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Phylogeny of Miconia (Melastomataceae): Patterns of Stamen Diversification

in a Megadiverse Neotropical Genus

Article  in  International Journal of Plant Sciences · September 2008

DOI: 10.1086/589697

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Int. J. Plant Sci. 169(7):963–979. 2008.
Ó 2008 by The University of Chicago. All rights reserved.
1058-5893/2008/16907-0014$15.00 DOI: 10.1086/589697

PHYLOGENY OF MICONIA (MELASTOMATACEAE): PATTERNS OF STAMEN

DIVERSIFICATION IN A MEGADIVERSE NEOTROPICAL GENUS
Renato Goldenberg,1 ,* Darin S. Penneys,y Frank Almeda,z Walter S. Judd,y and Fabián A. Michelangeli§
*Universidade Federal do Paraná, Departamento de Botânica, Campus do Centro Politécnico, Curitiba PR 81540-560, Brazil;
yDepartment of Botany, University of Florida, Gainesville, Florida 32611-8526, U.S.A.; zDepartment of Botany,
California Academy of Sciences, San Francisco, California 94103-3098, U.S.A.; and §New York
Botanical Garden, Bronx, New York 10458, U.S.A.

Phylogenetic relationships within Miconia and other genera in the Neotropical tribe Miconieae were
investigated using a maximum parsimony analysis of nuclear internal transcribed spacer and ndhF nucleotide
sequences. Included were all sections in Miconia (212 species, ;20% of the genus) and 12 of the 15 remaining
genera assigned to the tribe (an additional 239 species). Given the tribe’s reputation for problematic generic
distinctions, it was not surprising that most traditionally recognized taxonomic groups—both genera and
sections—were shown to be polyphyletic or paraphyletic. Nevertheless, Miconia is composed of several distinct
monophyletic groups, with a large majority of the species belonging to only four clades. Some of these groups
represent parts of sections proposed in the last revision of the genus, but most of the diversification seems to
have occurred in geographical areas that are more restricted than would have been predicted by the distribution
of these sections. Moreover, parallel evolutionary trends are seen in anther form, i.e., shifts from elongate to
shorter anthers and from minute-pored to large-pored or slitlike dehiscent anthers. These changes may relate to
pollinator shifts, especially from buzz pollination to nonvibrational pollination. Thus, the major evolutionary
diversifications within the tribe have been obscured by convergence in stamen morphology, leading to many
arbitrary generic and sectional circumscriptions.

Keywords: internal transcribed spacer (ITS), megadiverse genus, Melastomataceae, Miconia, Miconieae, ndhF,
phylogeny, stamen morphology.

Online enhancement: appendix.

Introduction species are common in secondary environments, providing nat-

Miconia Ruiz & Pavón is the largest genus of Melastomata-
ceae, with about 1050 species (Goldenberg 2000), and is
probably the largest exclusively New World genus of flow-
ering plants, perhaps rivaled by only Pleurothallis R.Br.
(Orchidaceae) before its breakup (Frodin 2004). These species
range from western Mexico and the Caribbean to Uruguay
and northern Argentina, growing from sea level to the Andean
paramos. A few species, notably Miconia calvescens, have
been introduced to the Pacific Islands (Meyer 1996; Meyer
and Florence 1996; Medeiros and Loope 1997), where they
have become troublesome invasives. Apart from general uses,
such as low-quality wood and fuel, species of Miconia are not
economically important. Nevertheless, they play an important
ecological role in tropical and subtropical forests as a food re-
source for the fauna because their fleshy fruits are largely con-
sumed by birds and other animals (Snow 1965; Magnusson
and Sanaiotti 1987; Levey 1990; Stiles and Rosseli 1993; Fi-
gueiredo and Longatti 1997). As fast-growing shrubs or small
trees that develop dense populations in disturbed areas, these
1
Author for correspondence; e-mail: renato.goldenberg@pq.cnpq.br.
Manuscript received September 2007; revised manuscript received December
2007.
ural or human-induced forest regeneration (Ellison et al. 1993;
Baider et al. 1999). While most species are shrubs or small
trees, usually preferring very moist, hilly, and forested terrain
(Ruokolainen et al. 1997), some are vines, hemiepiphytes, or
epiphytic shrubs, and a few, such as M. poeppigii, are large
trees, up to 30 m (Wurdack et al. 1993; Almeda, forthcoming).
Some species occur in areas with seasonal rainfall, and many
grow in the perpetually wet lowland rain forests. A smaller
number of species occur in deciduous forests and savannas,
but Miconia is virtually absent in the dry South American
Chaco and the Caatinga of northeastern Brazil. Most species
prefer acidic soils (Ruokolainen et al. 1997), but in the Antilles
(Judd 2007) and northern Mesoamerica, a number of species
grow on limestone or limestone-derived soils. The majority of
the species are pollinated by bees that extract the pollen by vi-
brating the poricidal anthers from nectarless flowers (Renner
1989), but there are records of pollination by bats, birds
(Dent-Acosta and Breckon 1989; Penneys and Judd 2003;
Judd 2007), flies (Goldenberg and Shepherd 1998), and wasps
(I. Varassin, personal communication) on nectar-producing
flowers (Stein and Tobe 1989), whose anthers open by slits or
large pores that do not need vibration to release the pollen.
Agamospermy occurs in some species (Dent-Acosta and
Breckon 1989; Renner 1989; Goldenberg and Varassin 2001)

963
964 INTERNATIONAL JOURNAL OF PLANT SCIENCES
and apparently is related to polyploidy and hybridization (Solt
and Wurdack 1980; Almeda and Chuang 1992; Goldenberg and
Shepherd 1998), although it is not clear how widely these mech-
anisms are distributed within the group. Self-incompatibility
has also been reported (Renner 1989; Goldenberg and Shep-
herd 1998), while dioecism occurs in 37 species (Almeda and
Dorr 2006).
Within the Melastomataceae, Miconia belongs to the tribe
Miconieae sensu stricto, as circumscribed by Michelangeli
et al. (2004), i.e., excluding Henriettea DC., Henriettella Nau-
din, Loreya DC., and Bellucia Raf., as these represent a dis-
tinct new tribe (Penneys et al. 2004). Huilaea Wurdack and
Chalybea Naudin should also be removed from the Miconieae
and transferred to the Blakeeae (Penneys 2007). The Mico-
nieae are an exclusively Neotropical clade whose species share
tissues with druse crystals (but lacking megastyloids), cymose
inflorescences that are terminal or axillary but usually not cau-
liflorous, anthers lacking pedoconnectives, unappendaged, or
with only small dorsobasal connective appendages, fleshy fruits,
and noncochleate seeds. Within the Miconieae, the genus Miconia
is clearly paraphyletic (Judd and Skean 1991; Michelangeli
et al. 2004; Martin et al. 2008). It has long been known that
genera within the tribe are poorly characterized, often difficult
to discern, or even arbitrarily defined (Baillon 1887; Cogniaux
1891; Gleason 1925a, 1932b, 1958; Macbride 1941; Wurdack
1972, 1980; Judd 1986, 1989; Judd and Skean 1991). Perhaps
the best definition for Miconia came from Judd and Skean
(1991, p. 54), who, paraphrasing Macbride (1941), stated
that ‘‘if a particular species does not fit into any of the related,
segregate genera it should be placed in Miconia.’’ The little in-
formation about chromosomes suggests a base number of
x¼17 for the entire tribe (Solt and Wurdack 1980; Almeda
and Chuang 1992; Almeda 1997), with polyploidy also occur-
ring in scattered species.
Following Cogniaux (1891) and Judd and Skean (1991),
we could define the genus Miconia as including members of
Miconieae that are woody and have these traits: nonformicarial
leaves; terminal inflorescences; hypanthium not apically con-
stricted; calyx of small lobes, not forming a stout, conical,
circumscissile cap; free petals with obtuse, rounded, or emar-
ginate apices; and anthers without a bifurcation at the base.
As in many other large angiosperm genera (Kress et al. 2005),
one is forced to recognize Miconia only by eliminating other
genera; i.e., it is distinguished only by the plesiomorphic char-
acters within the tribe (Judd and Skean 1991; Judd 2007). If
we follow the generic alignments proposed by Cogniaux (1891),
the genera most closely resembling Miconia are Clidemia
D.Don, Tetrazygia Cogn., Leandra Raddi, and Charianthus
D.Don. All five have paniculate, multiflowered, terminal, or
pseudolateral inflorescences. However, Clidemia usually has
pseudolateral inflorescences and unappendaged stamens; many
but not all species have long external calyx teeth; Tetrazygia
has a long hypanthium, with a constricted apex; Leandra (in-
cluding Platycentrum Naudin and Pleiochiton Naudin; fol-
lowing Wurdack 1984; Judd and Skean 1991) has acute petals;
and Charianthus has red pseudocampanulate corollas and ri-
mose anthers and lacks druse crystals (Penneys and Judd
2005). Also related to Miconia are Tococa Aubl. and Maieta
Aublet (both usually with leaves bearing formicaria), Anaecto-
calyx Triana (with anthers bifurcate at the base), Conostegia
D.Don (with fused calyx lobes that fall away as a circumscis-
sile cap), Pachyanthus A.Rich. (with reduced inflorescences
with flattened axes, robust hypanthia, and calyx teeth, and
often asymmetrical and clawed petals), and Calycogonium
D.Don (with four-merous flowers and shoots that produce
only one or two nodes before each ends in a few-flowered in-
florescence). Several genera, i.e., Killipia Gleason, Kirkbridea
Wurdack, Mecranium Hook.f., Ossaea DC., and Sagraea
DC., are easily distinguished from Miconia because of their
axillary (i.e., lateral) inflorescences (see Judd 1989). Hetero-
trichum DC. has not been cited above because it has serious
delimitation and nomenclatural problems (Gleason 1925b):
several species were transferred to Miconia sect. Octomeris
by Wurdack (1972), who thought that the genera should be
merged, while Judd and Skean (1991) and Liogier (2000)
considered it within Clidemia.
Miconia was described by Ruiz and Pavon in 1794, with
three species. It was under Naudin (1851) that the genus ac-
quired its present circumscription through the inclusion of
several genera. Some of these were then used as the basis of
named infrageneric taxa, such as Miconia sects. Jucunda, Cre-
manium, Chaenopleura, and Glossocentrum. Triana (1871) and
Cogniaux (1888, 1891) ‘‘improved’’ on Naudin’s sectional clas-
sification (table 1), attempting to recognize what they perceived
as related species groups. Cogniaux (1891) published what would
be the last complete revision of the genus, including 518 spe-
cies. From then on, Miconia has been studied only in regional
floras, the most important being those from Mesoamerica
(Almeda, forthcoming); Cuba (Liogier 1963); Jamaica (Proc-
tor 1972); Hispaniola (Liogier 2000); the Lesser Antilles (How-
ard 1989); Trinidad and Tobago (Williams 1928); Venezuela
(Wurdack 1973); the Guianas (Wurdack et al. 1993); Ecuador
(Wurdack 1980); Peru (Macbride 1941); and the states of Pa-
raná (Goldenberg 2004), Santa Catarina (Wurdack 1962), and
São Paulo (Martins et al. 1996) in Brazil. These studies docu-
mented the ever-expanding melastome inventory for these geo-
graphic areas, but they made no serious attempts to provide a
better circumscription of Miconia or its sections. The only no-
table exceptions to this floristic emphasis are the recent revi-
sions of sect. Hypoxanthus (former Chaenanthera; Goldenberg
2000) and of the Antillean clade of Miconia sect. Chaenopleura
(including a phylogenetic analysis; Judd 2007). Detailed sys-
tematic work has also been provided for some species groups
within Jucunda, Tamonea, and Adenodesma (Gleason 1932a).
We note that the related genera Tococa (Michelangeli 2005)
and Charianthus (Penneys and Judd 2005) have also been re-
cently monographed, and these studies have included phyloge-
netic analyses involving species of Miconia. Mecranium, which
has also been revised (Skean 1993), was the first clade within
the tribe to be the subject of a phylogenetic analysis.
The sections proposed by Cogniaux (1891) were based pri-
marily on stamen morphology, but he also used hypanthium
and calyx morphology (as well as other reproductive charac-
ters; see table 2). These sections differ markedly in size, rang-
ing from six to 248 species, and distinctions among some of
them are frequently unclear. Nevertheless, much of the taxo-
nomic confusion results from species that either were clearly
misplaced by Cogniaux or are poorly known (and thus diffi-
cult to place). There are also species (or species groups) that
have unexpected character combinations that preclude clear
 GOLDENBERG ET AL.—PHYLOGENY OF MICONIA (MELASTOMATACEAE) 965

Table 1
History of the Infrageneric Classification of Miconia
de Candolle (1828) Naudin (1851) Triana (1871) Cogniaux (1891)
Miconia sections: Miconia subgenera: Miconia sections: Miconia sections:
1. Leiosphaera 1. Adenodesma 1. Jucunda 1. Jucunda
2. Eriosphaera 2. Diplochita 2. Laceraria 2. Tamonea
3. Miconia 3. Jucunda 3. Octomeris 3. Adenodesma
4. Laceraria 4. Diplochita 4. Octomeris
Other genera: 5. Miconia 5. Miconia 5. Laceraria
Cremanium 5.1 Haplostachyae 6. Glossocentrum 6. Miconia
Diplochita 5.2. Diplostachyae 7. Hypoxanthus 6.1. Aplostachyae
Chaenopleura 5.3. Impetiolares 8. Amblyarrhena 6.2. Diplostachyae
5.4. Glomeratiflorae 9. Cremanium 6.3. Impetiolares
5.5. Stenostachyeae 10. Chaenopleura 6.4. Glomeratiflorae
5.6. Seriatiflorae 6.5. Seriatiflorae
5.7. Paniculares Other genus: 6.6. Paniculares
6. Amblyarrhena Pterocladum 7. Glossocentrum
7. Arrhenotoma 8. Chaenantheraa
8. Cremanium 9. Amblyarrhena (incl. Hartigia)
8.1. Pseudocremanium 10. Cremanium
8.2. Chiloporus 11. Chaenopleura
9. Hartigia
10. Chaenanthera
10.1. Euchaenanthera
10.2. Chaenopleura
10.3. Dichaena
a Synonymized under sect. Hypoxanthus by Goldenberg (2000).

assignment to any existing section. Finally, most sections have
no designated types, except for sects. Chaenopleura and Ta-
monea, whose names came from genera that were described
based on single species, and sect. Hypoxanthus, whose type
has been designated only recently (Goldenberg 2000). For ex-
ample, sect. Jucunda comes from the genus described by Cha-
misso (1834), with six species, all of them synonimized under
three other species by Cogniaux (1891), of which only two were
placed by him within sect. Jucunda; he considered the third
in sect. Miconia. Section Miconia was established by de Can-
dolle (1828) with 51 species, and these were placed in several
different sections in the classification proposed by Cogniaux
(1891). Given these taxonomic factors, it is not possible to
use the type species as stakes to position the sections in the
trees. Instead, we have adopted, for the purposes of this arti-
cle, the sectional circumscriptions of Cogniaux (1891; as slightly
modified by Goldenberg [2000]) because his monograph is the
only current comprehensive taxonomic treatment of Miconieae.
The most compelling rationale for attempting this study is
that we now have modern techniques at our disposal to criti-
cally analyze difficult paraphyletic groups and make progress
in identifying their component clades. While poorly defined,
Miconia has an astonishing number of species, and these are
often conspicuous members of the Neotropical flora. In the
absence of modern taxonomic treatments, we lack a phyloge-
netic perspective not only of variation in traditionally em-
ployed morphological features (e.g., inflorescence architecture,
hypanthium shape, or staminal features such as the form of
the pores/slits or connective appendages) but also of more
difficult-to-access features such as pollen, secondary chemis-
try, and chromosome numbers. As systematists, we are faced
with some practical difficulties. How do we begin to determine
(and diagnose) the most significant clades within an obviously
nonmonophyletic Miconia? And how are we going to deal with
this large slice of melastome—and also angiosperm—diversity?
Because we cannot work on a ‘‘ground zero’’ basis, i.e., simply
throw away the taxonomic information that is available, we
present here the available phylogenetic data on Miconia and
compare them with the existing infrageneric classification. In
addition, various clades within Miconia will be compared to
other genera in the tribe.
Material and Methods
Taxon Sampling
The appendix in the online edition of the International Jour-
nal of Plant Sciences contains all of the names, voucher infor-
mation, and GenBank accession numbers for the 481 sequences
of the internal transcribed spacer region of the nuclear ribo-
somal DNA (nrITS) and the 247 sequences of ndhF included
in this study. The nrITS data set includes 21 species of Meria-
nieae, one species of Eriocnema, and 459 accessions from the
Miconieae. These 459 sequences correspond to 449 species
because multiple infraspecific taxa were included for three
species and five widely distributed and highly variable species
of Miconia (Miconia calycina, M. dodecandra, M. minutiflora,
M. mirabilis, and M. theaezans) are represented by multiple se-
quences. Additionally, another 22 species were sequenced for
 Table 2
Sectional Features as Defined by Cogniaux (1891)
Anthers (shape, glands, Hypanthium
Section dehiscence, length)a (shape, length) Calyx (dehiscence, lobes) Others
Jucunda (Cham.)
Triana (24) Elongate, linear-subulate, falcate, Oblong, 2–7 mma Open in bud, lobes triangular to lanceolate Petals frequently subacute
not glandulose, one minute pore,
2.7–9 mm
Tamonea Cogn. (71) Elongate, linear-subulate, falcate, Oblong, 2–7.5 mm Open in bud, lobes absent or denticulate Petals obtuse to retuse
not glandulose, one minute pore,
2–11 mm
Adenodesma (Naudin)
Cogn. (6) Elongate, linear-subulate, flexuose, Oblong, 3.8–6.5 mm Open in bud, lobes absent or short Leaves sessile
glandulose, one minute pore, 2.6–8 mm
Octomeris (Naudin)
Benth. & Hook.f. (58) Elongate, linear-subulate, not glandulose, Campanulate, 2.5–8 mm Open in bud, lobes irregular or triangular
one minute pore, 1.1–10 mm
Laceraria (Naudin)
Triana (21) Elongate to linear-subulate, not Campanulate, 1–2.3 mm Closed in bud, opening through irregular
glandulose, one minute pore, .9–2 mm lobes
Miconia DC. (248)b Short, linear, straight, apex attenuate, Campanulate to hemispheric, Open in bud, lobes obsolete or triangular Connective with ventral
one or two minute pores, 1–5 mm 1.2–4 mm appendages
Glossocentrum (Crueger)
Hook.f. (84) Short, linear, straight, apex truncate, Campanulate to hemispheric, Open in bud, lobes short Connective lacking or only
one or two large pores, .7–4 mm .8–4 mm with a dorsal appendage
Hypoxanthus (Rich. Ex
DC.) Hook.f. (17) Short, linear, straight, one or two Campanulate to hemispheric, Open in bud, lobes obsolete or triangular Connective lacking or only
rimose, .4–2.3 mm .9–2.4 mm with a dorsal appendage
Amblyarrhena (Naudin)
Triana (206) Very short, wide, obovate to oblong, Campanulate, 1.3–6 mm Open in bud, lobes obsolete or short Panicles regular
straight to slightly arcuate, apex obtuse
to retuse, one minute pore, .8–4.3 mm
Hartigia Griseb. (8)c Very short, wide, obovate to oblong, Campanulate, 1.3–2.2 mm Open in bud, lobes obsolete or short Panicles scorpioid
straight to slightly arcuate, apex obtuse
to retuse, one minute pore, 1.3–1.9 mm
Cremanium (D.Don)
Hook.f. (209) Very short, subcuneate, straight, apex Wide-campanulate, .7–4.5 mm Open in bud, lobes obsolete or short
rounded to retuse, two to four large
pores, .3–2.7 mm
Chaenopleura (Rich. ex
DC.) Hook.f. (87) Very short, obovate or cuneate, apex Suburceolate, 1.3–6 mm Open in bud, lobes short
obtuse, pore ventrally prolonged into
one or two slits, .4–3.2 mm
Note. The number of species appears in parentheses after each section name (following Goldenberg 2000).
aMeasurements based on work by Wurdack (1962, 1973, 1980), Martins et al. (1996), Goldenberg (2000), Judd (2007), and Almeda (forthcoming).
b Cogniaux (1891) recognized six subsections (see table 1) based on inflorescence and leaf morphology. The distinctions of these subsections are insignificant, and subsequent students of

Miconia did not assign new species to any of the subsections.

c Hartigia has been treated as a subsection of Amblyarrhena by Cogniaux (1891) but is discussed apart from it in this article.
 GOLDENBERG ET AL.—PHYLOGENY OF MICONIA (MELASTOMATACEAE)
multiple accessions but are represented here by a single se-
quence each because there was no intraspecific variation
in those cases. Within the Miconieae, the sampling spans 16
genera (only Catocoryne, Killipia, and Kirkbridea were not
sampled). The four genera (Cyphostyla, Allomaieta, Alloneuron,
and Wurdastom) assigned to tribe Cyphostyleae (Gleason
1929) and placed in Miconieae by Renner (1993) also were
not sampled here. Miconia is represented by 218 sequences
from 212 taxa and 208 species (;20% of the species of Mico-
nia). All sections of Miconia were sampled (sectional placement
following Goldenberg 2000): Adenodesma (3 spp. sampled),
Amblyarrhena (24 spp.), Hypoxanthus (9 spp.), Chaenopleura
(29 spp.), Cremanium (28 spp.), Miconia (52 spp.), Glosso-
centrum (22 spp.), Hartigia (4 spp.), Laceraria (4 spp.), Octo-
meris (11 spp.), Tamonea/Jucunda (19 spp.), and incertae sedis
(3 spp.). The ndhF data set is a subset of the nuclear data
set containing 13 species of the Merianieae and 234 species
of the Miconieae (145 from Miconia; again, all sections were
sampled).
The tribe Merianieae has been chosen here as the outgroup
because it has repeatedly been shown to be sister to the Mi-
conieae sensu stricto (Clausing and Renner 2001a, 2001b;
Renner et al. 2001; Fritsch et al. 2004; Michelangeli et al.
2004; Renner 2004) and including taxa from more distantly
related tribes rendered the alignment of the nrITS data prob-
lematic. Preliminary analyses of more than 300 sequences of
ndhF spanning the entire family confirmed the sister relation-
ship of Merianieae and Miconieae. Additionally, Eriocnema,
a capsular-fruited taxon from Brazil that has been tradition-
ally placed in the Microliceae, was included in this analysis
because it has been shown to be sister to the remaining mem-
bers of the Miconieae (Fritsch et al. 2004; Martin et al. 2008).
Most of the genomic DNA used in this study was isolated
from silica-dried leaf tissue, but herbarium material was used
for ;8% of the taxa. DNA extractions were performed using
the Qiagen DNeasy plant mini kit, following the manufac-
turer’s protocol with the addition of 30 mL of Proteinase K
(20 mg/mL) and 30 mL of b-mercaptoethanol to each sample
along with the AP1 buffer. The homogenate was incubated at
42°C for 12 h, with slow rocking. Alternatively, the glass milk
DNA extraction method, as outlined by Struwe et al. (1998),
was employed. For some samples that were hard to amplify,
the glass milk extraction method was used to clean DNA iso-
lated with the DNeasy kit.
The nrITS was amplified using specific primers, as detailed
by Michelangeli et al. (2004). PCR was performed in a 25-mL
volume with the following reaction components: 0.8 mL tem-
plate DNA (;30 ng/mL), 2.5 mL 10X Ex Taq buffer (Takara
Bio), 0.2 mM dNTP mixture, 6.5 mg BSA, 1 mmol of each primer,
2 units of Takara DNA polymerase (Takara Bio), and 5% (v/v) of
DMSO. The PCR parameters were 94°C for 5 min and 35 cycles
of 94°C for 10 s, 50°C for 45 s, and 72°C for 50 s, followed by
72°C for 10 min.
The ndhF gene was amplified with primers developed by
Olmstead and Sweere (1994). Following Clausing and Ren-
ner’s (2001b) study, we amplified the 39 end of the gene between
positions 972 (i.e., codon 305 of solanaceous sequences) and
1955, using forward primer ndhF-972F, reverse primer ndhF-
1955R, and one or two pairs of internal primers (ndhF-1318F,
ndhF-1318R, ndhF-1603F, and ndhF-1603R). Sequencing condi-
967
tions and reagents were similar to those used for the internal
transcribed spacer (ITS), but the annealing temperature was set
to 48°C, and DMSO was not included. Alternatively, a similar
PCR program was run with 10 initial cycles with an annealing
temperature of 45°C, followed by 25 cycles with an annealing
temperature of 48°C.
Cycle sequencing reactions were performed with the same
PCR primers, using ABI Prism Big Dye 3.1 terminator cycle
sequencing kit (Perkin Elmer, Norwalk, CT), and were then
analyzed with an Applied Biosystems 377XL automated DNA
sequencer. Resulting sequences were edited using Sequencher
4.5 (GeneCode, Ann Arbor, MI).
Sequence Alignment and Phylogenetic Analyses
The complete matrix was initially aligned using CLUSTAL
X (Thompson et al. 1997) and then adjusted manually, espe-
cially at the edges of large insertions/deletions (indels). Data
editing, manual alignment, tree viewing, and character opti-
mization were performed in WinClada (Nixon 1999–2002).
Indels were coded using the ‘‘simple gap coding’’ method of
Simmons and Ochoterena (2000), as implemented in 2xRead
(Little 2005).
Three phylogenetic analyses were conducted using the
parameters described below: the nuclear (ITS) and plastid
(ndhF) data sets were each analyzed separately and in a com-
bined analysis, using all nrITS and ndhF sequences. All maxi-
mum parsimony analyses were performed with TNT (Goloboff
et al. 2001). One thousand random addition sequence repli-
cates holding 20 trees per replicate were conducted. Each start-
ing tree was first exhaustively swapped with subtree pruning
and regrafting, then tree bisection reconnection (TBR), and
was then subjected to a 200-iteration ratchet (Nixon 1999).
The ratchet used a probability of 5 for both up-weighting and
down-weighting; 10% of the informative characters were re-
weighed for each replicate (other parameters were set to default).
After the random addition sequences were complete, trees were
swapped to 750,000 trees using TBR.
Strict consensus jackknife support values were calculated
from 1000 replicates (Farris et al. 1996). Each replicate was
performed with 20 random taxon entry sequences and swapped
using the parameters described above. Branches were collapsed
if supported ambiguously. The consensus tree was retained from
each replicate.
Results
The aligned nrITS data matrix is 1050 bp long, of which 387
sites are potentially informative. Simple gap coding yielded 321
indels, of which 183 are potentially informative. The aligned
ndhF data matrix is 1000 bp long, with 154 potentially infor-
mative sites. Nineteen gaps were coded, and only four are po-
tentially informative.
All phylogenetic analyses were stopped once 750,000 most
parsimonious trees (MPTs) were stored and memory capacity
was reached. MPTs of the nrITS analysis have length ðLÞ ¼ 3171,
consistency index ðCIÞ ¼ 0:27, and retention index ðRIÞ ¼ 0:75,
and in the strict consensus, 256 nodes are collapsed (not shown).
The ndhF analysis yielded MPTs of L ¼ 486, CI ¼ 0:47, and
968 INTERNATIONAL JOURNAL OF PLANT SCIENCES
RI ¼ 0:79, and 181 nodes (for 247 taxa) are collapsed in the strict
consensus (not shown). In both analyses, Miconieae (including
Eriocnema) is resolved as monophyletic. In the ndhF analysis,
there is very little resolution within Miconieae, but the resulting
clades are not in conflict with those present in the strict consensus
of the nrITS analysis. The combined analysis yielded MPTs of
L ¼ 3818, CI ¼ 0:28, and RI ¼ 0:74, and in the strict consensus,
209 nodes are collapsed (figs. 1–3). Even though jackknife support
values are not particularly high along the spine of the tree, they
are considerably higher in the combined analysis than in the nrITS
analysis alone for all clades. Because there is no hard conflict be-
tween the nuclear analyses and the plastid analyses or between
these and the combined analysis and because the combined analy-
sis both is the best resolved and has the highest support values,
from here on, we will discuss only the results of the combined
analysis.
Species of Miconia are present in almost every clade within
Miconieae(figs. 1–3). They are absent only from the Leandra þ
Ossaea (scorpioid), Tococa, and Ossaea p.p. clades, which will
not be discussed in detail here. On the other hand, they can
be regarded as the major components of at least four clades
(Miconia I-IV) and one grade (Miconia V). In the other parts
of the cladogram, species of Miconia occur in small subclades
or are scattered among species from other genera, as in the
Caribbean þ Conostegia, Mecranium þ allies, and Leandra s.s.
clades and the Clidemia grade. Approximately 85% (188 out
of 220) of the terminals sampled here that belong to Miconia
are in the five clades and grade (Miconia I–V), which also
include all species from sects. Tamonea/Jucunda, Laceraria,
Chaenopleura, Glossocentrum, Hypoxanthus, and Adenodesma;
almost all species from sects. Cremanium and Amblyarrhena
(excluding Hartigia); and most terminals from sect. Miconia.
Thus, the only Miconia groups that are absent or unimportant
in these clades are sect. Hartigia (formerly in sect. Amblyarrhena)
and sect. Octomeris (including the species transferred from
Heterotrichum).
The Miconia I and II clades are the basalmost branches in
the tribe, and both are composed exclusively of species of
Miconia. Miconia I has three species from sect. Tamonea and
also one from sect. Miconia. Miconia II has three out of the
four sampled species from the small sect. Laceraria.
The Caribbean þ Conostegia clade consists of a grade
made up of mainly species and small clades from the Antilles,
from the genera Miconia and Ossaea (with some of the latter
often considered within Leandra), and all sampled species of
the genera Calycogonium, Tetrazygia, Pachyanthus, and Char-
ianthus. This clade also has a subclade with northern South
American and Central American species, with all sampled spe-
cies of Conostegia included, plus a few species of Leandra, Cli-
demia, Miconia, and Tococa. The species of Miconia in this
large clade belong to sects. Cremanium and Octomeris, both at
the base of the grade, and also a small clade with six Cuban
and Puerto Rican species from sects. Octomeris, Amblyarrhena,
and incertae sedis, along with two species from other genera. In
the Conostegia subclade, there are four species of Miconia,
from sects. Miconia and Octomeris, and one incertae sedis.
The Mecranium þ Anaectocalyx þ allies clade contains a
grade made up of primarily species and small clades from
Miconia, Tococa, and Clidemia, plus all sampled species of
Anaectocalyx and Mecranium. The species of Miconia belong to
sects. Amblyarrhena, Hartigia, and Octomeris. The species in
this clade either are restricted to the Greater Antilles (Mecra-
nium) or northwestern South America (Miconia pulvinata,
M. spinulosa, and M. ulmarioides) or are widespread but with
a strong Antillean and Central American presence (M. racemosa,
M. ciliata, and M. lacera).
Miconia III is made up by mainly Andean, Central American,
and Antillean species of Miconia, from sects. Chaenopleura,
Cremanium, and Amblyarrhena, plus single species from sects.
Octomeris and Miconia and a few from Leandra and Clidemia.
All species sampled from Chaenopleura are included in this
clade, with all Greater Antillean species except for two (M.
selleana and M. stenobotrys) plus one from Central America
(M. grandidentata) in one subclade. The Andean and Central Amer-
ican species of sects. Chaenopleura, Cremanium, and Amblyar-
rhena are interdigitated and dispersed across the grade at the
base of the clade, with at least four species of sect. Chaeno-
pleura in a monophyletic subgroup (including the most recent
common ancestor [MRCA]—of M. bullata and M. latifolia).
Almost all species from sects. Cremanium and Amblyarrhena
sampled in this study belong to this clade, with some excep-
tions in clades Miconia IV and Caribbean þ Conostegia for
Cremanium and in several places for Amblyarrhena. The clado-
gram shows no resolution among species from these two sec-
tions or among the Andean Chaenopleura.
Miconia IV has 69 terminals, with all but four (all from Cli-
demia) belonging to Miconia. These consist of species mainly
from sects. Tamonea/Jucunda, Miconia, and Glossocentrum
but also part of sect. Hypoxanthus, the extra-Andean South
American species from sect. Cremanium, and one species each
from sects. Laceraria and Octomeris. The distribution of the
species based on traditional sectional assignments does not fol-
low a clear pattern. For instance, the five extra-Andean mem-
bers of sect. Cremanium are in three different subclades, while
the three species of sect. Hypoxanthus are in two subclades.
Nevertheless, species from sect. Tamonea/Jucunda always seem
to cluster with species from sect. Miconia, and similarly, species
of sect. Glossocentrum often are placed as close relatives of
others in sect. Miconia. This group has a strong geographical
presence in extra-Andean South America, with some wide-
spread species reaching Central America and the Caribbean
and one small lineage (M. striata and allies) from the Lesser
Antilles and adjacent South America. The subclades including
the MRCAs of M. rubiginosa/M. ligustroides and M. discolor/
M. cinerascens have mostly eastern Brazilian and Amazonian
species, along with some widespread ones (i.e., M. chrysophylla,
M. albicans, and M. stenostachya). The subclade including the
MRCA of M. smaragdina and M. magdalenae contains the
type of the genus, M. triplinervis, and is composed mostly of
species from sect. Miconia from the Andes, Mesoamerica, or
the Antilles; however, some species within this subclade are
currently assigned to other sections or occur in extra-Andean
South American regions.
The Miconia V grade is composed of three clades. The first
is composed of Clidemia heptamera and two species of Mico-
nia, these from sects. Amblyarrhena and Miconia. The second
is made up of species of mainly Leandra (mostly sect. Tschu-
dya; see Martin et al. 2008) and M. ceramicarpa (sect. Mico-
nia), mostly from the Guayana Shield. The large third clade
has species of Miconia, mainly representatives of sects. Tamonea/
 Fig. 1 Strict consensus tree resulting from the combined analyses of nrITS and ndhF sequence data. Numbers above the branches correspond
to estimated jackknife support. Sectional assignments within Miconia are indicated by color (see legend at the bottom of the figure). All names in
black belong to other genera. One asterisk indicates the type of the genus Miconia; two asterisks indicate the type of a section.
Fig. 2 Strict consensus tree (continued).

970
Fig. 3 Strict consensus tree (continued).

971
972 INTERNATIONAL JOURNAL OF PLANT SCIENCES
Jucunda and Miconia, and also species of sects. Glossocen-
trum and Hypoxanthus, all three species sampled from sect.
Adenodesma, and one eastern Brazilian species of sect. Am-
blyarrhena. The geographical distribution of the species fol-
lows the same pattern found in Miconia IV: all but one (M.
ernstii, from Dominica) are from extra-Andean South America,
plus several widespread species.
The Clidemia grade has many isolated species and small
clades composed of species of Clidemia, Leandra, Miconia,
Leandra, Tococa, and Maieta, plus a large clade (including
the MRCA of Sagraea capillaris and Clidemia septuplinervia)
with several species of Clidemia, plus some from Ossaea, Sa-
graea, and the monospecific Necramium. All the eight species
of Miconia in this grade belong to sect. Miconia, but these
species are not placed together in the cladogram.
Finally, the Leandra s.s. clade has only a single sampled spe-
cies of Miconia (sect. Octomeris). The remaining species of this
clade, which are from eastern Brazil, belong mainly to Lean-
dra, but a few species of Clidemia, Ossaea, and Pleiochiton are
also placed here.
Discussion
The best way to evaluate morphological character evolution
would be to produce a complete morphological character ma-
trix parallel to the molecular matrix, and this is currently un-
der way. Because of the large number of taxa in this study and
the fact that most of the anatomical and seed morphology por-
tion of this study is just beginning, at this point, we will be dis-
cussing only those morphological characters that have been
traditionally used in delimiting genera within the Miconieae
and sections within Miconia or characters currently known to
support more inclusive clades.
The sections of Miconia provide an efficient way to summa-
rize morphological characters and can be used as a proxy for
character distribution through the group (see table 2). This is
especially true for the stamens, which have been extensively
used to define these groups (Triana 1871; Cogniaux 1891;
Goldenberg et al. 2003; Judd 2007). For instance, long, sub-
ulate, and minute-pored anthers occur in sects. Jucunda, Ta-
monea, Octomeris, and Adenodesma (fig. 4A, 4B, 4D), the
latter also bearing glands on the connective. Shorter and linear
anthers occur in sects. Miconia (still minute pored and with con-
nective appendages ventrally projecting; fig. 4P, 4Q), Glossocen-
trum (broad pored and connective unappendaged or with a
dorsal appendage; fig. 4G, 4H), and Hypoxanthus (broad, ven-
tral pores resembling slits that expose two locules; fig. 4L–4O).
Finally, short and cuneate or obovate anthers occur in sects. Am-
blyarrhena and Hartigia (with tiny apical pores; fig. 4C), Crema-
nium (with two to four broad pores; fig. 4E, 4F), and
Chaenopleura (opening through slits that expose four locules;
fig. 4I–4K).
The Sections of Miconia with Elongate Anthers
Sections Jucunda, Tamonea, Adenodesma, and Octomeris
have been regarded as basally branching groups within the
genus or even the tribe as a whole (J. J. Wurdack, personal
notes; Judd and Skean 1991). This hypothesis was probably
based on their relatively large flowers (table 2), somewhat re-
sembling those in many genera outside Miconieae, and the
absence of specialized features (mostly involving the sta-
mens). In part, these authors were correct because Miconia I
is composed mostly of species of sect. Tamonea, but it is dif-
ficult to explain why the other species sampled from the first
three sections are positioned in Miconia IV and V. Neverthe-
less, these species are frequently positioned in basal grades or
basally within each clade or subclade in our trees. The same
pattern can be found, with some exceptions, in sect. Octomeris, in
the Caribbean þ Conostegia and Mecranium þ Anaectocalyx þ
allies clades. Wherever there is a species of sect. Tamonea/Jucunda
at the base of a clade, there is not one from sect. Octomeris, and
vice versa. Also, wherever there is a species of sect. Tamonea/
Jucunda at the base of a grade or clade, it is almost always related
to species from sect. Miconia and rarely related to species in the
predominantly West Indian/Andean clades with species from sects.
Cremanium, Amblyarrhena, and Chaenopleura. The opposite is
true for the basally placed species of sect. Octomeris, which are al-
most never related to species from sect. Miconia but are frequently
related to species from Cremanium, Amblyarrhena, and Chaeno-
pleura. If one considers the position of these species of sects. Ta-
monea/Jucunda and Octomeris, then it may be logical to assume
that they could have retained an array of ancestral character states
(for the tribe), and thus, the traditional circumscription of these
sections may have been based on these symplesiomorphic charac-
ters. Judd and Skean (1991) stated that almost every specialized
line in Miconieae has basal species that in some way resemble
those in sect. Tamonea/Jucunda or Octomeris. The same authors
also noted that the difficulties found in the delimitation of groups
within Miconieae are due to the lack of morphological gaps,
which could be related to rapid diversification from a basal com-
plex, coupled with the lack of extinctions.
The difficulty in defining the boundary between the Tamonea/
Jucunda complex and sect. Miconia was emphasized by Golden-
berg (2000). These problematic boundaries could be the result
of mistaken/careless sectional placements of species by previous
authors. We suspect, however, that a more likely explanation is
that the lack of a clear distinction between these three sections
(as evidenced by the placement of their species on our clado-
grams) relates to multiple and parallel evolutionary shifts in the
size and shape of flowers and stamens, probably correlated with
pollination modes. This may have led to the independent and
convergent origin of several lineages with smaller flowers and
stamens (leading to the divergent placements of such species that
we see in our trees).
The small sect. Adenodesma may be monophyletic; it is sup-
ported by at least one distinctive morphological synapomor-
phy, glands on the stamen connective (see Gleason 1932a). It
has been regarded as a part of the Tamonea/Jucunda complex
(Gleason 1925a, 1932a), but in our cladogram, it is more
closely related to species of sect. Miconia, within a grade that
includes some species of the Tamonea/Jucunda complex.
From a phylogenetic perspective, Miconia sect. Octomeris
makes little sense, and the species traditionally assigned to
this section are placed throughout several clades and are al-
most never paired with other members from the same section.
Judd and Skean (1991) suggested the transfer of some of its spe-
cies to Clidemia and others to early-divergent lineages within
 GOLDENBERG ET AL.—PHYLOGENY OF MICONIA (MELASTOMATACEAE) 973

Fig. 4 Stamens of Miconia. A, Miconia tomentosa (Rich.) D.Don (Lugo 4144, CAS); B, M. tuberculata (Naudin) Triana (Aymard 1848, CAS);
C, M. livida Triana (Wallnoffer 113–21782, US); D, M. jucunda (DC.) Triana (Tozzi 94–232, UEC); E, M. hymenanthera Triana (Asplund 16222,
US); F, M. theaezans (Bonpl.) Cogn. (Leitão-Filho 11873, UEC); G, M. cinnamomifolia (DC.) Naudin (Goldenberg s.n., UEC); H, M. tetragona
Cogn. (Vásquez 6864, US); I, M. hypiodes Urb & Ekman (Ekman 7552, US); J, M. bullata (Turcz.) Triana (Luteyn 6446, US); K, M. melanotricha
(Triana) Gleason (Standley 51574, US); L, M. chrysophylla (Rich.) DC. (Plowman, 12294, US); M, M. sellowiana Naudin (Glaziou 8690, BR); N,
M. sellowiana Naudin (Araújo 723, UEC); O, M. pusilliflora (DC.) Naudin (Goldenberg 37, UEC); P, M. tetrasperma Gleason (Vásquez 4747,
US); Q, M. tiliaefolia (Hutchinson 8655, US). Assignment of the species follows Cogniaux’s (1891) sections: A, Adenodesma; B, Octomeris; C,
Amblyarrhena; D, Jucunda; E, F, Cremanium; G, H, Glossocentrum; I–K: Chaenopleura; L–O, Hypoxanthus; P, Q, Miconia.

Tetrazygia. Within sect. Octomeris, several species resemble some
members of sect. Amblyarrhena (i.e., those having campanulate
hypanthia and stout, minute-pored anthers) but have larger flow-
ers and anthers (table 2). Polyphyly explains the proximate posi-
tions of some species of sects. Octomeris and Amblyarrhena (and
Hartigia) in several places in the cladogram. The small subclade
including the MRCA of Miconia pachyphylla and Pachyanthus
moaensis in the Caribbean clade is the only part of the cladogram
where two species of Octomeris are placed together and in de-
rived positions along with species from other sections. All the spe-
cies from this distinctive clade are from Cuba and Puerto Rico and
have moderate-sized flowers, obovate to spathulate petals, strongly
fused calyx lobes, few-seeded fruits, and—most notably—either
basal or, less commonly, axile placentation with the placental tis-
sue reduced (but nonreduced in Pachyanthus monocephalus; E.
Becquer, personal observation). Most are shrubs from strongly sea-
sonal areas and occur on limestone soils, as is also characteristic
of many other species within the Caribbean þ Conostegia clade.
Finally, the two eastern Brazilian species of sect. Octomeris are re-
solved in very distant clades: M. octopetala belongs to the Miconia
974 INTERNATIONAL JOURNAL OF PLANT SCIENCES
IV clade, and its flowers look like larger versions of those of spe-
cies of sect. Glossocentrum; it also has the hairy leaves and glomer-
ulate inflorescences that apparently are shared among several
species in the clade. Miconia plumosa has glandular trichomes and
narrow petals with a rounded tip, and it is not surprising that
it is resolved within the Leandra s.s. clade, which consists of
mainly eastern Brazilian species of Leandra (Martin et al.
2008).
The small sect. Laceraria was established for a group of spe-
cies with a fused, irregularly rupturing calyx, a condition that
is known for several other species of Miconia (Kriebel et al. 2005;
Almeda, forthcoming) that have been variously assigned to sects.
Amblyarrhena, Laceraria, and Miconia. Within the tribe, Cono-
stegia also has a calyx that is closed in bud, but it ruptures cleanly
along a well-defined circumscissile line and then falls away as a
cap. The fact that three of the four species in the section form a
monophyletic group shows that this character may be a useful
synapomorphy, although its presence also in M. striata (of Mico-
nia IV), M. friedmaniorum (of the Conostegia clade), and some
species of Clidemia and Tococa not sampled here indicates that it
has arisen more than once within the genus and tribe. A similar
condition is exhibited by M. rubiginosa (of Miconia IV), which
has a calyx tube and lobes that are circumscissile and collectively
fall away as a ring on fruiting hypanthia. An irregularly rupturing
calyptrate calyx is a putative synapomorphy of Mecranium (in the
Mecranium þ Anaectocalyx þ allies clade).
Although it is evident from the above discussion that the spe-
cies of Miconieae with elongate anthers constitute an extremely
polyphyletic assemblage, having representatives in widely di-
vergent positions in our cladograms (see figs. 1–3), many of
these species do form a clade (i.e., those occurring primarily in
the Caribbean region). The Caribbean clade exhibits extensive
morphological diversity; major subclades include the core Tetra-
zygia (including the MRCA of Tetrazygia bicolor and Tetra-
zygia cristalensis), Charianthus (Penneys and Judd 2005), the
core Pachyanthus (including the MRCA of Pachyanthus cuben-
sis and Pachyanthus tetramerus), and the basal placentation-
reduced placenta clade (including the MRCA of M. pachyphylla
and P. moaensis; see Becquer-Granados et al. 2008). Finally,
Conostegia, a well-defined genus whose species often have pleio-
stemonous flowers and lack external calyx lobes, with the inner
lobes fused into a stout, conical calyptra (Schnell 1996), is also
apparently related to these Caribbean taxa.
Miconia Sects. Amblyarrhena, Cremanium, and
Chaenopleura and the Andean/Central
American/Antillean clade
All species from sect. Chaenopleura and the majority from
sects. Cremanium and Amblyarrhena belong to a single clade
(Miconia III). These three sections account for ;500 species,
close to half of the described species of Miconia. Except in the
Antillean Chaenopleura subclade, the relationships among the
species in this clade are unclear. Nevertheless, this clade ex-
hibits strong geographical cohesion. As mentioned, a distinct
subclade is restricted to the Antilles, and the remaining species
occur in the Andes or Central America, along with the wide-
spread M. theaezans. The species of sect. Chaenopleura in the
Greater Antilles represent a major radiation of the family in
this region (Michelangeli et al. 2008) and are resolved as a
monophyletic group with an actinomorphic androecium of
white stamens with erectly held, obovate anthers that open by
two longitudinal slits exposing the contents of the four locules,
pale blue berries, and seeds with a smooth testa (Judd 2007).
The presence of a radially symmetrical androecium and usually
white anthers is shared with the related species of sect. Crema-
nium. The phylogenetic proximity between Andean/Central Amer-
ican Chaenopleura and Cremanium already has been suggested by
Gleason (1925a) and Judd and Skean (1991), but some species,
such as M. nigricans (Peru) and M. melanotricha (Costa Rica and
Panama), resemble certain Antillean ones in vegetative features. A
close relationship between Andean species of sects. Chaenopleura
and Cremanium was also supported by the preliminary cladistic
analysis of Judd (2007), and in that analysis (based on ITS se-
quences), the Antillean species of sect. Chaenopleura form a clade
nested within a paraphyletic sect. Cremanium. Miconia tetrastoma
(an Antillean species of sect. Cremanium) is resolved here within
the Antillean Chaenopleura clade but has been previously placed
with other species from Cremanium (see Judd and Penneys 2004;
Judd 2007). The phylogenetic position of M. desportesii and M.
sphagnicola, which may be close relatives of M. tetrastoma, is in
need of additional study (Judd and Penneys 2004).
As for the rest of the clade, it seems that all species share
the characteristic short, stout anthers, but the mode of dehis-
cence has evolved in at least two different ways: either the
two to four broad-pored Cremanium type (sometimes ven-
trally inclined and resembling longitudinal slits in those spe-
cies assigned to sect. Chaenopleura) or the single small-pored
Amblyarrhena type, although intermediates occur. Broader
character sampling among these groups could determine
whether the species of Amblyarrhena and Cremanium belong
to distinct clades and how many times broad-pored or small-
pored anthers have evolved. Also, studies of pollination ecol-
ogy may help us understand the selective pressures driving
changes in anther morphology because these species probably
lack nectar and offer only pollen as a reward. The way that
pollen is collected from the anthers by visitors must be differ-
ent because the size of the pores is different. Wind may also
help to facilitate pollen removal from broad-pored anthers
(F. Almeda, personal observation).
Some species of sect. Cremanium that are distributed out-
side the Andes and Central America are not resolved in Mico-
nia III. The eastern Brazilian species of sect. Cremanium were
placed by Cogniaux (1891) in this section because their an-
thers have two broad pores. However, their anthers are not
short and cuneate, as are those of their Andean counterparts,
but slender and oblong, and they resemble those of sect. Glos-
socentrum. In fact, the number of pores, whether one or two,
is sometimes difficult to assess because it depends solely on
the persistence, thickness, and degree of protrusion of the sep-
tum between the two thecae (see Goldenberg et al. 2003).
Also M. tetrandra, from the Antilles, has anthers that are
more slender than those of core Cremanium, despite its large
pores. In the same way, the only Brazilian species from sect.
Amblyarrhena (M. ramboi) is placed in the Miconia V grade,
along with species from the same region that belong to other
sections. This species and other Brazilian Amblyarrhena (M.
paradoxa and M. penduliflora; not sampled for this study)
have anthers that do not look like their Andean counterparts;
 GOLDENBERG ET AL.—PHYLOGENY OF MICONIA (MELASTOMATACEAE) 975

instead they are similar to those of species of sect. Miconia and Glossocentrum. The species of sect. Miconia are always inter-
but shorter and thicker. mixed with species of sects. Tamonea/Jucunda, Glossocentrum,
and Hypoxanthus and the few species of eastern Brazilian Crema-
Section Hartigia and Relatives in the Mecranium, nium, Octomeris, and Amblyarrhena. They are also frequently
Anaectocalyx, and Allies Clade mixed with species of Clidemia, Leandra, and even Conostegia.
Cogniaux (1891) divided sect. Miconia into six subsections based
The distinction of Hartigia as a section apart from Amblyar-
largely on inflorescence morphology. An attempt to plot these sub-
rhena seems to be correct because all its species belong to a sin-
sections onto the cladogram (not depicted) showed that they do
gle subclade within the Mecranium þ Anaectocalyx þ allies
not deserve further consideration.
clade. The distribution of these species agrees with that of their
The Ossaea p.p. clade (¼Ossaea sect. Octopleura) is placed
counterparts in the clade: all come from Central America and
as the sister group of Miconia IV (which includes many species
northern South America, as well as the Antilles, and there is at
of sect. Miconia), and both groups contain many species with
least one widespread species (M. ciliata). The two morphologi-
ribbed hypanthia and dorsobasal anther appendages (these
cal characters that define Hartigia occur elsewhere in the tribe
are sometimes gland edged). These features could be synapo-
but not together. The first one is the scorpioid inflorescence,
morphic, and this clade is discussed in more detail by Judd
which has apparently evolved in only two other clades within
and Skean (1991).
Miconieae (twice in Miconia IV and in the scorpioid Leandra þ
The species of sect. Glossocentrum are placed in three differ-
Ossaea clade). This unusual inflorescence architecture may
ent regions of the cladogram: M. rubiginosa and M. discolor
help to position reproductive structures in a way that optimizes
subclades in Miconia IV and the large subclade including the
pollination and fruit dispersal. In some species with scorpioid
MRCA of M. furfuracea and M. rigidiuscula in Miconia V. The
inflorescences, the flowers are somewhat congested at anthesis,
species with glabrous to glabrescent leaves and regular panicles
but the inflorescence axes lengthen in fruit. Thus, flowers can
(i.e., nonglomerulate and nonscorpioid inflorescences) are re-
be offered close to each other for pollinators, but the fruits are
stricted to the M. rubiginosa and M. furfuracea subclades, and
offered individually for the dispersers. The second character is
they have remarkably similar inflorescences and vegetative
the short, stout, and minute-pored anthers. Similar anthers ap-
characters. On the contrary, all the species in the M. discolor
parently evolved at least twice in the Mecranium þ allies clade
subclade have hairy abaxial leaf surfaces and glomerulate or
and perhaps more than once in Miconia III.
scorpioid inflorescences.
A related, well-supported clade is represented by Mecra-
The species sampled from sect. Hypoxanthus come out in
nium, a group that is easily distinguished from the species of
the same three subclades cited for Glossocentrum (figs. 2, 3). In
sect. Hartigia (as well as other species of Miconia) by its axil-
these three lineages, the species from both sections are always
lary inflorescences. Other putative synapomorphies include
placed together. Goldenberg (2000) found that sect. Hypoxan-
the calyx lobes fused into a domelike, apiculate cap that rup-
thus has two distinctive groups: one bearing stamens with long
tures irregularly at anthesis, the reduced external calyx lobes,
anthers on short to absent basal connective prolongations and
an androecial fringe, and perhaps the four-merous flowers
the other with very short anthers on long connectives. All of
(Skean 1993). Tococa broadwayi and Tococa perclara form a
the species with long anthers on short connectives are in the
clade; these species, which do not produce formicaria, are
Miconia V grade (M. furfuracea subclade), while the species
not placed in the Tococa clade, in agreement with the mor-
with short anthers on long connectives are in both subclades in
phological cladistic analysis of Michelangeli (2000). Anaecto-
the Miconia IV clade. Thus, these two groups are nonmono-
calyx is from South America and has conspicuously bracted,
phyletic. Finally, species from both sections that have anthers
six-merous flowers with a calyx composed of prominent, in-
opening through slits (sects. Hypoxanthus and Chaenopleura)
dividually caducous lobes and anthers, with the thecae and
are not directly related. According to Cogniaux (1891), they
part of the connective bilobed and prolonged ventrally below
differ only in the shape of the anthers (linear in the former and
the insertion of the filament.
obovate to cuneate in the latter), but if we exclude the Andean
species from Chaenopleura, the species in this section have an-
Miconia Sects. Miconia, Glossocentrum, and
thers that expose four locules, while species from Hypoxanthus
Hypoxanthus and the South American
expose only two (Goldenberg et al. 2003; Judd 2007). Prob-
Lowlands Clades
lems regarding the diffuse sectional limits between sects. Miconia
Species from sect. Miconia are restricted only to the large and Glossocentrum, between Glossocentrum and Hypoxanthus,
clade that comprises all species from Miconia IV to Leandra s.s., and between Glossocentrum and Cremanium have already been
except for a few species placed in Miconia I and Miconia III and noted (Goldenberg 2000; Goldenberg et al. 2003) and certainly
in the Conostegia subclade. Nevertheless, they are absent in some point to convergent evolution of staminal morphology.
large portions of this clade, such as in the Leandra s.s. clade
and in a large part of the Clidemia grade. This suggests that
Stamens and Pollination
most of the species of sect. Miconia have no close relationship
to the species in core Cremanium, Amblyarrhena, or Chaeno- The conventional delimitation of sections in Miconia has
pleura. The species of this section also appear not to be inti- been based largely on stamen morphology. When one looks at
mately related to the core Leandra or the large Caribbean clade. the androecium characters in some sections (fig. 4), it seems
On the other hand, there are not just one or two clades where the that there are strong parallel trends in several clades, leading
species of sect. Miconia are prevalent, as is the case for sects. Ad- from large anthers in Tamonea/Jucunda to shorter anthers in
enodesma, Laceraria, Cremanium, Amblyarrhena, Chaenopleura, sects. Miconia and Glossocentrum (Gleason 1925a) and also
976 INTERNATIONAL JOURNAL OF PLANT SCIENCES
from minute-pored anthers in sects. Tamonea and Miconia to
large-pored Glossocentrum-type anthers and finally the large
and long-pored (resembling slits) anthers in sect. Hypoxan-
thus and Antillean sect. Chaenopleura. These trends can per-
haps be explained by a slight shift in the pollination mode: the
large and minute-pored flowers are usually visited, one by
one, by large- to medium-sized buzzing bees, and visits from
small bees or other insects are unlikely to result in pollination
because they either cannot extract the pollen or cannot touch
the stigma while extracting the pollen (Renner 1989). Smaller
flowers in dense clusters can be visited by the same large- to
medium-sized buzzing bees that vibrate whole inflorescence
branches or flower clusters and also individually by smaller
bees that would not be able to pollinate large flowers because
of their size. Finally, the pollen from broad-pored anthers can
be released without vibration (Goldenberg and Shepherd 1998;
Goldenberg and Varassin 2001). Nonbuzzing bees and syr-
phid flies have been observed feeding or gathering pollen from
M. pusilliflora (sect. Hypoxanthus; R. Goldenberg, personal
observation), while wasps and muscid flies have been observed
visiting the nectar-producing M. hyemalis (eastern Brazilian
sect. Cremanium; I. G. Varassin, personal communication) and
M. pepericarpa (sect. Glossocentrum; Goldenberg and Shep-
herd 1998), respectively. These species, which are visited by
nonvibrating insects, are also visited by buzzing bees, leading
us to conclude that the shortening of the anthers and the broad-
ening of the pores has not restricted but actually increased pol-
linator diversity, which in turn may represent a trend toward a
generalization among the relations between plants and pollina-
tors (Gomez and Zamora 2006). In some groups, the enlarge-
ment of the dehiscence area of the anthers, coupled with nectar
production, has led to either bat (M. sintenisii and perhaps
some other Antillean sect. Chaenopleura species; Judd 2007) or
bird pollination (M. melanotricha [F. Almeda, personal obser-
vation] and Charianthus and Tetrazygia fadyenii [Penneys and
Judd 2003, 2005]). These characters related to pollination ecol-
ogy are under strong selection pressure and therefore are more
subject to convergence (Anderson et al. 2002), as seen, for ex-
ample, in the remarkably similar, bird-pollinated flowers of T.
fadyenii and the species of Charianthus (Penneys and Judd 2003,
2005). It seems clear that stamen morphology, at least when
used alone, is not a reliable character on which to base taxo-
nomic groups because similar anthers seem to have evolved
multiple times in the Miconieae. Other floral features linked
to pollinator syndromes (such as petal form and color) are
also suspect. It is evident from even a casual examination of
figures 1–3 that there has been extensive homoplasy in sev-
eral floral characters.
It is possible that other morphological characters will clarify
the circumscription of particular clades because morphology
has been shown to be a source of numerous phylogenetically
informative characters in several recent analyses of taxa within
the tribe (Skean 1993; Michelangeli 2000; Penneys and Judd
2005; Judd 2007; Martin et al. 2008). Characters related to
seeds are especially promising because they are highly variable
within the tribe (Groenendijk et al. 1996) and have been used
successfully as phylogenetic characters in Melastomataceae
(Whiffin and Tomb 1972; Fritsch et al. 2004) and even as synapo-
morphies within groups of Miconieae (Michelangeli 2000;
Martin et al. 2008; E. Becquer, personal communication).
Geographical Trends and Local Diversification
This study shows that the lineages within the Miconieae are
strongly correlated with geography. Some taxa that until now
have been regarded as widespread are in fact restricted to par-
ticular regions, with geographically distant members actually
belonging to other clades. This is readily apparent in the case
of sect. Cremanium, with a clearly Andean/Central American–
based diversity (Miconia III clade) and whose extra-Andean
species actually belong to other groups. A similar pattern was
found for sect. Chaenopleura, where the Antillean species are
not closely related to the Andean ones, the latter being placed
within a Cremanium/Amblyarrhena complex. Outside Mico-
nia, the genus Leandra has a clade based in eastern Brazil
(Leandra s.s.) and others in other parts of Central America or
northern South America (scorpioid Leandra þ Ossaea, Lean-
dra clidemioides subclade at the base of the Clidemia grade;
see Martin et al. 2008). A large array of Caribbean species tra-
ditionally placed in Pachyanthus, Calycogonium, Tetrazygia,
or Charianthus, and even with a few species placed in Clide-
mia or Miconia, was found to constitute a clade—here called
the Caribbean clade—which again highlights the close con-
nection between phylogeny and geography.
Much of the diversity of Miconia (and Miconieae) found
in some geographical areas reflects only local diversification
and not multiple arrivals or introductions of distantly related
groups. The best example of this pattern is the diversity of Mi-
conieae within the Caribbean. The Antillean species are derived
mostly from only three clades: the large Caribbean clade, Mico-
nia sect. Chaenopleura in Miconia III, and a portion of the
Mecranium þ allies clade. However, a fourth clade may also be
significant in terms of Antillean diversity within Miconieae,
i.e., the axillary-flowered members of Clidemia and Ossaea in
the Clidemia grade (i.e., species treated as Sagraea; Judd and
Skean 1991). Another good example comes from clades Mico-
nia IV and V, both encompassing most of the morphological
and species diversity of Miconia in eastern Brazil, regardless of
their current sectional placement. These two clades consist of
species that have been placed in at least eight sections (Tamo-
nea, Jucunda, Octomeris, Miconia, Cremanium, Amblyarrhena,
Glossocentrum, and Hypoxanthus). Speciation in these evolu-
tionary lines has apparently involved extensive morphological
differentiation and convergence. This has led students of the
family to assign some species to geographically distant groups
to which they really do not belong.
Moreover, almost all the diversity of the Miconieae (includ-
ing species placed in Miconia, Leandra, Clidemia, Pleiochiton,
and Ossaea) that is centered in eastern Brazil belongs to only
three clades (the ones cited above and the Leandra s.s. clade).
All eastern Brazilian species belonging to other clades are ei-
ther widespread (i.e., M. dodecandra, M. theaezans, and Cli-
demia hirta) or part of widespread species complexes (i.e.,
from the scorpioid Leandra þ Ossaea clade).
Major taxonomic realignments, such as changes in the circum-
scriptions of the sections or genera in Miconieae, are premature.
They must await a more detailed and highly resolved phylogeny
that includes well-defined morphological characters. Neverthe-
less, the traditionally recognized genera within Miconieae, which
have been diagnosed largely on the basis of very few characters
(drawn from highly homoplasious floral features) and are largely
 GOLDENBERG ET AL.—PHYLOGENY OF MICONIA (MELASTOMATACEAE)
widespread (with a few exceptions, mostly in the Caribbean),
will be replaced by the geographically cohesive clades discovered
in our phylogenetic analyses. Work in progress will allow the
more accurate delimitation and morphological characterization
of these clades and will then form the basis of a new phyloge-
netically based classification of Miconieae.
Acknowledgments
We thank the following individuals for providing plant mate-
rial: J. Dan Skean Jr., Claire Martin, Eldis Becquer, Andrea K.
dos Santos, André Amorim, Ludovic Kollmann, Karen Redden,
Mac Alford, Larry Kelly, Robbin Moran, Scott Mori, Maria E.
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