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Systematics and Phytogeography |
Institute of Systematic Botany, The New York Botanical Garden, Bronx, New York 10458 USA; Institute of Plant and Microbial Biology, Academia Sinica, Taipei, Taiwan 115, Republic of China; Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado 80309-0334 USA; Laboratory for Molecular Systematics, Swedish Museum of Natural History, P.O. Box 50007, SE 104–05, Stockholm, Sweden; Department of Phanerogamic Botany, Swedish Museum of Natural History, P.O. Box 50007, SE-106 91, Stockholm, Sweden
Received for publication March 8, 2006. Accepted for publication December 20, 2006.
ABSTRACT
The Lecythidaceae comprise a pantropical family best known for the edible seeds of the Brazil nut (Bertholletia excelsa) and the cannon-ball tree (Couroupita guianensis), which is planted as a botanical curiosity in subtropical and tropical gardens. In addition, species of the family are often among the most common in neotropical forests, especially in the Amazon Basin. The Brazil nut family is diverse and abundant in the Amazon and is considered to be an indicator of undisturbed or scarcely disturbed lowland forests; thus, what is learned about its evolution, ecology, and biogeography may suggest similar patterns for other Amazonian tree families. We used combined data sets derived from the ndhF and trnL-F genes to elucidate relationships of genera in both the Old and New Worlds that have been associated with Lecythidaceae. Our molecular tree agrees with the recognition of Napoleonaeaceae and Scytopetalaceae. Within the Lecythidaceae, there is molecular support for recognizing three subfamilies: Foetidioideae, Planchonioideae, and Lecythidoideae. We then focused on genera of the Lecythidoideae and found support for recognizing Allantoma (when the actinomorphic-flowered species of Cariniana are included in it), Grias, Gustavia, Corythophora, Couratari, and Couroupita, but conclude that Cariniana, Lecythis, and Eschweilera are not monoyphyletic. Because the position of the monotypic Bertholletia excelsa in relation to the other zygomorphic-flowered genera is not resolved, we are not able to comment on its generic relationships.
Key Words: Bertholletia excelsa • Brazil nut • Lecythidaceae • ndhF • phylogeny • trnL-F • tropical trees
Lowland Amazonia is one of the richest places in the world for different kinds of trees (Gentry, 1988
). In its forests, as many as 280–300 species with diameters greater than 10 cm can occur in a hectare (Gentry, 1988
; Oliveira and Mori, 1999
) causing biologists to ask, "Why so many species in a single place?" This is a question that has occupied the thoughts of tropical biologists since the 18th century when they first started exploring the Amazon for plants and animals. Today, knowledge of evolutionary relationships among and within families of trees based on molecular data has begun to provide insights into the evolution of tropical trees. For this study, we chose one of the symbols of Amazonian forests, the Brazil nut family (Lecythidaceae), to begin to address its evolutionary relationships using data from gene sequences. Our first goal was to examine the classification of the family, which is based on anatomical, cytological, and morphological evidence because only through a classification that reflects true relationships can we answer evolutionary, ecological, and biogeographic questions.
Molecular studies indicate that the Lecythidaceae, together with Napoleonaeaceae and Scytopetalaceae, are a monophyletic group in the Ericales (Morton et al., 1997
; Anderberg et al., 2002
; Schönenberger et al., 2005
). Their monophyly is strongly supported, but the exact systematic position of the group is not fully understood.
The Lecythidaceae and its allies comprise a pantropical clade of trees (Mori, 2004
) (Table 1). In The Families and Genera of Vascular Plants (Kubitzki, 2004
), the clade is divided into three families: the Napoleonaeaceae (Prance, 2004
), Scytopetalaceae (Tsou, 1994b
; Appel, 1996
, 2004
), and the Lecythidaceae (Prance and Mori, 2004
). The Lecythidaceae include three subfamilies, the Foetidioideae, Planchonioideae, and the Lecythidoideae (Prance and Mori, 2004
). In Table 1, we provide a summary of the Lecythidaceae and its allies, which includes a list of the genera placed in their respective families and subfamilies. It is this classification scheme that we will discuss in this paper.
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). Neotropical Lecythidaceae are best known for the Brazil nut of commerce (Bertholletia excelsa Bonpl.), the seeds of which are harvested from what seem to be naturally occurring groves of trees throughout Amazonia that may have been enriched by Amerindians. The cannon-ball tree (Couroupita guianensis Aubl.), frequently planted in tropical and subtropical botanical gardens because of its showy and aromatic flowers and large cannon-ball like fruits, is one of the neotropics' most spectacular trees. Some species of the Brazil nut family produce high quality timber, for example, species of Cariniana with their long, straight boles, the best known being the albarco (C. pyriformis Miers) of northwestern South America and the jequitibás [C. estrellensis of eastern Brazil and southwestern Amazonia and C. legalis (Mart.) Kuntze of eastern Brazil]. Brazil nut trees also produce high-grade timber, but they are protected by law because of their greater value as producers of edible seeds.
During the course of monographic work on New World Lecythidaceae, it has become apparent that some of the genera may not be monophyletic. For example, the genus Cariniana seems to comprise two separate clades (Huang, 2005
); the variation in floral structure within Lecythis is greater than that found among other genera; and the limits of the largest genus, Eschweilera, are sometimes confused with those of Lecythis. (Prance and Mori, 1979
; Mori and Prance, 1990a
).
The aim of this paper is to use a molecular phylogeny based on analysis of the coding ndhF and the noncoding trnL-F chloroplast loci to test current concepts of classification of Lecythidaceae (Prance and Mori, 1979
, 2004
; Mori and Prance, 1990a
, 2004
; Morton et al., 1998
). In addition, we examine the relationship of New World Lecythidaceae to Old World Lecythidaceae.
MATERIALS AND METHODS
ndhF
DNA was extracted from leaves taken from herbarium specimens or material dried in silica gel or from living plants. Leaves were ground with zirconia/silica beads in a Mini-Bead Beater (Biospec Products, Bartlesville, Oklahoma, USA) and subsequently treated with the DNEasy plant DNA extraction kit from Qiagen (Valencia, California, USA), following the manufacturer's protocol. The ndhF gene from the chloroplast genome was amplified using PCR with 10 µmol/L primers in 25-µL reactions using Ready-to-Go PCR beads (Amersham Pharmacia Biotech, Uppsala, Sweden) following the manufacturer's standard protocol. The thermal cycling profile was 95°C for 5 min, followed by 35 cycles of 95°C for 30 s, 50°–60°C for 30 s, 72°C for 2 min, and finally 72°C for 8 min. For sequencing reactions, the Big Dye Terminator Sequencing kit (Applied Biosystems, Warrington, Cheshire, UK) was used, and fragments were separated on an ABI377 or AB13100 Sequencers from Applied Biosystems. Primers (Table 2) used for PCR and for sequencing were those employed by Källersjö et al. (2000)
. Sequences were assembled and checked with the Staden software (Staden and Bonfield, 1998
) and aligned manually with the BioEdit software (Hall, 1999
).
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. The amplification of trnL-trnF, which is composed of the trnL intron, trnL3' gene, and trnL-trnF intergenic spacer, was done by using the TabC and TabF primers (Taberlet et al., 1991
). The target loci were amplified in 25-µL volumes using standard PCR protocols and the thermal cycling profile 94°C for 5 min followed by 30 cycles of 94°C for 1 min, 49°C for 1 min, 72°C for 1 min 30 s, and finally 72°C for 7 min. Then the PCR products were purified using the QIAquick PCR purification kit (Qiagen). Sequencing was usually done using primers TabC and TabF, or occasionally primers TabD and TabE (Taberlet et al., 1991
), on an ABI 377 sequencer (Applied Biosystems). Sequences were assembled from both directions. All sequence data were aligned with the GCG program (Wisconsin Package, version 10.3) and then adjusted manually using the program Se-Al (Rambaut, 1996
).
Vouchers
The new sequences have been submitted to GenBank (see Appendix 1 for accession numbers and voucher information).
Parsimony analysis
Sapotaceae have in some recent papers been found to be sister to the Lecythidaceae (Morton et al., 1997
; Anderberg et al., 2002
), but that relationship was not confirmed in a study based on a greater number of genes (Schönenberger et al., 2005
) in which Lecythidaceae were unresolved in a position at the base of the larger clade of families of the Ericales. A robust hypothesis regarding its sister group is still to be presented, and therefore we used Marcgravia as outgroup for the analysis. Following the results of Anderberg et al. (2002)
and Schönenberger et al. (2005)
, this family is part of the sister group of the larger clade to which Lecythidaceae belong.
The separate ndhF and trnL-F data sets and the combined ndhF + trnL-F data matrix were analyzed by parsimony jackknifing (Farris et al., 1996
) using the computer program Xac (Farris, 1997
) with the following settings: 1000 replicates, each with branch swapping and 10 random addition sequences.
Following Eernisse and Kluge (1993)
, we consider the best phylogenetic hypothesis to be the one based on analysis of as much data as possible, and, therefore, we based most of our discussion on the results of the analysis of the combined data. The combined ndhF + trnL-F data matrix and tree were submitted to the TreeBase database (http://www.treebase.org).
RESULTS
The ndhF data set is comprised of 2062 characters of which 422 were informative, and the trnL-F includes 1159 characters of which 195 were informative. The trees from the separate analyses are more collapsed than the tree resulting from an analysis of the two in combination. The combined tree is entirely congruent with the ndhF tree, and almost congruent with the trnL-F tree. The latter differs from the combined tree in two minor ways. First, Cariniana pyriformis, which is in an unresolved position in the combined (Fig. 1) and the trnL-F trees, is sister to C. estrellensis in the ndhF tree. Cariniana pyriformis and C. estrellensis, in turn, are sister to C. domestica, and this clade is sister to C. ianeirensis. The support in the tree derived from the trnL-F data is very low, but the topology is congruent with that of a morphological analysis of the phylogenetic relationships of Cariniana by Huang (2005)
. Second, Lecythis minor, which is sister to L. tuyrana in the combined tree (Fig. 1), groups with L. ampla, L. pisonis, and L. zabucajo in the trnL-F tree. The L. ampla group has been recognized as Lecythis sect. pisonis by Mori (1990)
, and its species are morphologically very different from L. minor. On the other hand, L. minor and L. tuyrana share morphological characters such as androecial hoods that are expanded at the apex, hood staminodes without anthers, and seeds with only the major veins apparent.
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The Lecythidoideae include representatives of all New World genera of Lecythidaceae. This clade has 100% jackknife support and includes one monophyletic group consisting of the actinomorphic-flowered genera Grias and Gustavia with weak jackknife support (55%) and another monophyletic group encompassing all remaining Lecythidaceae (99%). Within the Grias-Gustavia clade, Grias forms one clade (99%) and Gustavia (87%) another. The Gustavia clade contains two subclades, the Gustavia hexapetala (100%) and the G. longifolia (99%) lineages.
The New World zygomorphic-flowered clade is comprised of two clades, the Couroupita clade (100%) and a clade encompassing all remaining Lecythidaeae (100%). Within the latter, relationships of the Cariniana pyriformis, Allantoma lineata-Cariniana decandra (100%), C. ianeirensis (58%), Couratari (86%), and Bertholletia (55%) lineages are unresolved. Among these, the flowers are zygomorphic in all but the A. lineata-C. decandra lineage.
The Bertholletia clade includes the following lineages: B. excelsa, Lecythis mesophylla, Eschweilera amazoniformis-E. nana (54%), L. minor (four species, 89%), Corythophora (four species, 95%), L. lanceolata (four species, 87%), L. chartacea (six species, 99%), E. tessmannii (six species, 100%), and L. confertiflora (five species, 93%), and E. ovata (25 species, 61%).
DISCUSSION
Monophyly of Lecythidaceae
As circumscribed by Prance and Mori (1979)
, the Lecythidaceae (including subfamilies Lecythidoideae, Planchonioideae, Foetidioideae, and Napoleonaeoideae) are not monophyletic because Asteranthos brasiliensis has been shown to be more closely related to Scytopetalaceae. Moreover, species of Napoleonaea form a separate clade even further removed from the core Lecythidaceae than are the Scytopetalaceae.
Prance and Mori (1979)
considered Asteranthos as belonging to the Lecythidaceae subfam. Napoleonaeoideae and did not include Scytopetalaceae as part of the Lecythidaceae. Asteranthos brasiliensis has been treated as a monotypic family (Knuth, 1939a
), allied with the Napoleonaeaceae (Pichon, 1945
; Prance and Mori, 1979
), or aligned in the Scytopetalaceae subfamily Syctopetaloideae (Appel, 1996
, 2004
). Based on embryological features, Tsou (1994b)
was the first to suggest the relationship of A. brasiliensis with species of the West African Scytopetalaceae. Carlquist (1988)
pointed out the similarity of the wood of Scytopetalaceae with that of the Lecythidaceae, but his study did not include Asteranthos. The close relationship of Asteranthos with the Scytopetalaceae has been supported on morphological grounds by Appel (1996)
and by molecular data from Morton et al. (1997)
. The rbcL analysis of Lecythidaceae by Morton et al. (1998)
shows A, brasiliensis as sister to Oubanguia-Brazzeia of the Scytopetalaceae and the Asteranthos-Oubanguia-Brazzeia clade embedded in the Lecythidaceae sensu lato. Thus, the systematic position of Asteranthos close to the African species of Scytopetalaceae is supported both by morphological and molecular data.
Our combined analysis of ndhF and trnL-F is based on a much greater number of taxa than that in Morton et al. (1997
, 1998
) and gives strong support for a Scytopetalaceae clade within which are two strongly supported clades that conform to Appel's (1996) division of the Scytopetalaceae into two subfamilies, the Scytopetaloideae (Oubanguia-Scytopetalum in our tree, but also including Asteranthos) and the Rhaptopetaloideae (Brazzeia and Rhaptopetalum in our tree, but also including Pierrina) (Fig. 1). Appel (2004)
provides arguments for treating the scytopetaloids as a separate family, and their position as sister to Lecythidaceae proper is consistent with our combined ndhF and trnL-F tree. If Lecythidaceae are to include Asteranthos, then Scytopetalaceae proper also have to be included in order for Lecythidaceae to be monophyletic. However, we concur with Appel (2004)
that the Old World Scytopetalaceae merits the rank of a separate family sister to the Lecythidaceae because of their mostly superior vs. mostly inferior ovaries and the presence vs. absence of endosperm (Appel, 1996
).
Subdivision of Lecythidaceae lineage
Lecythidaceae have been viewed as one family divided into three (Pichon, 1945
) or five subfamilies (Morton et al., 1998
), or various combinations of the subfamilies have been recognized as separate but related families. When all five subfamilies are included in a broadly defined Lecythidaceae, nonmolecular synapomorphies for it are (1) numerous stamens, (2) bitegmic ovules, and (3) the presence of cortical bundles (Morton et al., 1997
). On the other hand, when three subfamilies comprise the Lecythidaceae (i.e., Foetidioideae, Planchonioideae, and Lecythidoideae), there are no known nonmolecular synapomorphies for it (Morton et al., 1997
, Fig. 6). However, this is not without precedent in the Ericales, a group for which there are no known anatomical or morphological synapomorphies.
Prance (2004)
treated Crateranthus and Napoleonaea as Napoleonaeaceae, Appel (1996
, 2004
) placed the scytopetaloids in Scytopetalaceae, and Prance and Mori (2004)
divided Lecythidaceae into subfamilies Foetidioideae, Planchonioideae, and Lecythidoideae. In our combined ndhF+trnL-F tree (Fig. 1) the Napoleonaeaceae are represented by our Napoleonaea clade, the Scytopetalaceae conform to our Brazzeia-Rhaptopetalum-Oubanguia-Scytopetalum clade, and the core Lecythidaceae include all remaining taxa in our tree.
Our analysis demonstrates that the three subfamilies of Lecythidaceae as defined by Prance and Mori (2004)
correspond to separate clades in our tree (Fig. 1) as follows: (1) our Foetidia clade to the Foetidioideae, (2) our Petersianthus-Chydenanthus-Barringtonia clade to the Planchonioideae, and (3) our New World Lecythidaceae clade to the Lecythidoideae.
The core Lecythidaceae as defined by Tsou (1994b)
comprises the Lecythidoideae and Planchonioideae, but does not include Foetidia. Our results, however, show a close relationship between Foetidia and the Planchonioideae (Fig. 1) and make Tsou's core Lecythidaceae nonmonophyletic if Foetidia is excluded. All of the Old World clades have very strong jackknife support (Fig. 1) and are in agreement with the family classification outlined in Kubitzki (2004)
but differ from the Angiosperm Phylogeny Group's recognition of a more broadly defined family with five subfamilies (APG, 2003
).
Another possible classification is to recognize Foetidia as Foetidiaceae, the Petersianthus-Chydenanthus-Barringtonia africanus clade as Barringtoniaceae, and all remaining taxa as Lecythidaceae. When the subfamilies are recognized as families, there is at least one nonmolecular synapomorphy for each family, the most convincing of which are uniseriate perianths for Foetidiaceae, syntricolpate pollen for Barringtoniaceae, and a chromosome base number of x = 17 for Lecythidaceae (Morton et al., 1997
).
All permutations of Lecythidaceae been recognized in the past by other systematists, so there is no need to publish new combinations if the three subfamilies are either retained or recognized as separate families. Although chromosome numbers do not lend to ease of identification as suggested by Backlund and Bremer (1998) as a secondary principal for recognizing taxonomic groups, they at least represent a nonmolecular synapomorphy for Lecythidaceae if it is recognized as a family equivalent to subfamily Lecythidoideae. The common occurrence of actinomorphic flowers among species of Grias, Gustavia, and the genera of Barringtoniaceae makes the presence of actinomorphic flowers homoplasious in Lecythidoideae, thus negating the unique zygomorphic androecium found in approximately 73% of New World Lecythidaceae (Mori, 2004
) as a synapomorphy.
Because there are no known nonmolecular synapomorphies for a Lecythidaceae comprised of subfamilies Foetidioideae, Planchonioideae, and Lecythidoideae, the recognition of this lineage as a family (Prance and Mori, 2004
) is based only on molecular evidence. Conflicts of the Lecythidaceae lineage in the classifications of the APG (2003)
and Prance and Mori (2004)
, e.g., one family with five subfamilies in the former or three families in the latter, demonstrate that the higher level classification of Lecythidaceae is not nomenclaturally stable. Modern authors have not supported recognizing five separate families, a possibility that should not be discarded without further study; but until this is done we will continue to treat the Lecythidaceae lineage as three families: Napoleonaeaceae, Scytopetalaceae, and Lecythidaceae, with the latter comprised of three subfamilies.
Relationship of New World Lecythidaceae
There are no apparent morphological synapomorphies that unite all New World Lecythidaceae because the actinomorphic-flowered Grias and Gustavia (Fig. 2) share floral symmetry, indehiscent fruits, and other plesiomorphic characters with the Old World Planchonioideae. A nonmorphological synapomorphy for the Lecythidoideae is a chromosome number of x = 17 (Kowal et al., 1989
). Other taxa have chromosome numbers of x = 13 (Planchonioideae) and x = 16 (Napoleonaeaceae) (Kowal, 1977
). There are no known chromosome counts of Foetidia and Scytopetalaceae other than Asteranthos (x = 21) (Kowal, 1989
). The New World Lecythidaceae universally possess tricolpate pollen (see figs. 20, 21 in Muller, 1979
) in contrast to the syntricolpate pollen of the Planchonioideae (see figs. 1–4 in Muller, 1972
; pls. I, III in Muller, 1973
; and figs. 1–5 in Tsou, 1994a
), but tricolpate pollen is plesiomorphic as it is also found in the Old World Crateranthus and Napoleonaea of Napoleonaeaceae, Foetidia of Lecythidaceae subfam. Foetidioideae, and Scytopetalaceae (Muller, 1972
, 1979
). Syntricolpate pollen is most likely a synapomorphy for the planchonioids because it is only found among them. Moreover, studies by Muller (1973)
and Tsou (1994a) provide plausible arguments that syntricolpate pollen is derived from tricolpate pollen. The pollen grains of Scytopetalaceae subfam. Scytopetaloideae (Asteranthos, Scytopetalum, and Oubanguia) are tricolpate, while those of Scytopetalaceae subfam. Rhaptopetaloideae (Rhaptopetalum, Brazzeia, and Pierrina) are tricolporoidate (Appel, 1996
). Zygomorphic flowers (Fig. 2) and woody circumscissile fruits (although some species have secondarily indehiscent fruits) are, however, synapomorphies for the zygomorphic-flowered Lecythidoideae.
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), possibly some species of Foetidia (see fig. 14 in Knuth, 1939b
and fig. 4 in Bosser, 1988
), and species of Napoleonaea (Frame and Durou, 2001
; see fig. 2 in Knuth, 1939b
) have a disc situated between the androecium and style that is not found in Lecythidoideae or Scytopetalaceae. The disc is apparently a loss in the New World taxa because it is found frequently in several clades of Old World Lecythidaceae (Fig. 3).
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The evolution of floral zygomorphy
Within Lecythidoideae, there are two major clades, one formed by the actinomorphic-flowered Gustavia (Fig. 2) and Grias (Fig. 3) and another by all other mostly zygomorphic-flowered New World Lecythidaceae. The latter clade is in turn divided into two, one consisting of the species of Couroupita and the other made up of all remaining Lecythidoideae. Although both of these clades consist of species with predominantly zygomorphic flowers, the Allantoma-Cariniana decandra clade (Fig. 1) is an exception. As discussed, actinomorphic flowers are plesiomophic, and the clade with the actinomorphic-flowered genera is sister to the clade with the predominantly zygomorphic-flowered taxa (Fig. 1). Although a few species within the zygomorphic-flowered clade have actinomorphic flowers (viz. the species of the Allantoma-C. decandra clade), there are no species of Old World Lecythidaceae with them. The evolution of zygmorphy in the New World Lecythidaceae is most likely an adaptive feature related to pollination by bees and to a lesser extent by bats (Mori and Boeke, 1987
). Beetle pollination is suspected in species of Grias, but this has not led to zygomorphy (Knudsen and Mori, 1996
).
In Cariniana, as currently circumbscribed, there are two distinctive groups, one with actinomorphic flowers and the other with zygomorphic flowers (Fig. 4) (Huang, 2005
). The actinomorphic-flower type is represented by species in the Allantoma lineata-C. decandra clade and the zygomorphic-flowered group by the C. ianeirensis-C. domestica-C. estrellensis clade (Fig. 1). If, as suggested by our cladogram (Fig. 1), zygomorphic flowers evolved only once in New World Lecythidaceae, then the presence of the actinomorphic-flowered A. lineata-C. decandra clade among the zygomorphic-flowered taxa probably represents a reversal from zygomorphic back to actinomorphic flowers.
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; Mori and Prance, 1990a
) and examine which genera and subgenera are supported by our molecular data. Species of Grias have cauline inflorescences, actinomorphic flowers, a thick and fleshy staminal ring, 85–200 stamens arising on the inwardly slanted upper rim of the staminal ring, indehiscent fruits, a fleshy, edible mesocarp, a single fusiform seed, and a macropodial embryo (i.e., lacks well-developed cotyledons as in the Brazil nut). Grias can be recognized by this unique combination of characters, albeit none is synapomorphic for species of the genus. The combined molecular tree (Fig. 1) supports the recognition of Grias as a genus but provides no further insight into its subgeneric classification. In agreement with this finding, the seven species of Grias have not been divided into sections. The only significant variation found in the genus is the presence of persistent bracteoles on the pedicels and six distinct calyx lobes in G. neuberthii (not included in our analysis). The other species lack the bracteoles and possess calyces that surround the bud and break open irregularly at anthesis.
The actinomorphic-flowered Gustavia possesses from 500 to 1200 stamens that arise at the same level from the apex of a staminal ring (Fig. 2). It is the only genus of Lecythidaceae with poricidal anther dehiscence and planoconvex cotyledons, and these features are synapomorphies for species of the genus. Mori (1979)
recognized three sections of Gustavia: (1) sect. Hexapetala with a leptocaul growth form and flowers with six sepals that possess inverted y-shaped thickenings on the adaxial surface; (2) sect. Grandibracteata with a pachycaul growth form and a large bract that subtends the flowers and two large bracteoles on the pedicel; and (3) sect. Gustavia by the absence of features found in the other two sections. Within section Gustavia, some of the species possess seeds with expanded, contorted, yellow funicles (e.g., G. augusta), and others lack expanded funicles (e.g., G. superba). Our molecular tree (Fig. 1) supports the recognition of Gustavia as a monophyletic genus and shows that the two species (G. hexapetala and G. dubia) of sect. Hexapetala form a clade sister to the remaining species of Gustavia. There is, however, no support for the recognition of any of the other sections of the genus.
The zygomorphic-flowered Couroupita is diagnosed by long cauline inflorescences; ovules inserted along a bilamellar placenta that runs the length of the locule; cannon-ball like, indehiscent fruits; lenticular seeds with trichomes; and seeds embedded in a pulpy mass (see fig. 36 in Mori and Prance, 1990). All these features, except the indehiscent fruits, are synapomorphies for species of this genus. Each of the three species of Couroupita has flowers with distinctive androecia by which they can be told apart (see fig. 34 in Mori and Prance, 1990), whereas the cannon-ball like fruits are difficult, if not impossible, to distinguish from one another. The androecial hood of C. nicaraguarensis is flat with the numerous stamens continuous from the staminal ring to the end of the hood, the hood of C. guianensis is flat with a stamen-free area between the stamens of the staminal ring and the hood proper, and the hood of C. sessilis is notched at the apex and has an invagination (see fig. 34 in Mori and Prance, 1990). In the combined tree, the two species of Couroupita form a strongly supported clade sister to all species of neotropical Lecythidaceae except Gustavia and Grias.
The genus Cariniana sensu lato possesses small flowers in comparison to other Lecythidaceae (<2 cm diam.), three-locular ovaries, seeds with unilateral wings adapted for wind dispersal, and foliaceous cotyledons. Within Cariniana, there are two morphologically distinct clades, one with actinomorphic (the C. decandra clade) and the other with zygomorphic (our C. ianeirensis clade but referred to as the C. legalis clade in other papers including this species) flowers (Fig. 4). In addition to androecial symmetry, the C. decandra clade differs from the C. ianeirensis clade by eucamptodromous vs. brochidodromous secondary venation, percurrent vs. reticulate tertiary venation, five- vs. six-merous corolla, entire vs. marginally pubescent petal margins, hooked vs. flat petal apices, and reflexed vs. straight stamens (Huang, 2005
). In our analysis the monotypic Allantoma groups with C. decandra, thus rendering Cariniana paraphyletic in its present circumscription. Allantoma has been characterized by eucamptodromous secondary venation, percurrent tertiary venation, five-merous corolla, entire petal margins, hooked petal apices, stamens that are scattered all over the inside of a relatively long and carnose tube, reflexed stamens, dehiscent and cylindrical fruits, seeds with a papillate surface and a notch at the base, and a vestigial seed wing. All but the long androecial tube and the seed features are also found in the actinomorphic-flowered species of Cariniana. In the combined tree (Fig. 1), A. lineata is sister to C. decandra thereby supporting the hypothesis that species of Cariniana with actinomorphic flowers are more closely related to Allantoma than they are to the zygomorphic-flowered species of the currently circumscribed Cariniana (Huang, 2005
). Additional taxa of actinomorphic-flowered species of Cariniana are needed to further test this hypothesis. In the combined tree, C. ianeirensis-C. domestica-C. estrellensis, all with zygomorphic flowers, form a clade with low jackknife support (58%), but their relationships to other clades are unresolved. The position of the zygomorphic-flowered C. pyriformis is unresolved with our data but could be anticipated to group with the other zygomorphic-flowered species. A morphological analysis of Allantoma and Cariniana (Huang, 2005
) also found support for the actinomorphic-flowered species of Cariniana being more closely related to Allantoma than they are to the zygomorphic-flowered species of Cariniana. The fleshy androecial tube and reflexed stamens are synapomorphies for A. lineata and the actinomorphic-flowered species of Cariniana, whereas an obliquely zygomorphic androecium is a synapomorphy for the zygomorphic-flowered species of Cariniana. Although zygomorphy is pleisiomorphic for the C. ianeirensis clade, the androecial hood of species of this clade differs from all other zygomorphic-flowered species of Lecythidaceae by lacking a hood with sterile stamens and no tissue differentiation between the staminal ring and the hood proper. Because there is no hood modification, such as the occurrence of staminodes, the presence of fodder pollen, or tissue proliferation in the most distal part of the androecium, we call the flowers of the C. ianeirensis clade obliquely zygomorphic (Fig. 4) and distinguish this type of hood from that of all other zygomorphic-flowered species of Lecythidaceae.
Couratari possesses zygomorphic flowers, three-locular ovaries, an androecial hood that forms an external flap over the hood proper, a wing that completely surrounds the seed, and foliaceous cotyledons. The external flap and circumferentially winged seeds are synapomorphies for species of the genus. Prance (1990)
divided Couratari into three sections: (1) sect. Echinata with the external flap of the hood echinate, hard and woody fruits, and stellate hairs on the hypanthium and axes of the inflorescence, and sometimes on the abaxial surface of the leaf blades; (2) sect. Couratari with the external flap of the hood verrucose, hard and woody fruits, and stellate hairs on the leaves and inflorescences of some species; and (3) sect. Microcarpa with the external flap of the hood verrucose, coriaceous fruits, and stellate hairs never present. In the combined tree, species of Couratari are placed in a clade with 86% jackknife support. Within this clade, there are two subgroups, the C. macrosperma-C. stellata clade that corresponds to Couratari sect. Echinata. In the other clade, the two species of sect. Couratari (C. guianensis and C. calycina) and the two species of sect. Microcarpa (C. multiflora and C. oblongifolia) group with each other, but their relationships are not resolved and, thus, provide no support for the other two sections recognized by Prance (1990)
.
The zygomorphic-flowered Brazil nut, Bertholletia excelsa, is the only species of a genus characterized by two calyx lobes at anthesis, an opercular opening of the fruit smaller in diameter than the size of the seeds, and triangular seeds with a boney testa (Tsou and Mori, 2002
). Floral developmental studies reveal that the two-parted calyx is the result of the fusion of six sepal primordia soon after their initiation (C.-H. Tsou, Academia Sinica, personal communication) with three small teeth visible at the apex of each lobe of mature flowers. All diagnostic features of Bertholletia are autapomorphies and in the combined tree, the monospecific Bertholletia does not group with any other genus; thus its systematic position is still pending better resolution of the relationships within the zygomorphic-flowered New World clade.
The zygomorphic-flowered Corythophora is characterized by a flat, somewhat thickened androecial hood (see figs. 31, 42–44 in Mori and Prance, 1990); the presence of fodder anthers either in the hood or in the inner rows of the staminal ring stamens; and campanulate or cylindrical, thick-walled fruits. There are no known morphological synapomorphies for the species of this genus as all morphological features used to recognize its species are plesiomorphies that are also known in other genera of Lecythidoideae. In spite of this, our molecular data provide strong support for Corythophora as a monophyletic group with two distinctive clades (Fig. 1). The C. alta-C. rimosa clade is characterized by small, triangular calyx lobes; calyx lobes and hypanthium of the same texture and color; and the presence of fodder anthers in the hood. The C. labriculata-C. amapaensis clade has larger, rounded calyx lobes; a distinction in color between the calyx lobes and the hypanthium; and fodder anthers located in the inner most part of the staminal ring. The Corythophora clade has high jackknife support (95%), but its sister relationships are not resolved.
Species of Lecythis, as currently circumscribed (Mori and Prance, 1990), are characterized by four-locular ovaries and seeds with a basal aril (see fig. 101 in Mori and Prance, 1990), neither of which are synapomorphic for species of the genus. Lecythis possesses two types of androecial hood, one that is flat and the other that is swept inwards (see fig. 31 in Mori and Prance, 1990), and these and other features resulted in the recognition of four sections by Mori (1990)
: (1) sect. Corrugata characterized by flat androecial hoods and rugose hypanthia and pedicels; (2) sect. Pisonis with flat androecial hoods and hood staminodes with fodder pollen; styles with an annular ring near the apex; petals, fruits, and foliage that turn bluish-green when bruised; enormous fruits up to the size of a child's head; and sulcate seeds with very large basal arils (see fig. 101 in Mori and Prance, 1990); (3) sect. Poiteaui with nocturnal flowers, ca. 1000 stamens, unbranched inflorescences that project above the canopy, and flat androecial hoods; and (4) sect. Lecythis with androecial hoods that are enlarged at the apex and appendages that are curved back into the flower without forming a complete coil.
In the combined molecular tree, currently recognized species of Lecythis are found in five different clades: (1) as the single species L. mesophylla, (2) as the L. minor clade with five species, (3) as the L. lanceolata clade with four species, (4) as the L. chartacea clade with six species, and (5) as the L. confertiflora clade with six species. The relationships of L. mesophylla (sect. Lecythis) are unresolved, but its morphological characters would indicate that it is most closely related to L. minor and L. tuyrana. The L. minor clade includes only one of the three species of bat-pollinated species of Lecythidaceae (L. poiteaui) that make up sect. Poiteaui. The other bat-pollinated species (L. barnebyi and L. brancoensis) should be included in future analyses. Species of the L. minor clade include representatives from sect. Poiteaui (L. poiteaui) and from sect. Lecythis (L. prancei, L. minor, L. tuyrana). The L. lanceolata clade conforms to Lecythis sect. Pisonis. All species in the L. chartacea clade are from sect. Lecythis, except for Eschweilera congestiflora and E. simiorum, which are morphologically more closely related to species of Lecythis than they are to species of Eschweilera (discussed later). The L. confertiflora clade conforms to Lecythis. sect. Corrugata (Fig. 1). As currently defined, there are no morphological synapomorphies that distinguish species of Lecythis. There is, however, at least one synapomorphy for the species of three of the four sections of Lecythis as recognized by Mori (1990)
: species of Lecythis sect. Pisonis (all of the species in our L. lanceolata clade) have sulcate seeds (see fig. 101 in Mori and Prance, 1990); species of Lecythis sect. Poiteaui (represented only by L. poiteaui in our L. poiteaui clade) possess nocturnal flowers with the smell of rotting cabbage; and species of Lecythis sect. Corrugata (all of the species of our L. confertiflora clade) have rugose pedicels and hypanthia (see fig. 97 in Mori and Prance, 1990). Species of Lecythis sect. Lecythis are recognized by inwardly curved androecial hood appendages that do not form a full coil (see L. holcogyne in fig. 31 in Mori and Prance, 1990), but this feature is also found in Bertholletia (see fig. 31 in Mori and Prance, 1990) as well as in several species currently classified as Eschweilera, e.g., E. nana (see fig. 11 in Mori, 1995
). In our cladogram (Fig. 1), E. nana does not fall within either of the two clades of Eschweilera. The fate of other generic names historically applied to species of Lecythis as defined by Mori and Prance (1990), e.g., Chytroma, Holopyxidium, and Sapucaya, have not yet been established because the first has not been typified, and the latter two are not represented in our analysis.
Most species of Eschweilera, as currently defined, are characterized by fully coiled androecial hoods (see figs. 69, 72, 75, 76, 85, 87 in Mori and Prance, 1990), two-locular ovaries, ovules that are attached to the floor of the locule, and seeds with either a lateral aril (see fig. 85 in Mori and Prance, 1990) or a sarcotesta (see figs. 1, 16 in Tsou and Mori, 2002
). Four sections have been recognized in this genus (Mori and Prance, 1990b
): (1) sect. Tetrapetala, a group of three species found in southern coastal Brazil characterized by four petals and an androecial hood that does not form a complete coil (see figs. 63, 65 in Mori and Prance, 1990), (2) sect. Bracteosa, a group of four Amazonian species that have persistent bracts and bracteoles, (3) sect. Jugastrum, with a single species that has wedge-shaped seeds with a corky seed coat, the absence of an aril, and germination in the middle rather than at the ends of the seeds (See figs. 32H, 67 in Mori and Prance, 1990a
), and (4) sect. Eschweilera, the largest group mostly characterized by six petals, fully coiled androecial hoods, and either a lateral aril or a sarcotesta.
Species of Eschweilera do not form a monophyletic group and are found in four clades in our tree: (1) a poorly supported clade (58%) with two species (E. amazoniformis-E. nana), (2) the Lecythis chartacea clade with two species of Eschweilera, E. simiorum and E. congestiflora, embedded in it, (3) the E. tessmannii clade with six species, and (4) the E. ovata clade with 25 species. The androecial hoods of E. amazoniciformis and E. nana do not form a complete coil, and in this feature are more closely related to species of Lecythis sect. Lecythis than they are to species of Eschweilera. Moreover, support for this clade is so low that it may be possible that the two species have relationships with species of Lecythis (Fig. 1). In the E. tessmannii clade, E. ovalifolia and E. longirachis possess seeds surrounded by a sarcotesta. It is likely that at least E. andina and E. rimbachii also have sarcotestas, but this is not possible to confirm with the herbarium material available. Nevertheless, sarcotestas are only found in Eschweilera, so if they are limited to our E. andina clade, they are synapomorphic for species of that clade. Finally, the E. ovata clade is made of species that have a lateral aril, a feature that is likely synapomorphic. The type of the genus, E. parvifolia, has not been possible to include in the analysis, but based on the possession of a lateral aril, it probably belongs in the E. ovata clade. Inclusion of this species in future analyses will be given priority.
The presence of E. congestiflora and E. simiorum embedded in a clade with species of Lecythis is most likely the result of their placement in the wrong genus. Because of their curved inward hood appendages, four-locular ovaries, and basal arils they are more correctly accommodated in Lecythis sect. Lecythis to which the other species in that clade belong.
Our combined analysis demonstrates that Eschweilera, as currently circumscribed, is not monophyletic and that there is little correspondence between the sections of Eschweilera as defined by Mori and Prance (1990a)
and the clades of Eschweilera found in our combined trnL-F and ndhF tree. However, sect. Tetrapetala is not represented in our analysis, and sect. Bracteosa is represented by only E. bracteosa. Eschweilera tenuifolia is sometimes segregated as Jugastrum, but our tree (Fig. 1) does not support or reject this option. In addition, the species of Eschweilera with a sarcotesta and those with a lateral aril fall into two groups in our molecular tree (Fig. 1), and this dichotomy in the genus had not been previously recognized.
Our analysis shows that the Napoleonaeaceae, Scytopetalaceae, and Lecythidaceae conform to highly supported clades. Separation of the Lecythidaceae into subfamilies Foetidioideae, Planchonioideae, and Lecythidoideae is consistent with strongly supported clades found in our analysis (Fig. 1). Molecular data show that the New World Lecythidoideae are sister to the Old World Foetidia-Petersianthus clade, and morphological features suggest that the link is through the actinomorphic-flowered ancestors of Grias and Gustavia that are in turn sister to the zygomorphic-flowered New World taxa. Zygomorphy is restricted to the New World Lecythidaceae and appears to have evolved once, but this interpretation may require a reversal back to actinomorphic flowers in the Allantoma lineata-Cariniana decandra lineage. An examination of generic concepts of New World Lecythidaceae points out problems with the current circumscriptions of Allantoma, Cariniana, Eschweilera, and Lecythis.
APPENDIX
Voucher information and GenBank accession numbers for taxa used in this study. Voucher specimens are deposited in the following herbaria: B = Berlin Botanical Garden, CAY = Herbier de Guyane, HAST = Academia Sinica in Taiwan, INB = Costa Rican National Biodiversity Institute, K = Royal Botanic Gardens Kew, LSCR = La Selva Biological Station, NY = The New York Botanical Garden, MO = Missouri Botanical Garden, PMA = University of Panama, S = Swedish Natural History Museum, US = United States National Herbarium, WAG = Herbarium Vadense in Wageningen.
Taxon—GenBank accessions nos.: ndhF, trnL; Source, Voucher specimen, Country of collection, Herbarium.
Allantoma lineata (Mart. ex O. Berg) Miers—DQ388180, DQ417929; Kew DNA bank1945; —, Tree 19 Ducke Reserve, Amazonian Brazil, —.
Barringtonia asiatica (L.) Kurz—AF421044, DQ417930; Cult.; Chung & Anderberg 1417, Taiwan, S. B. edulis Seem.—DQ388174, DQ417931; Cult., Tsou 1552, Singapore, specimen lost. B. racemosa (L.) Spreng—DQ388175, DQ417932; Pell 684, Madagascar, NY.
Bertholletia excelsa Bonpl.—DQ388181, DQ417933; Cult.; Tsou 1543, Taiwan, NY.
Brazzieia sp.—DQ388167, DQ417934; Kew DNA bank 1621, Breteler 12916, Gabon, WAG.
Cariniana decandra Ducke—DQ388185, DQ417935; Mori et al. 25640, Peru, NY. C. domestica (Mart.) Miers—DQ388186, DQ417936; Solomon 7848, Bolivia, NY. C. estrellensis (Raddi) Kuntze—DQ388187, DQ417937; Nee 38522, Bolivia, NY. C. ianeirensis R. Knuth—DQ388184, DQ417938; Justiniano 12, Bolivia, NY. C. pyriformis Miers—DQ388273, DQ417939; Bunting et al. 10965, Venezuela, NY.
Chydenanthus excelsus Miers—DQ388173, DQ417940; Kew DNA bank 1298, Chase 1298, K.
Corythophora alta R. Knuth—DQ388188, DQ417941; Vicentini & da Silva 423, Brazil, NY. C. amapaensis Pires ex S. A. Mori & Prance—DQ388189, DQ417942; Mori et al. 24148, French Guiana, CAY. C. labriculata (Eyma) S. A. Mori & Prance—DQ388190, DQ417943; Mori 25518, Surinam, NY. C. rimosa W. A. Rodrigues ssp. rubra S. A. Mori—DQ388191, DQ417944; Mori et al. 25475, French Guiana, NY.
Couratari calycina Sandwith—DQ388192, DQ417945; Molino & Sabatier 2018, French Guiana, NY. C. guianensis Aubl.—DQ388193, DQ417946; Mori et al. 25406, French Guiana, NY. C. macrosperma A. C. Sm.—DQ388194, DQ417947; Mori et al. 25634, Peru, NY. C. multiflora (Sm.) Eyma—DQ388195 and DQ417948; Prévost & Sabatier 4691 and Prévost & Sabatier 4503, respectively, both from French Guiana and both at NY. C. oblongifolia Ducke & R. Knuth—DQ388197, DQ417949; Mori et al. 22246, French Guiana, NY. C. stellata A. C. Sm.—DQ388196, DQ417950; Mori et al. 24092, French Guiana, CAY.
Couroupita guianensis Aubl.—DQ388182, DQ417950; Tsou 1550, NY, photo only. C. nicaraguensis DC—DQ388183, DQ417952; Aguilar 8041, Costa Rica, NY.
Eschweilera alata A. C. Sm.—DQ388262, DQ417953; Prévost & Sabatier 4615, French Guiana, NY. E. albiflora (DC.) Miers—DQ388226, DQ417954; Mori et al. 9199, Brazil, NY. E. amazoniciformis S. A. Mori—DQ388228, DQ417955; Nascimento et al. 644, Brazil, NY. E. andina (Rusby) J. F. Macbr.—DQ388229, DQ417956; Pitman 5892, Ecuador, NY. E. atropetiolata S. A. Mori—DQ388270, DQ417957; Pacheco et al. 91, Brazil, NY. E. bracteosa (Poepp. ex O. Berg) Miers—DQ388230, DQ417958; Prance et al. 22703, Brazil, NY. E. chartaceifolia S. A. Mori—DQ388231, DQ417959; Prévost & Sabatier 4498, French Guiana, NY. E. collina Eyma—DQ388323, DQ417960; Mori & Smith 25145, French Guiana, NY. E. congestiflora (Benoist) Eyma—DQ388225, DQ417961; Molino & Sabatier 2019, French Guiana, NY. E. coriacea (DC.) S. A. Mori—DQ388246, DQ417962; Mori et al. 25420A, French Guiana, NY. E. decolorans Sandwith—DQ388247, DQ417963; Mori et al. 25452, French Guiana, NY. E. grandiflora (Aubl.) Sandwith—DQ388251, DQ417964; Mori et al. 25435, French Guiana, NY. E. integrifolia (Ruiz & Pav. ex Miers) R. Knuth—DQ388234, DQ417965; Aguilar 6521, Costa Rica, INB. E. juruensis R. Knuth—DQ388242, DQ417966; Daly et al. 10998, Brazil, NY. E. laevicarpa S. A. Mori—DQ388252, DQ417967; Mori & Pepper 24314, French Guiana, NY. E. longirachis S. A. Mori—DQ388266, DQ417968; Aguilar 7967, Costa Rica, LSCR. E. mexicana T. Wendt, S. A. Mori & Prance—DQ388269, DQ417969; Wendt et al. 4180, Mexico, NY. E. micrantha (O. Berg) Miers—DQ388248, DQ417970; Mori et al. 25448, French Guiana, NY. E. nana (O. Berg) Miers—DQ388271, DQ417971; Teixeira 874, Brazil, NY. E. neei S. A. Mori—DQ388253, DQ417972; Aguilar 6517, Costa Rica, INB. E. ovalifolia (DC.) Nied—DQ388245, DQ417973; Mori et al. 9068, Brazil, NY. E. ovata (Cambess.) Miers—DQ388224, DQ417974; Thomas et al. 11060, Brazil, NY. E. parviflora (Aubl.) Miers—DQ388223, DQ417975; Mori et al. 25458, French Guiana, NY. E. pedicellata (Rich.) S. A. Mori—DQ388250, DQ417976; Mori et al. 25372, French Guiana, NY. E. rimbachii Standley—DQ388233, DQ417977; Clark & Guiz 6380, Ecuador, NY. E. rimbachii Standley—DQ388235, DQ417978; Ståhl & Cornejo 5930, Ecuador, S. E. sagotiana Miers—DQ388249, DQ417979; Mori et al. 25470, French Guiana, NY. E. simiorum (Benoist) Eyma—DQ388227, DQ417979; Mori et al. 25507, French Guiana, NY. E. simiorum (Benoist) Eyma—DQ388243, DQ417981; Sabatier et al. 4804, French Guiana, NY. E. tenuifolia (O. Berg) Miers—DQ388255, DQ417982; Ferreira 135, Brazil, NY. E. tessmanii R. Knuth—DQ388268, DQ417983; Mori et al. 25642, Peru, NY. E. wachenheimii (Benoist) Sandwith—DQ388254, DQ417984; Prévost & Sabatier 4252, French Guiana, NY. Eschweilerasp. A—DQ388256, DQ417985; Mori 25577, French Guiana, NY. Eschweilerasp. A—DQ388267, DQ417986; Mori & Moonen 25649, French Guaina, NY. Eschweilerasp. B—DQ388257, DQ417987; Prévost et al. 4591, French Guiana (NY). Eschweilerasp. B—DQ388261, DQ417988; Prévost & Sabatier 4609, French Guiana, NY. Eschweilerasp. B—DQ388259, DQ417989; Prévost & Sabatier 4656, French Guiana, NY. Eschweilerasp.—DQ388264, DQ417990; Aguilar 6572, Costa Rica, INB. Eschweilerasp.—DQ388263, DQ417991; Aguilar 7979, Costa Rica, LSCR. Eschweilerasp.—DQ388260, DQ417992; Mori et al. 25593, French Guiana, NY. Eschweilerasp.—DQ388265, DQ417993; Mori et al. 25606, Peru, NY. Eschweilerasp.—DQ388258, DQ417994; Prévost & Sabatier 4645, French Guiana, NY.
Foetidia mauritiana Lam.—DQ388177, DQ417996; Civeyrel 1375, Madagascar, K. F. obliqua Blume—DQ388176, DQ417995; Pell 620, Madacasgar, NY.
Grias cauliflora L.—DQ388179, DQ417997; Galdames 5180, Panama, PMA. G. multinervia Cuatrec.—DQ388272, DQ417998; Clark 7103, Ecuador, NY. G. peruviana Miers—DQ388178, DQ417999; Clark 6426, Ecuador, NY.
Gustavia augusta L.—DQ388198, DQ418000; Mori 25012, French Guiana, NY. G. augusta L.—DQ388208, DQ418001; Prévost & Sabatier 4608, French Guiana, NY. G. augusta L.—DQ388207, DQ418002; Prévost et al. 4596, French Guiana, NY. G. dubia (Bonpl.) O. Berg—DQ388203, DQ418003; McPherson 16003 for ndhF and Akers 7 for trnL-F, both from Panama and both at NY. G. hexapetala (Aubl.) Sm.—DQ388205, DQ418004; Prévost & Grenand 4346, French Guiana, NY. G. longifolia Poepp. ex O. Berg—DQ399201, DQ418005; Acevedo-Rodriguez & Cedeño 7331, Ecuador, NY. G. macarenensis Philipson ssp macarenensis—DQ388200, DQ418006; Clark et al. 6508, Ecuador, NY. G. macarenensis Philipson ssp. macarenensis—DQ388202, DQ418007; Rios 415, Ecuador, NY. G. monocaulis S. A. Mori—DQ388206, DQ418008; Mori & Kallunki 5600, Panama, NY. G. speciosa (Kunth) DC.—DQ388204, DQ418009; Ståhl & Cornejo 5902, Ecuador, S. G. superba (Kunth) O. Berg—DQ388199, DQ418010; Mori et al. 6837, Panama, NY.
Lecythis alutacea (A. C. Sm.) S. A. Mori—DQ388244, DQ418011; Mori et al. 24622, Guyana, NY. L. ampla Miers—DQ388238, DQ418012; Aguilar 7958, Costa Rica, LSCR. L. chartacea O. Berg—DQ388209, DQ418013; Mori et al. 25364, French Guiana, NY. L. confertiflora (A. C. Sm.) S. A. Mori—DQ388210, DQ418014; Mori et al. 25411, French Guiana, NY. L. corrugata Poit. ssp. corrugata—DQ388211, DQ418015; Mori & Pepper 24265, French Guiana, NY. L. holcogyne (Sandwith) S. A. Mori—DQ388212, DQ418016; Prévost & Sabatier 4508, French Guiana, NY. L. holcogyne (Sandwith) S. A. Mori—DQ388236, DQ418017; Prévost & Sabatier 4511, French Guiana, NY. L. idatimon Aubl.—DQ388214, DQ418018; Mori et al. 25430, French Guiana, NY. L. idatimon Aubl.—DQ388215, DQ418019; Mori et al. 25498, French Guiana, NY. L. lanceolata Poir.—DQ388213, DQ418020; Cult., Prance et al. 25917, Brazil, NY. L. mesophylla S. A. Mori—DQ388217, DQ418021; Aguilar 1177, Costa Rica, NY. L. minor Jacq.—DQ388216, DQ418022; Cult., Tsou 1542, Taiwan, NY. L. persistens Sagot ssp. aurantiaca S. A. Mori—DQ388218, DQ418023; Mori et al. 25436, French Guiana, CAY. L. persistens Sagot ssp. persistens—DQ388239, DQ418024; Prévost & Grenand 4285, French Guiana, NY. L. pisonis Cambess.—DQ388237, DQ427110; Cult., Tsou 2150 (= Tsou 1541), not from same tree as sequenced material but it is the same species, Taiwan, NY. L. pneumatophora S. A. Mori—DQ388220, DQ418025; Prévost 4261, French Guiana, NY. L. poiteaui O. Berg—DQ388219, DQ418026; Mori et al. 25383, French Guiana, NY. L. prancei S. A. Mori—DQ388241, DQ418027; Prance & Ramos 23098, Brazil, NY. L. tuyrana Pittier—DQ388221, DQ418028; Cult., Mori & Kallunki 5772, Panama, NY. L. zabucajo Aubl.—DQ388240, DQ418029; Mori et al. 25034, French Guiana, NY. L. zabucajo Aubl.—DQ388222, DQ418030; Mori et al. 25474, French Guiana, NY.
Marcgravia sp.—GenBank AF421065; GenBank AJ430879; Cult. Stockholm, —S.
Napoleonaea imperialis P. Beauv.—AJ236258, DQ418031; DeWilde 35, cult., Netherlands, S. N. leonensis Hutchinson & Dalziel—DQ388163, DQ418032; Schmidt 1675, —, MO. N. vogelii Hook. & Planch.—DQ388164, DQ418033; Smith 1872, Gabon, US.
Oubanguia alata Baker f.—DQ388165, DQ418034; Kew DNA bank 622, Gereau 5202, Cameroon, MO.
Petersianthus africanus (P. Beauv.) Liben—DQ388171, DQ418035; Carvalho 2698, Bioco, B.
Rhaptopetalum beguei Mangenot—DQ388169, DQ418036; Jongkind 2174, Ghana, MO, WAG. Rhaptopetalumcoriaceum—DQ388168, DQ418037; Kew DNA bank 886, Cheek 5109, —, K.
Scytopetalum klaineanum Pierre—DQ388166, DQ418038; Kew DNA bank 1622, Breteler 13096, Gabon, WAG. S. tieghemii Hutchinson & Dalziel—DQ388170, DQ418039; Jongkind 4459, Ivory Coast, WAG.
FOOTNOTES
1 The authors thank R. Aguilar, P.-C. Cheng, M. Correa, C. Galdames, C. Jongkind, R. Kiew, S. Lee, T. Lobova, J. F. Molino, S. Pell, M.-F. Prévost, D. Sabatier, R. Sco, H.-F. Yen, R. Vogt, and J. Wieringa for help in obtaining collections; the National Science Council, Republic of China for grants NSC 92–2621-B-001–003 and NSC 93–2621-B-001–002 that supported work on this project at the Academia Sinica; U. Swenson for drawing the final cladogram; and S. Fredericks for funding the preparation of Figs. 3 and 4. 
2 Author for correspondence (e-mail: smori{at}nybg.org
)
101 These authors directed the sequencing of DNA and made significant contributions to writing the paper.
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