ¼ 0:431) and across all pairwise combinations of data partitions (infA 3 rbcL: P ¼ 0:819; infA 3 rps4: P ¼ 0:229; infA 3 rpl16 intron: P ¼ 0:363; rbcL 3 rps4: P ¼ 0:985; rbcL 3 rpl16 intron: P ¼ 0:115; rps4 3 rpl16 intron: P ¼ 0:254). Given adequate support for the basic ingroup topology recovered in analysis I, Tetracera was used to root the phylogeny. The strict consensus topology of this analysis is completely congruent with that found in analysis I, but with moderately increased resolution within generic-level clades, particularly in the case of Dillenia (fig. 3). Significantly, branch support across all measures is markedly increased throughout the phylogeny. As shown in figure 3, nearly all clades, from the generic level to those deepest in the phylogenetic hierarchy, are well supported (mostly with BP and BI of 100); the few exceptions are mentioned below. Within Tetracera, a topology congruent with current concepts of sectional groupings is recovered with moderate support (see ‘‘Discussion’’). The doliocarpoid clade consists of a monophyletic Davilla sister to a clade containing members of the three other Neotropical endemic genera sampled. Curatella and Pinzona, both monotypic, are weakly supported as sister. They, in turn, are sister to a monophyletic Doliocarpus. Schumacheria is sister to the remaining dillenioid clade, containing a paraphyletic Dillenia, into which Acrotrema costatum is embedded. Acrotrema costatum and the Malagasy/Sri Lankan Dillenia triquetra are poorly supported as sister and are in turn sister to the other Dillenia species sampled. Within this core clade of Dillenia (BP ¼ 60, BI ¼ 100, decay index ¼ d2), the sampled species resolve into two well-supported clades. The hibbertioid clade consists of a paraphyletic Hibbertia, into which the satellite genera Adrastaea and Pachynema are embedded. Four well-supported lineages are resolved within the hibbertioid clade. A monophyletic Pachynema is embedded within one of these four clades, here called the Pachynema clade, which otherwise contains the only two Hibbertia species with uniformly photosynthetic aerial stems (i.e., like Pachynema) as successively sister to Pachynema. The Pachynema clade is sister to a large and structurally diverse clade, here called Hibbertia I, in which species relationships are poorly resolved. A clade inclusive of the two clades just mentioned is sister to another clade containing two major lineages. This clade consists of the monotypic Adrastaea (indicated here by its combination in Hibbertia, H. salicifolia), sister to a clade of Hibbertia species here termed Hibbertia II.

Character Evolution Perforation plate type optimizes onto the phylogeny with three state transitions, and four reconstructions are equally parsimonious. A polymorphic condition of both simple and

scalariform perforation plates (as is present in the woods of Tetracera and the doliocarpoid clade) is reconstructed as ancestral for Dilleniaceae, with a subsequent loss of simple perforation plates in the dillenioid/hibbertioid clade in the DELTRAN optimization (fig. 4). Two other most parsimonious reconstructions also indicate that simple perforation plates are lost within the family. The ACCTRAN optimization indicates that scalariform perforation plates are ancestral for the family, with the polymorphic condition present in Tetracera and the doliocarpoid clade because of independent gains of simple perforation plates in these groups. Leaf venation architecture shows a single state transition to a less organized venation pattern at the basal node of the hibbertioid clade (fig. 5A). Androecial merosity shows six state transitions: highly polymerous androecia are gained at the node of the clade inclusive of Dillenia and Acrotrema (then lost in Acrotrema) or else gained independently in D. triquetra and the clade of the other Dillenia species (fig. 5C). Gynoecial merosity optimizes with 10 state transitions; polymerous gynoecia are gained only in the clade of Dillenia exclusive of D. triquetra (fig. 5C). Gynoecia synorganized with an internal compitum are independently gained in the Curtella/Pinzona clade and the Dillenia/Acrotrema clade (fig. 5B). Androecial monosymmetry is gained independently in Schumacheria and the Hibbertia I clade (fig. 6B). Within Hibbertia, parsimony optimizations (six steps) all favor multiple, independent gains. An asymmetry likelihood ratio test for this character rejected the one-parameter model in favor of a two-parameter model of evolution (2ln L ¼ 7:174, P < 0:01). Under the two-rate model (AsymmMk, in Mesquite), monosymmetry is gained at a critical proportional likelihood (0.8914) at the base of the Hibbertia I clade, with subsequent, mostly independent, reversions back to polysymmetry (fig. 6B).

Discussion Changing Concepts of Character Evolution in Dilleniaceae Evolutionary trends in angiosperms (Bessey 1915; Bailey 1953, 1957; Eames 1961; Cronquist 1988; Takhtajan 1991) played a prominent role in establishing previous inter- and infrafamilial phylogenetic hypotheses for Dilleniaceae. Dilleniaceae collectively share a suite of classically ‘‘primitive’’ character states with magnoliid dicots, such as polyandry, apocarpy, leaves with poorly organized venation, and secondary xylem that includes long, narrow vessel elements with strongly oblique, scalariform perforation plates. Yet because they are also distinct from magnoliids on the basis of triaperturate pollen and centrifugal stamen initiation, they were placed as the earliest family within a major group of (eu)dicots that was largely defined by having centrifugal stamens (Dilleniidae). This key position accorded Dilleniaceae in intuitive phylogenetic classifications strongly influenced subsequent hypotheses of infrafamilial relationships and evolution, because ideas of character state polarity within Dilleniaceae thus became implicitly informed by evolutionary trends. Dickison (1967a, 1968, 1970b) pioneered evolutionary analysis within Dilleniaceae by interpreting his numerous original observations of anatomy and morphology in the light of the then well-accepted evolutionary trends in angio-


Fig. 3 Analysis II: combined rbcL, infA, rps4, rpl16 intron sequence data, rooted with Tetracera (ingroup only). Strict consensus of 396 maximum parsimony trees (length 867 steps, consistency index ¼ 0.602, retention index ¼ 0.896). Numbers above branches indicate bootstrap support first and posterior probability second; decay indices are below the branches.


Fig. 4 Vessel element evolution in Dilleniaceae: DELTRAN optimization of perforation plate–type evolution. Quantitative data shown in corresponding bar graphs are taken from Dickison (1967a, 1979), Baretta-Kuipers (1972), and Dickison et al. (1978). Thin vertical bars indicate range of data (where reported), bold vertical highlights indicate a reported ‘‘frequent range,’’ and horizontal dashes indicate a mean value for reported data. Black lines indicate species-specific data, whereas gray ones indicate a summary of data reported for a particular genus. 802


Fig. 5 Parsimony reconstructions of ancestral states for structural characters of Dilleniaceae. A, Leaf venation architecture. B, Gynoecial synorganization. C, Mirror trees showing optimizations for androecial merosity (left) and gynoecial merosity (right). 803


Fig. 6 A, Schematic of phylogram of most optimal tree discovered in Bayesian analysis of four-gene data set. B, Maximum likelihood optimization of (floral) androecial symmetry onto topology, with relative branch lengths as shown in A.


HORN—PHYLOGENETICS OF DILLENIACEAE sperm structure put forth by I. W. Bailey and his students (Frost 1930; Bailey 1944, 1957) and by Eames (1961). Using data from wood anatomy and floral structure, Dickison substantiated the long-held view of Dillenioideae as the most primitive subfamily. Within Dillenioideae, Dickison and others identified many species of Hibbertia as possessing the largest number of putatively unspecialized character states within the whole family (Dickison 1969, 1970b; Stebbins and Hoogland 1976; Rury and Dickison 1977). Rury and Dickison (1977) supplemented the hypothesis of Hibbertia as the least specialized genus of Dilleniaceae by using leaf venation architecture, justifying this idea by interpreting their observations in the context of hypotheses of evolutionary trends in leaf architectural specialization presented by Hickey (1971), Wolfe (1973), and Hickey and Wolfe (1975). On the basis of Eames’s (1961) views of generalized trends in the evolution of carpels, Dickison (1968, 1970b), Kubitzki (1970, 1971), and Wilson (1974) suggested Tetracera as the least specialized genus within Delimoideae, on account of its seemingly more conduplicate carpel morphology and numerous ovules. Although the character-based trends mentioned above are now largely discredited as paradigms of evolution (Endress 2002; Soltis et al. 2005), their proponents were correct in locating among such characters many of the functionally significant aspects of angiosperm evolution. Trend-based characters therefore remain of interest, because studies revealing instances of unusual evolutionary directions and unexpected evolutionary lability in these characters have been critical to developing an understanding of angiosperm structure in a broader biological context (Kuzoff et al. 2001; Endress 2002; Jabbour et al. 2008; Preston and Hileman 2009). Below, I discuss the evolution of six trend-based characters that played a significant role in the development of evolutionary hypotheses for Dilleniaceae. Although the novel phylogenetic results of this study necessitate relatively minor classificatory changes, the albeit moderately supported relationship of Tetracera as sister to all other Dilleniaceae leads to substantially revised perspectives on character evolution within the family. The evolution of each character shows a direction of polarity or degree of lability that is surprisingly unorthodox. Wood anatomy: vessel element. Critically supporting the postulation that Dillenioideae (the dillenioid/hibbertioid clade of this study) are relatively less specialized than other members of the family was the dogmatic idea that perforation plate evolution is irreversible (Bailey and Tupper 1918; Frost 1930; Bailey 1944, 1957; Takhtajan 1991; Carlquist 2001). The logic of this assumption is that simple perforation plates, once gained within a lineage, would not be lost, because they confer greater hydraulic conductivity within a vessel relative to scalariform perforation plates. Counter to this, reconstructions of perforation plate–type evolution within Dilleniaceae indeed suggest that simple perforation plates might have been lost within the family (fig. 4), although one of the four most parsimonious reconstructions suggests an alternative scenario. Other studies demonstrate the reversibility of this ‘‘irreversible’’ character more conclusively (Baas and Wheeler 1996; Herendeen et al. 1999; Baas et al. 2000). The wood anatomy of Dilleniaceae provides another example of unusual evolutionary directions. The tracheid-like vessel elements of Schumacheria, considered to be among the most

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classically ‘‘primitive’’ of angiosperms (Dickison 1967a; Takhtajan 1997), are clearly a derived type within Dilleniaceae. Heuristic correlation of quantitative data on vessel element length, width, and perforation plate bar number with the phylogeny suggests a derived increase in both vessel element length and perforation plate bar number in Schumacheria (fig. 4). Although a clear hypothesis of the functional significance of both the above examples remains out of reach, contemporary studies on wood ecophysiology demonstrate considerable complexity in wood anatomical structure–function relationships (Zimmerman 1983; Hacke and Sperry 2001; Sperry 2003). Important recent additions to the well-known correlates of vessel dimensions and perforation plate type with conductance and safety from cavitation are the total area of intervessel pits and the porosity of their pit membranes (Sperry et al. 2007; Christman et al. 2009). Vessels with a relatively greater intervessel pit area have a greater probability of having a rare ‘‘leaky’’ pit, thus increasing chances of cavitation. These traits of dilleniaceous woods remain little investigated and may be informative in resolving the unorthodox aspects of xylem evolution within the family. Among subfamilial clades, an exclusively ecological perspective cannot satisfactorily account for these features. Leaf venation architecture. Evolutionary trends in leaf venation architecture evolution proposed by Hickey and Wolfe (1975) and perpetuated by Cronquist (1988) and Takhtajan (1991) suggest that, in the absence of overt ecological specialization, poorly organized venation architecture with relatively undifferentiated orders of venation characterize primitive lineages, whereas well-organized and well-differentiated leaf venation architectures are derived. Rury and Dickison (1977) noted that leaves of Dilleniaceae show a high degree of diversity with respect to Hickey and Wolf’s trends. They observed, however, that most of this variation occurs within Hibbertia and does not overlap with that in other Dilleniaceae. In Hibbertia leaves, secondary venation is very rarely more or less parallel, rigidly percurrent tertiary venation is absent, and areolation is absent or, rarely, poorly developed. Leaves of other Dilleniaceae are remarkable in both the homogeneity and the high degree of organization of their venation architecture (Rury 1976). They have parallel secondaries, rigidly percurrent tertiaries, and higher orders of venation forming well-developed areoles that are often clearly oriented to the secondary and tertiary venation. In Dilleniaceae, the poorly organized venation of the leaves of Hibbertia is derived, while highly organized leaf venation, characterizing the rest of the family, is plesiomorphic (fig. 5A). A possible explanation for this phenomenon is that the leaves of Hibbertia represent homeotic inflorescence bracteoles (prophylls; Horn 2007; see ‘‘Hibbertioid Clade’’). Floral evolution. The extraordinarily large numbers of organs present in the flowers of most Dillenia species, as well as those of a few species of Hibbertia and Tetracera, represent a derived condition within the family (fig. 5C). In the core clade of Dillenia (i.e., the clade exclusive of D. triquetra), highly polymerous androecia and polymerous gynoecia are likely correlated with the spectacular floral gigantism for which this genus is renowned. Dillenia flowers may show a great deal of architectural complexity that belies the relative simplicity of their bauplan (Endress 1997). Anthetic flowers of many species within the core Dillenia clade exhibit heteranthery to a remarkable de-


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gree, such that two distinct size classes of stamens occur within the androecium. The most pronounced manifestation of this condition occurs in the largest-flowered species of the genus, in which an inner group of large stamens interpose between the outwardly arching stylodia of the polymerous gynoecium. Peripheral to this unit are numerous short stamens (and sometimes also staminodes), which often contrast in color with the inner stamens and gynoecium. This two-tiered floral architecture gives rise to an elaborate pollination mechanism, in which large Xylocopa bees circle around the outer group of short ‘‘feeder’’ stamens, buzzing to collect pollen while concomitantly having to squeeze beneath the canopy of stylodia. In this process, pollen from the inner stamen set is liberated onto the bee’s back and side (roundabout flowers; Endress 1997). The precision of this mechanism shows many parallels with that in monosymmetric flowers, insofar as it constrains the approaches by which a pollinator can successfully manipulate the flower. All the more remarkable, the specialized architectural features of Dillenia flowers are closely linked to the developmental basis of the extreme polyandry exhibited in this genus. Endress (1997) relates heteranthery to the process of centrifugal stamen inception, which, although prevalent within Dilleniaceae (Corner 1946; Tucker and Bernhard 2000), is unusually protracted in Dillenia flowers. In the context of the phylogenetic hypothesis presented here, giant roundabout flowers occur in both major clades of the core Dillenia clade (amplexicaul clade: D. alata and D. philippinensis; nonamplexicaul clade: D. retusa and D. indica; see ‘‘Dillenioid Clade’’), although androecia with stamens of only one type occur in the clade of D. hookeri and D. parkinsonii, suggesting that floral architecture in Dillenia may be evolutionarily rather labile. Although roundabout flowers are frequent in Dillenia, androecial architecture is diverse in the genus (Hoogland 1952; Endress 1997), and further study is required to elucidate the evolutionary history of both heteranthery and the complex pollination mechanisms with which it is associated. Nevertheless, it is clear that many of the largest-flowered Dillenia species, far from being ‘‘giant buttercups,’’ as they were dubbed by Corner (1940), represent instances of floral specialization through gigantism. Because Dilleniaceae have often been regarded as an apocarpous family par excellence, it is notable that syncarpous gynoecia, all with an internal compitum (an internal pollen tube transmitting tract shared among carpels of a flower; Endress 1994), are documented in four genera (these have hemisyncarpous gynoecia, whereas other genera are at least structurally apocarpous; Dickison 1968, 1971; Wilson 1974; Endress 1997; Horn 2007). A synorganized gynoecium with an internal compitum has two independent origins when reconstructed: one diagnosing the Curatella/Pinzona clade, the other diagnosing the Acrotrema/Dillenia clade (fig. 5B). Beyond fusion, an internal compitum enables all carpels within a gynoecium to function as a unit during the process of fertilization. Pollen tubes may grow among carpels, potentially maximizing the reproductive success of the gynoecium as a whole (Endress 1982). Thus, Endress (1994) suggests that an internal compitum is perhaps as significant an innovation in angiosperm evolution as angiospermy itself. Floral monosymmetry, another classic ‘‘advanced’’ angiosperm trait (Bessey 1915; Cronquist 1988), is characteristic of

many Hibbertia species, Didesmandra, and Schumacheria, where it is expressed principally in the androecium (fig. 7B; Wilson 1965, 1974; Dickison 1970b; Tucker and Bernhardt 2000). Monosymmetric flowers constrain the approach of a potential pollinator to a single orientation, ensuring that anthers and stigmas are in maximal contact with the pollinator. In the context of the phylogeny, there are independent origins of floral monosymmetry in Schumacheria and the Hibbertia I clade (fig. 6B). Within the Hibbertia I clade, species relationships are poorly resolved, so no conclusion can yet be drawn regarding the complexity of floral-symmetry evolution in this group. Yet even this preliminary evidence suggests that floral symmetry is unusually labile within Dilleniaceae; this is noteworthy, given

Fig. 7 SEM images of Dilleniaceae flowers (calyx and corolla removed). A, Flower of Curatella americana immediately before anthesis; stamens in front view removed to show carpels. Note annuliform, peltate stigmas with even margins. Scale bar ¼ 2 mm. B, Anthetic flower of Schumacheria castaneifolia. Androecium is monosymmetric, with the stamen filaments fused into a single ligulate fascicle. Gynoecium has three carpels; stylodia have minute, punctiform stigmas. Scale bar ¼ 2.5 mm.


HORN—PHYLOGENETICS OF DILLENIACEAE both the size of the family (;500 spp.) and the rarity of monosymmetric flowers among early core eudicot lineages.

Tetracera This genus of ;50 species is distinguished from other Dilleniaceae by its strongly fimbriate or lacerate arils (Kubitzki 1970; Horn 2007). The most recent taxonomic conspectus of Tetracera (Kubitzki 1970) recognizes two sections within the genus, the circumscriptions of which are corroborated by the results of this study. Tetracera masuiana, the only taxon sampled of the exclusively paleotropical sect. Akara Kubitzki, is sister to clade containing all the other Tetracera species sampled. This moderately supported clade (fig. 3), consisting entirely of species currently placed in sect. Tetracera, includes taxa formerly placed in the segregate genera Delima L. (T. scandens) and Empedoclea A.St.-Hil. (T. empedoclea). Perhaps the most remarkable feature of Tetracera is its pantropical distribution, which is largely coincident with the distribution of the family as a whole (fig. 1A), excepting temperate Australia. The other three major clades of the family have mostly nonoverlapping distributions (fig. 1). Given that Tetracera is sister to the remaining Dilleniaceae, which show a fundamental split between the exclusively Old World dillenioid/ hibbertioid clade and the exclusively Neotropical doliocarpoid clade, a knowledge of the biogeographic history of Tetracera is key to understanding the broader biogeographic history of Dilleniaceae and, in particular, their area of origin. General poor resolution within Tetracera, however, currently hinders any attempt at a comprehensive biogeographic analysis of the family.

Doliocarpoid Clade This clade contains all the sampled genera that are endemic to the Neotropics: Davilla, Doliocarpus, Curatella, and Pinzona. The removal of Tetracera from this assemblage of genera creates a more biogeographically and morphologically cohesive group. In contrast to the rest of the family, prophylls have no role in organizing the structure of the inflorescences of the doliocarpoid clade; prophylls are entirely suppressed or absent (or, very rarely, vestigial in a few large-flowered species of Davilla, where they do not contain a branch in their axil). The consequence of this is that cymose branching (i.e., branching exclusively from the axil of a prophyll; Weberling 1989) never occurs in the inflorescences of the doliocarpoid clade. Inflorescences in this clade are panicles (in the sense of Troll 1964; Weberling 1989) or impoverished variants of panicles (botryoids—unbranched, multiflowered, determinate inflorescences—or, rarely, solitary, terminal flowers; Kubitzki 1971; Horn 2007). Cymose (principally cincinnate) inflorescences or partial inflorescences occur in all other genera of Dilleniaceae (Wagner 1906a, 1906b; Kubitzki 1970; Stebbins and Hoogland 1976; Corner 1978; Horn 2007; descriptions of racemes in Acrotrema [Dickison 1971] and Dillenia [Hoogland 1952] are misinterpretations; these inflorescences are cincinni). The only potential exceptions involve species with solitary or very minimal inflorescences. Another potential synapomorphy for the doliocarpoid clade is its possession of a peltate stigma with an even, annuliform margin (fig. 7A). This stigma type is sharply distinct from those of other Dilleniaceae, which have minute, puncti-

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form stigmas that are not differentiated in shape from the stylodia (figs. 7B, 8B). Some Neotropical Tetracera species do have somewhat peltate stigmas, but in these species the tissue at the apex of each stylodium is splayed flat, and the margin of the stigmatic region is irregular and jagged. The doliocarpoid clade is also characterized by the stabilization of two ovules per carpel. While individual species in other parts of the family may possess two ovules per carpel, ovule number is highly variable outside of the doliocarpoid clade, ranging from 2(?) to 20 in Tetracera, from 1 to 25 in the hibbertioid clade, and from 1 to 80 in the dillenioid clade (Dickison 1968; Veillon 1990). A new finding of this study is that in the doliocarpoid clade, one of the two basal, erect ovules is apotropous (abaxially curved) while the other is epitropous (adaxially curved). Rarely, a few flowers on a given individual may vary with respect to this character state, having ovules curved in a uniform direction. In other Dilleniaceae with only one or two ovules per carpel, the ovules are always apotropous. Within the doliocarpoid clade, the subclade containing Doliocarpus and the monotypic genera Curatella and Pinzona also has diagnostic inflorescence features that are probable synapomorphies. In this group, plants exhibit monopodial growth and inflorescences are always axillary and ramiflorous. Old, defoliated nodes produce multiple inflorescence flushes by the formation of proliferation buds, up to two flushes per year for several years (Croat 1978). Ramiflorous inflorescences are also found in a few deciduous species of Dillenia that bear flowers on lateral short shoots before foliage production (Hoogland 1952). Although these Dillenia species were not sampled in the phylogenetic analyses, they almost certainly exhibit an independent derivation of ramiflory.

Dillenioid Clade This clade, containing the genera Acrotrema, Dillenia, and Schumacheria, is diagnosed by the possession of completely amplexicaul petiolar wings and profusely mutilacunar nodes (7–27 leaf traces and gaps; Dickison 1969, 1971). These putative synapomorphies each show a single instance of a reversal back to the plesiomorphic state: one clade of Dillenia is characterized by its nonamplexicaul petiole wings, and the Sri Lankan species of Acrotrema (not sampled here) have trilacunar nodes (Dickison 1971). The phylogenetic position of Schumacheria, recently the source of confusion (cf. Hilu et al. 2003), is here clarified. This genus is firmly embedded within Dilleniaceae, well supported as sister to other members of the dillenioid clade. A close relationship between Schumacheria and Theaceae, suggested by Hilu et al. (2003), is not supported by the results of this study. Likely also a member of this clade is Didesmandra, a monotypic genus endemic to Sarawak, Borneo. Although not sampled as a part of this study, it possesses both of the putative structural synapomorphies of this group (Hoogland 1952; nodes 17 : 17, Dickison 1969). Didesmandra has always been associated with this grouping of genera, in particular with the Sri Lankan endemic Schumacheria, with which it shares monosymmetric flowers, one ovule per carpel, and (mostly) 4-aperturate pollen (Dickison 1967b, 1968; Dickison et al. 1982). All of these features are unique to these two genera within the dillenioid clade; the last is also unique within the family.


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Fig. 8 SEM images of flowers of Pachynema clade of Hibbertia. All flowers are oriented such that the top of the photo is adaxial. A, Preanthetic flower of Hibbertia conspicua, showing an outer whorl of seven stamens (median stamen adaxial), with two large staminodes in the transverse plane of the flower (calyx and corolla removed). Scale bar ¼ 0.5 mm. B, Anthetic flower of H. conspicua, with punctiform stigmas and two carpels in median plane of the flower (calyx and corolla removed). Scale bar ¼ 1 mm. C, Anthetic flower of Pachynema dilatatum (corolla removed). Scale bar ¼ 2 mm. D, Anthetic flower of Hibbertia goyderi, with an outer corona of filamentous staminodes, an outer whorl of seven fertile stamens, and an inner whorl of two fertile stamens in the transverse plane of the flower (calyx and corolla removed). Scale bar ¼ 2 mm.

The relationship between Dillenia and Acrotrema requires further investigation. Interestingly, the derivation of a hemisyncarpous gynoecium is a synapomorphy for the clade containing these two genera. What has hampered the detection of a close relationship between Dillenia and Acrotrema in the past—and what makes the discovery of close relationship between the two particularly significant here—is that Acrotrema species are rosette-forming herbs that produce only

limited amounts of secondary xylem in their rhizomes (Dickison 1971). Dillenia species, by contrast, range from large shrubs to, most commonly, sizeable trees (Hoogland 1952).

Hibbertioid Clade This clade, consisting of a paraphyletic Hibbertia—with Adrastaea and Pachynema nested within it—shows the great-



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Table 3 Outline of Classification of Dilleniaceae Dilleniaceae Salisb., Parad. Lond. 2(1): ad t. 73 (1807), nom. cons. (‘Dilleneae’) Soramiaceae Martinov (1820) Hibbertiaceae J. Agardh (1858) Subfamily Delimoideae Burnett, Outl. Bot.: 836. (1835) (‘Delimidae’) Tetracera L. Subfamily Doliocarpoideae J.W. Horn, subfamilius nova; typus: Doliocarpus Rol. Inflorescentia plerumque paniculatis, ramificans cymosa absentis. Stigma infudibuliformis, margo apicalis annuliformis. Ovula in quoque carpellum duo collateralia, basi; unus usitas epitropa, ceterus apotropa. Davilla Vand. Curatella Loefl. Pinzona Mart. & Zucc. Doliocarpus Rol. Neodillenia Aymard (provisional placement) Subfamily Hibbertioideae J.W. Horn, subfamilius nova; typus: Hibbertia Andrews Folia per venatio tertiarius fortuitus ut infirme percurrens. Areola non vel trunco effectus. Nodi uni vel trilacunae. Hibbertia Andrews Subgenus Pachynema (R. Br. ex DC.) J.W. Horn, comb et stat. nov. Basionym Pachynema R.Br. ex DC. Syst. Nat. (de Candolle) 1: 411. 1817 Subgenus Hemistemma (DC. in Thou.) J.W. Horn, comb et stat. nov. Basionym: Hemistemma DC. in Thou. Hist. Veg. Isles Austr. Afr. ed. 2 t. 30 (1805) Subgenus Adrastaea (R. Br. ex DC.) J.W. Horn, comb et stat. nov. Basionym: Adrastaea DC. Syst. Nat. (de Candolle) 1: 424. 1817 Subgenus Hibbertia (Andrews) J.W. Horn, comb et stat. nov. Basionym: Hibbertia Andrews Bot. Rep. t. 126, 472 (1800) Subfamily Dillenioideae Burnett, Outl. Bot.: 836 (1835) (‘Dillenidae’) Schumacheria Vahl Didesmandra Stapf (provisional placement) Acrotrema Jack Dillenia L.

est diversity with respect to floral bauplan, leaf structure, and ecological preferences of the four major clades of the family (Stebbins and Hoogland 1976; Rury and Dickison 1977; Tucker and Bernhardt 2000). Stebbins (1974; also Stebbins and Hoogland 1976) considered Hibbertia to be among the most structurally and ecologically diverse angiosperm genera and an outstanding example of an adaptive radiation. Previous studies (Gilg and Werdermann 1925) suggest that New Caledonian species are likely ‘‘primitive,’’ because many are among the species with both the largest flowers (and the great-

est number of stamens) and the largest leaves (with brochidodromous venation) in the genus. The results of this study demonstrate that relationships within the genus are significantly different from those suggested by all previous classifications and that four major groups should be recognized within Hibbertia (fig. 3). Further, Pachynema and Adrastaea should be included within Hibbertia. Species richness among these four clades is strongly unequal: Hibbertia I (;160 spp.) and Hibbertia II (;80–90 spp.) contain the preponderance of species within the genus (Horn

Table 4 Transfer of Pachynema R.Br. ex DC. Epithets into Hibbertia Andrews Hibbertia complanata (R.Br. ex DC.) J.W. Horn, comb. nov. Basionym: Pachynema complanatum R.Br. ex DC., Syst. Nat. (de Candolle) 1: 412 (1817) Hibbertia cravenii J.W. Horn, nomen novum Synonym: Pachynema hooglandii Craven & Dunlop, Austral. Syst. Bot. 5(4): 488 (1992) Not Hibbertia hooglandii J.R. Wheeler, Nuytsia 7(1): 69, fig. 1 (1989) Hibbertia dilatata (Benth.) J.W. Horn, comb. nov. Basionym: Pachynema dilatatum Benth., Fl. Austral. 1: 48 (1863) Hibbertia haplostemona J.W. Horn, nomen novum Synonym: Pachynema diffusum Craven & Dunlop, Austral. Syst. Bot. 5(4): 493 (1992) Not Hibbertia diffusa R.Br. ex DC., Syst. Nat. (de Candolle) 1: 429 (1817) Hibbertia juncea (Benth.) J.W. Horn, comb. nov. Basionym: Pachynema junceum Benth., Fl. Austral. 1: 47 (1863) Hibbertia praestans (Craven & Dunlop) J.W. Horn, comb. nov. Basionym: Pachynema praestans Craven & Dunlop, Austral. Syst. Bot. 5(4): 495 (1992) Hibbertia sphenandra (F. Muell. & Tate) J.W. Horn, comb. nov. Basionym: Pachynema sphenandrum F. Muell. & Tate, Trans. & Proc. Roy. Soc. South Australia 5: 79 (1882)


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2007). Hibbertia I contains all sampled species with monosymmetric androecia; and/or secund, cincinnate (boragoid) inflorescences; and/or multiradiate to peltate trichomes; and/or ericoid leaves with 1 : 1 nodal anatomy and sclerified adaxial epidermal cells (Gilg and Werdermann 1925; Dickison 1970a; Horn 2007). Species in the Hibbertia II clade always have solitary, polysymmetric flowers and leaves with mostly 3 : 3 nodal anatomy, uniformly without sclerified epidermal cells. Hibbertia salicifolia, sometimes recognized as the sole species of Adrastaea, is sister to the Hibbertia II clade. It is characterized by a unique floral bauplan, the outstanding features of which are an obdiplostemonous androecium and a bicarpellate gynoecium (Tucker and Bernhard 2000; Horn 2007). Of particular interest is the small (7 spp.) arid-tropical Australian genus Pachynema, which is clearly embedded within a clade (Pachynema clade) that is sister to the Hibbertia I clade. This result is basically concurrent with previous suggestions that Pachynema, with its photosynthetic, sometimes flattened and phyllocladous, aerial shoots and ‘‘foliage’’ consisting almost exclusively of tiny, linear bracts and prophylls, is an extreme, xeromorphic offshoot of Hibbertia (Dickison et al. 1978; Craven and Dunlop 1992). Pachynema, as circumscribed, appears to be a monophyletic group (both of Craven and Dunlop’s [1992] sections are represented in this study), but it has been considered distinct from Hibbertia because of its swollen, bottle-shaped stamen filaments. Shared similarities with the two successively sister Hibbertia species of the Pachynema clade, H. conspicua and H. goyderi, are far more extensive. Most members of the Pachynema clade (including all sampled in this study) share a distinctive fertile androecial organization, with an outer whorl of typically seven (8–10) stamens and an inner whorl of two stamens (or large staminodes) in the transverse plane of the flower (fig. 8; the two carpels are median). This androecial organization is unique in Dilleniaceae and perhaps also in angiosperms as a whole. All members of the Pachynema clade also share the extremely distinctive life form of having photosynthetic, hapaxanthic, annual or short-lived shoot systems as their only aerial axes (with 1–5-mm-long bracts and prophylls), which, upon analysis, are predominantly all inflorescence (Wagner 1906b; Craven and Dunlop 1992; both for Pachynema only). The aerial shoot systems of the Pachynema clade contrast sharply with those of all other members of the family (perhaps excepting Acrotrema), which are distinctly pleonanthic and basically nonphotosynthetic, as all but the primary shoots are covered with bark (i.e., they are typical woody eudicots). The assertion that the aerial shoot systems of Pachynema represent inflorescences is strengthened with the addition of H. goyderi and, particularly, H. conspicua, which is sister to the remaining Pachynema clade. The inflorescence of H. conspicua is a thyrsoid (determinate thyrse), with side branches composed

exclusively of one-flowered, 2-prophyllate modules. These side branches are (branched) cincinni and are fundamentally like those of the dillenioid clade (and other Hibbertia spp.; Wagner 1906a), with one of the two prophylls displaced (recaulescent) onto the sylleptic branch (peduncle) borne in its axil. In Dilleniaceae exclusive of the hibbertioid clade, recaulescent foliar appendages are restricted in occurrence to the inflorescence (where they occur in Acrotrema spp., Didesmandra, Dillenia spp., Schumacheria, and Tetracera spp.).

Classification The robustly supported phylogenetic hypothesis of Dilleniaceae presented here (table 3) necessitates few but important changes to the classification of the family. As with any classification, arbitrary decisions must be made that require further justification. Generic circumscriptions within Dilleniaceae have essentially remained stable for at least the past 50 yr; these are maintained unless there is strong support for an alternative approach. Hence, Acrotrema, although it is resolved within Dillenia, is retained as distinct from Dillenia because the resolution is insufficiently supported. The four major subclades within the hibbertioid clade are well supported here and in a previous study (Horn 2005). Thus, Pachynema is included within Hibbertia. New combinations for Pachynema epithets into Hibbertia are provided in table 4. Adrastaea salicifolia is included within Hibbertia, in agreement with Stanley (1983) and Hnatiuk (1990). Hibbertia, in this slightly broadened circumscription, is diagnosable from other Dilleniaceae by its poorly organized leaf venation, in combination with its unilacunar, one-trace or trilacunar, three-trace nodal anatomy.

Acknowledgments I extend my gratitude to Paul S. Manos, who advised this study, in addition to A. Jonathan Shaw, Kathleen Pryer, Bruce Kirchoff, and V. Louise Roth, to whom I am grateful for guidance. W. C. Dickison provided early encouragement. Staff of the Western Australian Herbarium, the Royal Botanic Gardens Sydney, the Queensland Herbarium, the Northern Territory Herbarium, and the IRD Centre in Noumeá, New Caledonia, graciously enabled fieldwork. My thanks to the curatorial staff at NY, MO, and US for generously permitting sampling of material critical to this study. W. Burk and K. Wurdack assisted with locating obscure literature. Members of the Manos Lab provided moral support, helpful discussion, and advice. Funding for this research was provided in part by NSF award DEB 0105089 to P. S. Manos, in addition to support from the A. W. Mellon Foundation, the Graduate School of Duke University, and Sigma Xi.

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