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Botanical Journal of the Linnean Society, 2013, 171, 38–60. With 3 figures
Phylogenetic relationships and distribution of New
World Melastomeae (Melastomataceae)
FABIÁN A. MICHELANGELI1*, PAULO J. F. GUIMARAES2, DARIN S. PENNEYS3,
FRANK ALMEDA3 and RICARDO KRIEBEL1,4
1
The New York Botanical Garden, Bronx, NY 10458,USA
Jardim Botanico de Rio de Janeiro, Rio de Janeiro, RJ Brazil
3
The California Academy of Sciences, San Francisco, CA, USA
4
The Graduate Center, City University of New York, New York, NY, USA
2
Received 1 December 2011; revised 17 June 2012; accepted for publication 24 July 2012
In this study we present a phylogenetic analysis of Melastomeae, focusing on the Neotropical members of the tribe,
a group of c. 70 species in 30 genera. In total, 236 species, including outgroups (Miconieae and Merianieae) and
representatives of the Microlicieae and Rhexieae, were sequenced for the nuclear ribosomal internal transcribed
spacer (nrITS), and the plastid spacers accD-psaI and psbK-psbL. Melastomeae are not resolved as monophyletic
because a group of mostly herbs and small trees with mostly tetramerous flowers (Acanthella, Aciotis, Acisanthera,
Appendicularia, Comolia, Ernestia, Fritzschia, Marcetia, Macairea, Nepsera, Sandemania and Siphanthera) is
nested between Rhexieae and Microlicieae. The remaining New World Melastomeae are not resolved as monophyletic, because a group of Old World genera (Osbeckia, Melastoma, Tristemma and allied genera) are nested in
the tribe. The large genus Tibouchina is not monophyletic because Brachyotum, Bucquetia, Castratella, Centradenia, Chaetolepis, Heterocentron, Itatiaia, Microlepis, Monochaetum, Pilocosta, Svitramia, and Tibouchinopsis are
nested in it, even although all of these genera are recovered as monophyletic. Each major clade has remarkable
habitat and geographical integrity. The clade formed by Tibouchina and allies appears to have arisen in savannas
in lowland South America and later expanded to forest, campo and high Andean biomes. At least two groups have
radiated in eastern Brazil, and two other groups in the Andes and mountains of Central America. Niche
conservatism and colonization of adjacent environments seem to have driven speciation in Neotropical Melastomeae. © 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 38–60.
ADDITIONAL KEYWORDS: capsular fruit – Microlicieae – niche conservatism – Osbeckieae – Rhexieae –
Tibouchina.
INTRODUCTION
Phylogenetic analyses published over the last
10 years have shown that traditional tribal delimitations (e.g. Triana, 1871; Cogniaux, 1891; Renner,
1993) in Melastomataceae are unnatural and in need
of revision (Clausing & Renner, 2001; Michelangeli
et al., 2004; Renner, 2004a; Amorim, Goldenberg &
Michelangeli, 2009; Penneys et al., 2010; Penneys &
Judd, 2011). Most of these analyses also recovered
a clade that groups the species with anthers with
pedoconnectives and capsular fruits, corresponding
to tribes Melastomeae, Microlicieae and Rhexiae.
*Corresponding author. E-mail: fabian@nybg.org
38
However, generic and species sampling has been
insufficient to fully assess the relationships among
these tribes or to evaluate generic limits and relationships. This level of taxonomic confusion among Melastomeae, Rhexieae and Microlicieae is long-standing,
as evidenced by the fact that every infrafamilial classification to date has differed on how these groups are
related to each other and on the generic composition
of each tribe (Candolle, 1828; Naudin, 1849–1853;
Triana, 1871; Cogniaux, 1891; van Vliet, KoekNoorman & Ter Welle, 1981; Renner, 1993). These
differences have resulted from the relative importance that different authors have placed on calyx,
stamen, ovary and seed morphology, biogeography
and wood anatomy.
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 38–60
NEW WORLD MELASTOMEAE (MELASTOMATACEAE)
The lack of phylogenetic information for Melastomeae is unfortunate because, in Melastomataceae,
a large amount of generic diversity (and therefore
morphological diversity) is concentrated in the tribe.
Melastomeae are pantropical, and include > 870
species in 47 genera. The tribe is characterized by
having stamens provided with a pedoconnective
(poorly developed or reduced in some genera),
appendages when they are present only ventral and
paired, and capsular fruits that contain cochleate
seeds with curved embryos. In Melastomeae, the
majority of species are in South America (c. 570
species in 30 genera) (Renner, 1993), followed by
Africa (c. 185 species) (Wickens, 1974; Jacques-Félix,
1994). Madagascar, India, Indonesia and Malaysia
each have c. 50 species (Perrier de la Bâthie, 1934,
1951; Hansen, 1977; Hansen, 1992; Meyer, 2001;
Renner et al., 2001a) and the group extends, with four
species each, into northern Australia (Whiffin, 1990)
and Japan.
The 570 New World species are distributed among
30 genera that vary widely in size. Tibouchina Aubl.
is the largest genus with 240 species, six others have
20–60 species and eight genera are monotypic. To
date, < 25% of the genera have been included in
molecular analyses, and no genus has been represented by more than two species, thus making it
impossible to evaluate the monophyly of currently
recognized genera and phylogenetic relationships
among them. The distribution patterns also make the
New World Melastomeae a remarkable group. They
range from Mexico, through the Antilles, south to
Argentina, and from sea level to well above the tree
line in the Andes and eastern Brazil. New World
Melastomeae occupy a variety of forest and open
vegetation types including lowland savannas, cerrados, campos rupestres, lowland and cloud forests,
paramos and punas, and some species even grow in
seasonally flooded habitats. In habit they vary from
small annual herbs to medium-sized trees, although
the majority of the species are shrubs or small trees.
Such morphological and ecological diversity makes
this group an ideal candidate in which to study morphological character evolution and a model system to
track the establishment of different Neotropical vegetation types.
MATERIAL AND METHODS
TAXON SAMPLING
To study the phylogenetic relationships of taxa putatively assigned to Neotropical Melastomeae (sensu
Renner, 1993), ingroup sampling in this analysis comprises 219 terminals (217 species) from 42 genera. Of
these, 191 terminals from 32 genera correspond to
39
species found in the New World (25 genera out of 30
genera of Neotropical Melastomeae sensu Renner,
1993, plus seven genera from Rhexieae or of uncertain placement) and 28 species from ten genera from
Asia, Australia and Africa (including Madagascar).
Additionally, we included ten species from four genera
of Microlicieae. We also included two species of
Cambessedesia DC., a capsular-fruited Neotropical
genus previously considered to be a member of Microlicieae, but that has been shown to fall outside
that tribe (Fritsch et al., 2004). Seven species of
Miconieae (including the Physeterostemon R.Goldenb.
& Amorim + Eriocnema Naudin clade) and Merianieae were used as outgroups; following previous
family-wide analyses (Clausing & Renner, 2001;
Renner, 2004a; Amorim et al., 2009). Trees were
rooted at the node that unites the latter two tribes.
DNA
EXTRACTION AND SEQUENCING
Total genomic DNA was isolated from silica-dried or
herbarium material using the DNeasy plant mini
kit from Qiagen and following the manufacturer’s
instructions. Some samples were isolated with modifications that have been shown to improve DNA
quality and yield in Melastomataceae and/or with
herbarium specimens, such as the addition of
proteinase-K (30 mL per extraction to the lysis
buffer) and/or b-mercaptoethanol (30 mL per extraction to the lysis buffer), with longer incubation
periods at lower temperatures (6–24 h at 42 °C)
(Martin et al., 2008; Michelangeli et al., 2008). In
order to assess the phylogenetic relationships of
Melastomeae, we sequenced one nuclear locus [the
nuclear ribosomal internal transcribed spacer
(nrITS) region] and two plastid spacers (accD-psaI
and psbK-psbL). ITS has been used to elucidate phylogenetic relationships at the tribal and generic
level in Melastomataceae (Michelangeli et al., 2004,
2008; Ionta et al., 2007; Goldenberg et al., 2008) and
we used the protocols outlined in those publications.
The psbK-psbL spacer was amplified using primers
designed by Kim-Joong Kim (Korea University,
South Korea) and published by Reginato, Michelangeli & Goldenberg (2010), and the accD-psaI spacer
was amplified using primers designed by Shaw et al.
(2005). Protocols for amplifying the plastid markers
were detailed in Reginato et al. (2010). Cycle
sequencing was performed with the same forward
and reverse primers used for amplification at the
high-throughput sequencing service at the University of Washington (USA). Contigs were assembled
with Sequencher 4.9 (GeneCodes Corp., Ann Arbor,
MI, USA). Sequence alignment was performed with
Clustal X (Thompson et al., 1997) and manually
adjusted in BioEdit (Hall, 2007).
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 38–60
40
F. A. MICHELANGELI ET AL.
PYLOGENETIC
ANALYSES
The separate nuclear and plastid data sets and the
combined matrix were analysed using parsimony and
maximum likelihood. The resulting topologies from
the individual analyses were inspected by eye to
discount the possibility of hard incongruence across
data sets (i.e. support > 70% for placement of a taxon
in different clades or for relationships among major
clades identified in Fig. 1).
Parsimony analyses were performed in Tree analysis using New Technology (TNT) (Goloboff, Farris &
Nixon, 2008) after the indels were coded following the
‘simple gap coding’ procedure of Simmons & Ochoterena (2000) as implemented in 2xRead (Little, 2006).
Tree searches were performed with 1000 random
Miconieae + Merianieae
100
100
Cambessedesia
100
A-Microlicieae
100
100
100
79
66
B-Rhexieae
100
100
100
98
C-Marcetia and
allies
95
98
D-Pterolepis + Pterogastra
67
70
59
E-African + Asian
Melastomeae
(Osbeckieae)
67
80
83
Desmoscelis
F-Tibouchina sects.
Tibouchina + Barbigerae
83
65
G-Heterocentron and
allies
74
96
100
88
100
H-Monochaetum
and allies
98
72
99
57
I-Brachyotum and allies
65
100
51
90
J-Easten Brazilian
Tibouchina (Pleroma)
+ Microlepis, Svitramia,
Tibouchinopsis
99
Figure 1. Summary of phylogenetic analyses of Melastomeae based on the combined nuclear (nrITS; 1197 bp), and
plastid (accd-psaI; 1570 bp, and psbK-psbL; 666 bp) data sets. Maximum likelihood analysis (left) with bootstrap support
values below branches. Maximum parsimony analysis (right) with jackknife support values below branches.
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 38–60
NEW WORLD MELASTOMEAE (MELASTOMATACEAE)
addition sequences, holding five trees per replicate.
The resulting most-parsimonious trees were then
swapped to completion. Clade support was calculated
using the parsimony jackknife with 1000 replicates.
Each replicate was performed with 20 random addition sequences and holding three trees. The strict
consensus of each replicate was saved. Data editing
and examination of phylogenetic trees was performed
with WinClada (Nixon, 1999–2002). To ensure that
the entire tree space had been searched, we also
conducted a search using the parsimony ratchet
(Nixon, 1999) as implemented in WinClada (Nixon,
1999–2002) and spawned to NONA (Goloboff, 1993).
Three sequential runs were performed, each of them
with 300 iterations, holding five trees per iteration
and sampling 10% of the characters. The resulting
most-parsimonious trees obtained were then swapped
to completion. Maximum likelihood analyses and
bootstrap were performed with RAxML using default
parameters (Stamatakis, 2006; Stamatakis, Hoover &
Rougemont, 2008), run through the Cypress Science
Gateway (http://www.phylo.org/; Miller, Pfeiffer &
Schwartz, 2010).
Morphological characters discussed in the text were
taken from a data set developed for a forthcoming
detailed study of Tibouchina and allies (P. J. F. Guimaraes & F. A. Michelangeli, unpubl. data).
RESULTS
Table 1 summarizes the number of taxa and the
length and level of variation for the three loci
included in this study. The Appendix contains all the
voucher and GenBank accession information for the
taxa included in this study. No strong topological
incongruence was found for major clades when comparing the nuclear and plastid data.
Parsimony analyses resulted in > 100 000 trees
(CI = 0.37, RI = 0.79). Fifty-one nodes collapsed in
the strict consensus (not shown). Melastomeae s.l.
(Renner, 1993) are not monophyletic in either
the parsimony or maximum likelihood analyses
(Fig. 1), as, in both cases, Microlicieae are nested in
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Melastomeae. Cambessedesia is resolved as sister to
all other Melastomeae + Microlicieae and Rhexieae.
In both likelihood and parsimony analyses there are
four well-supported clades excluding Cambessedesia:
(clade A) Microlicieae (sensu Fritsch et al., 2004),
(clade B) a clade composed of Rhexia L.,
Arthrostemma DC. and Pachyloma DC. (Rhexieae),
(clade C) a clade composed of Acanthella Hook.f.,
Aciotis D.Don, Acisanthera P.Browne, Appendicularia
DC., Comolia DC., Ernestia DC., Fritzschia Cham.,
Marcetia DC., Macairea DC., Nepsera Naudin, Sandemania Gleason and Siphanthera Pohl ex DC. (from
hereon called Marcetia and allies) and (clades D–J) a
clade of ‘core Melastomeae’. The clade of core Melastomeae is composed of the Neotropical genera Brachyotum (DC.) Triana, Bucquetia DC., Castratella
Naudin, Centradenia G. Don, Chaetolepis (DC.) Miq.,
Desmoscelis Naudin, Heterocentron Hook. & Arn., Itatiaia Ule, Microlepis (DC.) Miq., Monochaetum (DC.)
Naudin, Pilocosta Almeda & Whiffin, Pterolepis (DC.)
Miq., Pterogastra Naudin, Svitramia Cham.,
Tibouchina Aubl. and Tibouchinopsis Markgr. Additionally, in the Neotropical Melastomeae are nested
all the Old World members of the tribe sampled in
this study [Amphorocalyx Baker, Antherotoma
(Naudin) Hook.f., Dichaetanthera Endl., Dionycha
Naudin, Dissotis Benth., Guyonia Naudin, Heterotis
Benth., Melastoma L., Osbeckia L and Rousseauxia
DC.; i.e., Osbeckieae p.p., sensu Cogniaux, 1891],
forming a single clade (clade E).
Parsimony and likelihood analyses differ in the
relationships among these main four clades, with
Marcetia and allies (Figs 1–2, clade C) resolved as
sister to Rhexieae + Microlicieae in the maximum
parsimony (MP) analysis (Figs 1–2, clades A–B) and
as sister to core Melastomeae in the maximum likelihood (ML) analysis (Figs 1–2, clades D–J). However,
this relationship lacks support in the MP analysis
and has only moderate support in the ML analysis.
In core Melastomeae, there are three distinct
clades: Pterogastra + Pterolepis (Figs 1–2, clade D),
Old World Melastomeae (Figs 1–2, clade E) and New
World Tibouchina and allied genera (Figs 1–2; clades
Table 1. Aligned length, indels and informative characters for the three loci sequenced
Loci
Taxa
sampled
Aligned
base
pairs
Potentially
informative
nrITS
accD-psaI
psbK-psbL
Total
234
211
212
236
1197
1570
666
3433
518
458
251
1227
Indels
Potentially
informative
indels
Total potentially
informative
characters
378
298
179
855
175
144
89
408
693
602
340
1635
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 38–60
42
F. A. MICHELANGELI ET AL.
Meriania longifolia
Graffenrieda latifolia
Graffenrieda moritziana
Miconia tomentosa
Miconia dodecandra
Eriocnema fulva
Physeterostemon tomasii
Cambessedesia hilariana
Cambessedesia espora
Rhynchanthera grandiflora
Rhynchanthera bracteata
Rhynchanthera serrulata
Trembleya parviflora
Trembleya pentagona
Trembleya laniflora
Chaetostoma armata
Lavoisiera pulchella
Lavoisiera mucorifera
Lavoisiera imbricata
Arthrostemma primaevum
Arthrostemma ciliatum 1
Arthrostemma ciliatum 2
Pachyloma huberioides
Rhexia aristosa
Rhexia salicifolia
Rhexia nashii
Rhexia virginica
Rhexia alifanus
Rhexia nuttallii
Rhexia petiolata
Rhexia lutea
Rhexia parviflora
Rhexia cubensis
Rhexia mariana
Ernestia glandulosa
Comolia microphylla
Acisanthera hedyotidea
Acanthella sprucei
Acisanthera quadrata
Acisanthera alsinaefolia
Siphanthera hostmanii
Comolia vernicosa
Sandemania hoehnei
Ernestia tenella
Macairea thyrsiflora
Macairea pachyphylla
Macairea radula
Ernestia confertiflora
Nepsera aquatica
Aciotis acuminifolia
Ernestia pullei
Appendicularia thymifolia
Marcetia acerosa
Marcetia latifolia
Marcetia taxifolia
Marcetia ericoides
Marcetia harleyi
Marcetia eimeariana
Comolia sertularia
Fritzschia erecta
Aciotis paludosa
Aciotis circaeifolia
Aciotis indecora
Aciotis rubricaulis
Aciotis purpurascens
Pterolepis glomerata
Pterolepis rotundifolia
Pterolepis parnasiifolia
Pterogastra minor
Pterogastra divaricata
Pterolepis alpestris
Pterolepis repanda
Pterolepis sp.
Guyonia ciliata
Dissotis cf. phaeotricha
Tristemma mauritianum var. mauritianum
Tristemma littorale subsp. biaffranum
Tristemma coronatum
Tristemma hirtum
Dichaetanthera oblongifolia
Dichaetanthera africana
Heterotis decumbens
Heterotis rotundifolia
Antherotoma naudinii
Dissotis multiflora
Amphorocalyx rupestris
Amphorocalyx multiflorus
Rousseauxia andringitrensis
Dionycha bojeri
Rousseauxia minimifolia
Osbeckia stellata
Osbeckia courtallensis
Osbeckia nepalensis
Osbeckia australiana
Melastoma dodecandrum
Melastoma denticulatum
Melastoma affine
Melastoma intermedium
Melastoma candidum
Melastoma sanguineum
Melastoma malabathricum
Eastern Brazil
A-Eastern Brazil
(campos rupestres)
Bi-Central America
Bii-Amazonia
Biii-Eastern North America
C-Lowland
South America
D-Lowland
South America
E-Africa
E-Madagascar
E-SE Asia + Australia
To fig. 2B
Figure 2. A, estimation of phylogenetic relationships in Melastomeae. Maximum likelihood analysis of combined nuclear
(nrITS) and plastid (accd-psaI, psbK-psbL) data sets, with geographical distribution of each clade. See Figure 1 for support
values of major clades. B, continuation of Figure 2A, estimation of phylogenetic relationships in Melastomeae. Maximum
likelihood analysis of combined nuclear (nrITS) and plastid (accd-psaI, psbK-psbL) data sets, with geographical distribution of each clade. See Figure 1 for support values of major clades.
F–J). Pterogastra + Pterolepis are resolved as sister to
the Old World Melastomeae, and together these
clades are sister to Tibouchina and allies.
In the Tibouchina and allies clade (Figs 1–2; clades
F–J), Desmoscelis is resolved either as the first diverging branch, or as part of a basal polytomy. Above
Desmoscelis, the large genus Tibouchina is not recovered as monophyletic, as several smaller genera are
nested in it, although the majority of these genera
are recovered as monophyletic. Within this clade there
are five well-supported groups: F – Tibouchina sections
Tibouchina and Barbigerae (Naud.) Cogn.; G – Hetero-
centron, Centradenia and Pilocosta (with one species
of Tibouchina); H – Monochaetum, Bucquetia, Chaetolepis and Castratella. I – Brachyotum and members
of Tibouchina sections Simplicicaulis (Naudin) Cogn.,
Pseudopterolepis Cogn. and Lepidotae Cogn. and some
members of sections Diotanthera (Triana) Cogn. and
Purpurella (Naudin) Cogn.; and J – eastern Brazilian
Tibouchina, i.e. Tibouchina sections Pleroma (D.Don)
Cogn., Diplostegia (D.Don) Cogn., Involucrales Triana
and the remainder of section Diotanthera and
Purpurella, with the genera Itatiaia, Microlepis, Svitramia and Tibouchinopsis (Fig. 2B).
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 38–60
NEW WORLD MELASTOMEAE (MELASTOMATACEAE)
To fig. 2A
Desmoscelis villosa
Tibouchina aspera var. aspera
Tibouchina aspera var. asperrima
Tibouchina striphnocalyx
F-Lowland
Tibouchina fraterna
Tibouchina bipenicillata
South America
Tibouchina papyrus
Tibouchina aegopogon
Tibouchina llanorum
Tibouchina breedlovei
Heterocentron elegans
Heterocentron muricatum
Heterocentrum subtriplinervium
Centradenia grandifolia
G-Central America
Centradenia inaequilateralis
Pilocosta oerstedii
Pilocosta campanensi
Pilocosta nubicola
Pilocosta nana
Bucquetia glutinosa
Castratella piloselloides
Chaetolepis microphylla
Chaetolepis cufodontisii
Monochaetum polyneuron
H-Andes
Monochaetum discolor
Monochaetum uribei
Monochaetum meridense
Monochaetum humboldtianum
Monochaetum tenellum
Monochaetum bonplandii
Monochaetum vulcanicum
Central America
Tibouchina inopinata
Tibouchina wurdackii
Ii-Andes + Central America
Tibouchina gleasoniana
Tibouchina lepidota
Iiii-Lesser Antilles
Tibouchina geitneriana
Tibouchina longifolia
Iii-Widespread
Tibouchina chamaecistus
Tibouchina ornata
Tibouchina gracilis
Tibouchina minor
Iiv-Eastern Brazil
Tibouchina hieracioides
Tibouchina clinopodifolia
Tibouchina ciliaris
Tibouchina cerastifolia
Tibouchina sebastianopolitana
Tibouchina laxa
Tibouchina pendula
Tibouchina mollis
Tibouchina grossa
Tibouchina alpestris
Tibouchina gayana
Tibouchina sp.
Tibouchina citrina
Tibouchina confertiflora
Tibouchina naudiniana
Brachyotum rostratum
Tibouchina octopetala
Brachyotum microdon
Tibouchina bicolor
Brachyotum benthamianum
Iv-Andes
Brachyotum lindenii
Brachyotum ledifolium
Brachyotum incrassatum
Brachyotum confertum
Brachyotum fictum
Brachyotum harlingii
Brachyotum fraternum
Tibouchina melanocalyx
Tibouchinopsis mirabilis
Tibouchina blanchetiana
Tibouchina velutina
Tibouchina pereirae
Tibouchina oreophilla
Tibouchina castellenis
Tibouchina aemula
Tibouchina gardneriana
Svitramia wurdackiana
Svitramia sp. ined. 2
Svitramia sp. ined. 1
Svitramia pulchra
Svitramia hatschbachii
Svitramia minor
Tibouchina semidecandra
Tibouchina pulchra
Tibouchina valtheri
Tibouchina candolleana
Tibouchina urceolaris
Tibouchina clavata
Tibouchina cryptadena
Tibouchina clidemioides
Tibouchina heteromalla
Tibouchina manicata
Tibouchina sp. ined 2
Tibouchina sp. ined. 1
Tibouchina sp. ined 3
Tibouchina radula
Tibouchina mutabilis
Tibouchina sellowiana
Tibouchina nodosa
Tibouchina foveolata
J-Eastern Brazil
Tibouchina fothergillae
Tibouchina benthamiana
Tibouchina corymbosa
Tibouchina cristata
Tibouchina axillaris
Tibouchina arborea
Tibouchina barnebyana
Tibouchina trichopoda
Microlepis oleaefolia
Tibouchina dubia
Tibouchina ursina
Tibouchina kleinii
Tibouchina trinervia
Tibouchina ramboi
Tibouchina itatiaiae
Tibouchina boudetii
Tibouchina fissinervia
Tibouchina stenocarpa
Tibouchina hospita
Itatiaia cleistopetala
Tibouchina lindeniana
Tibouchina cinerea
Tibouchina microphylla
Tibouchina cardinalis
Tibouchina arenaria
Tibouchina martiusiana
Tibouchina frigidula
Tibouchina salviaefolia
Tibouchina estrellensis
Tibouchina granulosa
Tibouchina angustifolia
Tibouchina macrochiton
Tibouchina laevicaulis
Tibouchina martialis
0.03
Figure 2. Continued.
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 38–60
43
44
F. A. MICHELANGELI ET AL.
DISCUSSION
New Word Melastomeae, as currently defined
(Renner, 1993), are not resolved as monophyletic,
because Rhexia, tribe Microlicieae and Palaeotropical
Melastomeae are nested in it. Although these results
are incongruent with the traditional tribal classification of the family (Triana, 1871; Cogniaux, 1891) and
more recent realignments (van Vliet et al., 1981;
Renner, 1993), four major clades that have been identified in previous molecular phylogenetic studies
(Clausing & Renner, 2001; Renner, 2004a, b) are also
recovered here, with a significantly increased sampling, i.e. Marcetia and allies, an expanded Rhexieae,
Microlicieae and core Melastomeae. These four major
clades are united by the presence of anthers with
well-developed pedoconnectives (although these have
been lost a number of times; see below) as previously
shown in other molecular systematic studies (Clausing & Renner, 2001; Renner & Meyer, 2001; Renner,
2004a). Additionally, all of these groups except Microlicieae have cochleate seeds (with further modifications in some genera; see below).
MICROLICIEAE
Results of this study are in agreement with Fritsch
et al. (2004) regarding a reduced generic composition of
Microlicieae, including only Chaetostoma, Lavoisiera,
Microlicia, Rhynchanthera, Stenodon and Trembleya
(Fig. 2A, clade A). Likewise, the former study removed
Cambessedesia, Eriocnema, Siphanthera and Castratella from their ‘core Microlicieae.’ Microlicieae are
supported by reniform, ellipsoid or elongate seeds with
a foveolate or reticulate testa (Almeda & Martins,
2001; Fritsch et al., 2004) and the absence of a staminal dorsal vascular bundle (Wilson, 1950; P. J. F.
Guimaraes, K. Sosa, R. Kriebel & F. A. Michelangeli,
unpublished data). Most species also have rostrate
anthers with a ventrally oriented terminal pore, but
rostrate anthers are also present in some Acisanthera,
Siphanthera and Tibouchina. Additionally, if ventral
connective appendages are present in the stamens,
these are always vascularized, a trait otherwise
only found in Arthrostemma (Wilson, 1950). This
character probably evolved in the ancestor of
Rhexieae + Microlicieae and was later lost in Pachyloma and Rhexia, which have reduced ventral staminal
appendages. In most genera, the anthers are also
unique in having long pedoconnectives with short
thecae, a character combination not seen in other
groups with pedoconnectives. Chaetostoma, however,
has some species with long anthers and a greatly
reduced pedoconnective (Koschnitzke & Martins, 1999,
2006; Fritsch et al., 2004). Polysporangiate anthers
have been reported in some species of Microlicia
and Chaetostoma (Baumgratz et al., 1996; Almeda &
Martins, 2001), and may be a synapomorphy for these
two genera. For details on the systematics and biogeography of Microlicieae see Fritsch et al. (2004).
RHEXIEAE
Rhexia, Arthrostemma and Pachyloma form a clade
distinct from core Melastomeae (Fig. 2A, clade B).
These genera of herbs and shrubs have tetramerous
flowers and cochleate, costate seeds that are tuberculate or rugose. Unlike core Melastomeae, in which
the tuberculae are composed of a single cell, in these
genera the tuberculae are composed of several cells
(Whiffin & Tomb, 1972; Renner & Meyer, 2001). In
all three genera, the ovaries lack apical projections.
Anthers in this clade are widely variable, but in all
genera (but not all species) the anthers have dorsal
connective appendages. In Pachyloma the anthers
have a long dorsal appendage and two ventral
appendages that are not vascularized, whereas
Arthrostemma has two vascularized ventral appendages and a short or absent dorsal appendage
(Gleason, 1929; Wilson, 1950). Both of these genera
have well-developed pedoconnectives. In contrast,
Rhexia lacks pedoconnectives and either has short
dorsal appendages or lacks them altogether (Wilson,
1950; Kral & Bostick, 1969; Ionta et al., 2007). Additionally, Rhexia can be distinguished by its constricted hypanthia (in Neotropical capsular-fruited
generea, otherwise restricted to the small genus Poteranthera Bong.), ovary locules opposite the petals
(they are alternating in most Melastomataceae
where the number of petals is the same as the
number of ovary locules) and unilocular anthers
(Ionta et al., 2007). In spite of the differences in
anther morphology, Gleason (1929) postulated that
Pachyloma was closely related to Rhexia (and Monochaetum, see below), based on the presence of
stamens with dorsal appendages and their seed morphology, but he seems to have missed the connection
with Arthrostemma.
MARCETIA
ALLIANCE
Most genera in the clade comprising Marcetia and
allies [Fig. 2A, clade C; Acanthella, Aciotis (Fig. 3A),
Acisanthera, Appendicularia, Comolia, Ernestia,
Fritzschia, Marcetia (Fig. 3B), Macairea, Nepsera
(Fig. 3C), Sandemania and Siphanthera], were traditionally placed in Melastomeae based on anther and
fruit morphology. Most of the species in this group are
herbs or small shrubs, and the annual habit, although
rare in the family, has appeared repeatedly in this
group (Freire-Fierro, 2002; Almeda & Robinson, 2011;
Kriebel, 2012). Additionally, some species of Macairea
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NEW WORLD MELASTOMEAE (MELASTOMATACEAE)
Figure 3. See caption on next page.
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 38–60
45
46
F. A. MICHELANGELI ET AL.
Figure 3. Representatives of Neotropical Melastomeae. A, Aciotis paludosa. B, Nepsera aquatica. C, Marcetia taxifolia.
D, Pterogastra divaricata. E, Pterolepis sp., notice intercalycine emergence (against petal). F, Desmoscelis villosa. G,
Tibouchina bipenicillata (section Barbigerae). H, Chaetolepis microphylla. I, Monochetum humboldtianum. J, Bucquetia
glutinosa. K, Heterocetron elegans. L, Centradenia inaequilateralis. M, Brachyotum strigosum. N, Tibouchina gayana
(section Diotanthera, from the Andes). O, Tibouchina clinopodifolia (section Purpurella from eastern Brazil). P,
Tibouchina bicolor (section Diotanthera from the Andes), longitudinal section, showing persistent calyx and ovary with
apical appendages. Q, Tibouchina lepidota (section Lepidotae). R, Tibouchina heteromalla (section Pleroma). S,
Tibouchina stenocarpa (section Pleroma), fruit with caducous calyx. (All pictures by F. A. Michelangeli.).
are trees up to 12 m tall (Renner, 1989). This clade
is further characterized by tetramerous flowers
(Fig. 3A–C) (although pentamerous flowers are
present in Acisanthera and Ernestia cordifolia O.Berg
ex Triana) and ovaries that are either glabrous
or with glandular trichomes at the apex, but that
lack appendages (see below). In Marcetia, Aciotis,
Fritzschia, Siphanthera and Nepsera, the pedoconnectives are small or lacking and connective appendages
are absent (Fig. 3A–C). All genera sampled in this
clade have seeds that are cochleate, ovate or lacrimiform. With the exception of Siphanthera, all these
genera also have seeds with foveolate testas (Whiffin
& Tomb, 1972). In some cases, these features can be
obscured by the presence of tubercles or secondary
sculpturing, but the foveolate nature is evident at
least near the raphe. All of these genera were classified by Whiffin & Tomb (1972) as having a microlicioid
seed type, not the typical tibouchinoid type of other
Melastomeae. The number of ovary locules can be
equal to the number of petals (usually four), but
several taxa have a reduced number of locules, a
condition also common in Microlicieae, but not
common in Palaeotropical Melastomeae or the
Tibouchina and allies group. Lastly, all of these
species, except Acanthella sprucei Hook.f and Acisanthera hedyotoidea (C.Presl) Triana, have a deletion of
381 bp in the psbK-psbL spacer.
Generic limits in some elements of the Marcetia
alliance have been notoriously difficult, especially
between Comolia and Ernestia. Sampling in this
investigation is insufficient to resolve the problematic
generic circumscriptions in this clade, but results
suggest (Fig. 2A) that Macairea and Marcetia are
monophyletic. Almeda & Robinson (2011) demonstrated the monophyly of Siphanthera using morphological data; Almeda & Martins (2001) had previously
removed it from Microlicieae on the basis of seed
morphology, and that result is confirmed here. Aciotis
might be rendered monophyletic with some small
adjustments. Poteranthera and Mallophyton were not
sampled in this study, but, based on the presence of
tetramerous flowers, ovary apex without a corona or
hairs and seed morphology, they are likely to belong
to the Marcetia alliance (Wurdack, 1964; Kriebel,
2012). Loricalepis Brade, a monotypic genus of small
shrubs with tetramerous flowers and white petals
from northern Brazil (Brade, 1958), may also be in
this clade.
CORE
MELASTOMEAE
The largest group in number of genera and species is
what we have designated core Melastomeae (Fig. 2B,
clades D–J). Putative morphological synapomorphies
for this pantropical clade include cochleate seeds with
tubercles or papillae composed of a single cell
(tibouchinoid seeds sensu Whiffin & Tomb, 1972), a
crown of hairs or appendages on the ovary apex
(Fig. 3P) and the presence of staminal pedoconnectives with bifurcated dorsal vascular bundles (Wilson,
1950; P. J. F. Guimaraes, K. Sosa, R. Kriebel & F. A.
Michelangeli, unpubl. data).
Pterogastra and Pterolepis form a strongly supported clade sharing several plesiomorphic characters, but there are no clear synapomorphies for this
group (Fig. 2A, clade D). Both genera have tetra- and
pentamerous species, herbaceous to suffruticose
habit, dimorphic stamens with developed pedoconnectives and short, bilobed ventral appendages
(Fig. 3D–E) (Renner, 1994a, b). They also have emergences or trichomes in the calyx sinuses, but these
differ between them. In Pterolepis the intercalycine
emergences are stellate–penicillate (Fig. 3E), whereas
they are slender and simple in Pterogastra. Intercalycine emergences are also present in some Chaetolepis,
Tibouchina and Palaeotropical Melastomeae (see
below). Pterogastra has prominently ribbed or winged
hypanthia, but this homoplasious character is also
present in Schwackaea Cogn. and Pilocosta Ameda &
Whiffin (see below) (Renner, 1994b). Unlike Pterogastra, the latter two genera have the same number of
wings as sepals (instead of double). In Schwackaea
the hypanthium is terete and in Pilocosta it is quadrangular. Although the hypanthia in Pterolepis are
not winged, they can be slightly angular, especially
in fruit. Some Palaeotropical Melastomeae also
have intercalycine emergences, and these are similar
to those found in Pterolepis. However, this character
cannot be used as diagnostic of the Palaeotropical clade, because it is absent in some genera
(i.e. Guyonia, Dichaetanthera and Tristemma).
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NEW WORLD MELASTOMEAE (MELASTOMATACEAE)
Additionally, some Palaeotropical Melastomeae have
persistent fleshy placentas, and some species even
have berries (mostly in Melastoma) (Clausing, Meyer
& Renner, 2000; Clausing & Renner, 2001).
Although Tibouchina is not resolved as monophyletic, the groups in this large clade (Fig. 2B, clades
F–J) are each well characterized by stamen and hypanthium morphology, and biogeography (see below).
This large assemblage of Neotropical genera is well
supported by molecular analyses, but morphological
synapomorphies are not readily evident. Desmoscelis
(Fig. 3F), the first diverging group of Tibouchina and
allies, is a genus of two species from lowland savannas.
It is characterized by its erect, herbaceous habit,
pentamerous flowers, long simple (eglandular or glandular) trichomes and dimorphic anthers with long,
paired ventral connective appendages. The larger
anthers are slender and subulate, whereas the smaller
ones are short, truncate and with a broad pore. These
characters are plesiomorphic in core Melastomeae or
autapomorphic for Desmoscelis.
The species of Tibouchina sections Tibouchina and
Barbigerae (Fig. 2B, clade F) have pink to purple
anthers without glandular trichomes (Fig. 3G). In
section Barbigerae the union between the filament
and the connective has simple, long trichomes. The
hypanthium in section Tibouchina has tufts of simple
hairs in the calyx sinuses, but whether or not these
structures are homologous to the intercalycine emergences of Pterolepis and Palaeotropical Melastomeae
is hard to assess without a detailed study of these
structures and better resolution in that section of the
estimated phylogeny.
Heterocentron, Pilocosta and Centradenia (Fig. 2B,
clade G) are herbs or small shrubs (sprawling in the
case of Pilocosta and a few species of Heterocentron)
with tetramerous flowers and tetralocular ovaries
(Fig. 3 K–L). Species in this clade have stamens that
are almost always dimorphic with well-developed
pedoconnectives and ventral appendages that are
usually bilobed in the larger series (Whiffin, 1972;
Almeda, 1977, 1993; Almeda & Whiffin, 1980). Each of
these genera are resolved as monophyletic (Fig. 2B,
clade G), and characters of hypanthium shape and
leaf and anther morphology support the recognition of
each of them as separate. Tibouchina breedlovei
Wurdack, a rarely collected species from southern
Mexico, is also placed in this clade. This species also
has tetramerous flowers and anthers that closely
resemble those of Heterocentron. In the original
description, Wurdack (1967) suggested that T. breedlovei could be placed near or in Heterocentron. Most
Heterocentron spp. have penninerved venation
(Whiffin, 1972), a character otherwise rare in the
family, and all species of Centradenia have asymmetrical leaves, also rare in the family (Almeda,
47
1977). Schwackaea, a monotypic genus ranging from
Mexico to north-western Colombia, shares all these
features (Renner, 1994b), and recent DNA data
confirm this placement (D. S. Penneys, F. Almeda,
P. W. Fritsch & F. A. Michelangeli, unpubl. data).
The group formed by Monochaetum, Chaetolepis,
Castratella and Bucquetia (Fig. 2H), like the Heterocentron group, share tetramerous flowers with tetralocular ovaries. Chaetolepis, Castratella and Bucquetia
have isomorphic, linear anthers without pedoconnectives or well-developed appendages (Fig. 3H–J).
Monochaetum, however, has well-developed dorsal
appendages, at least in the largest set of stamens
(Fig 3I). Some Monochaetum spp. have one whorl of
stamens reduced to staminodia, or even lack them,
and the species in the genus exhibit a high degree of
variation in the size of the pedoconnective. In most
Melastomataceae with stamen dimorphism, the
larger series of stamens is usually opposite the calyx,
with the reduced series opposite the petals, but in
Monochaetum this situation is reversed (Almeda,
1978). Bucquetia and Castratella had been placed in
Microlicieae (Cogniaux, 1891), but seed morphology
clearly excluded them from this group (Whiffin &
Tomb, 1972; Fritsch et al., 2004).
Brachyotum is characterized by pendant flowers
with copious nectar, in which the dark purple or
yellow to greenish petals are pseudocampanulate
(Fig. 3 M). The pedoconnective is highly reduced in
this group, and the entire genus is pollinated by
birds, mostly hummingbirds (Wurdack, 1953; Vogel,
1958; Stiles, Ayala & Giron, 1992), although bat pollination may also be possible. At least one Tibouchina
sp. in this clade [T. grossa (L.f.) Cogn.] also produces
nectar, and it is visited by bats (Vogel, 1958, 1997)
and hummingbirds (K. Schumman, pers. comm. cited
in von Helversen & Winter, 2003). However T. grossa
lacks pendant flowers with closed petals that have
traditionally defined Brachyotum, and has a base
chromosome number of x = 10 instead of x = 9 (Solt &
Wurdack, 1980). Brachyotum is nested among representatives of Tibouchina that generally have yellow or
white anthers, and many of them also have reduced
pedoconnectives (Fig. 3N–Q). In this Brachyotum
clade, those species with tetramerous flowers
(Tibouchina section Pseudopterolepis) are resolved as
a unit, as are the species with lepidote scales on the
hypanthium, free bracteoles and glabrous stamens
(Tibouchina section Lepidotae; Fig. 3Q) (Todzia &
Almeda, 1991). This clade also contains the majority
of the species of Tibouchina section Diotanthera, characterized by attenuate anthers and persistent
calyx lobes (Fig. 3P) (Cogniaux, 1891; Todzia, 1999).
Several species in section Diotanthera also have bicoloured petals (Fig. 3N). Based on anther and calyx
morphology, we expect several Mexican and Central
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48
F. A. MICHELANGELI ET AL.
American species that were not sampled in this study
(Todzia, 1999) to fall within this clade.
The Pleroma group (Fig. 2B, clade J) is characterized by species with a calyx that is caducous in fruit
(Fig. 3S) (Guimaraes & Martins, 1997). Most species
in this group have well-developed pedoconnectives,
purple, pink or white anthers, and if the anther
connectives have trichomes these are glandular
(Fig. 3R) (Cogniaux, 1891; Guimaraes & Martins,
1997). Most species are pentamerous, but some
Tibouchina with small flowers are tetramerous. The
Pleroma clade also includes four genera that have
been maintained separate from Tibouchina (Itatiaia,
Microlepis, Svitramia and Tibouchinopsis); these
genera have persistent calyces (Triana, 1871; Ule,
1908; Brade & Markgraf, 1961; Romero & Martins,
2003), a character difference that may be responsible
for all of these groups not being recognized as part of
Tibouchina. Additionally, Svitramia has reduced
anthers that lack pedoconnectives and have highly
reduced or absent ventral appendages (Romero &
Martins, 2003).
TRIBAL
AND GENERIC TAXONOMY
This study contains more than 14 times the number
of species of Melastomeae and three times the
number of genera included in any previous published
molecular study of Melastomataceae. Many of the
generic groupings shown here are consistent with
those studies, but, as a result of increased generic and
specific sampling, a clearer picture of the evolution of
the capsular taxa with pedoconnectives in Melastomataceae is starting to emerge, with some new
groups clearly identified (i.e. Marcetia and allies, the
affinities of Monochaetum with other high Andean
taxa, the composition of Rhexieae, etc.). Additionally,
this study represents the first insight into the relationships in the large and complex genus Tibouchina
and between Tibouchina and other Neotropical
Melastomeae. However, the level of sampling of
some groups (particularly Ernestia, Comolia and
Central American and Mexican representatives of
Tibouchina) and the level of resolution and support
along the spine of the tree stills makes it premature
to propose any overhaul of the taxonomy. For
example, whether Marcetia and allies, or the Pterogastra clade, deserve tribal recognition will depend on
the final resolution of the relationships between this
latter group and Palaeotropical Melastomeae, or the
relationships between the Rhexieae and Marcetia
clades. Similarly, Tibouchina could be recognized as a
much expanded genus (but, as noted above, there are
no clear morphological synapomorphies for this clade)
or all the other genera maintained and Tibouchina
divided into smaller and diagnosable units. The
Tibouchina and allies clade is already the subject of a
more detailed study that includes additional species,
markers and a morphological matrix (P. J. F. Guimaraes, K. Sosa, R. Kriebel & F. A. Michelangeli, unpubl.
data), and these open questions will be addressed in
forthcoming publications.
The fact that many groupings at the generic or
sectional level are recovered here as monophyletic, or
nearly so, is evidence that characters traditionally
used in Melastomeae taxonomy, such as androecium
morphology, merosity, seed morphology, calyx persistence and hypanthium indument (Naudin, 1849–1853;
Triana, 1871; Cogniaux, 1885, 1891; Whiffin & Tomb,
1972; Wurdack, 1986), are good predictors of phylogenetic relationships. The presence/absence of a
corona on the ovary apex (core Melastomeae vs.
Microliceae + Rhexieae + Marcetia alliance), and the
difference between ventral staminal appendages
with or without vascular bundles (Microlicieae +
Arthrostemma vs. Marcetia alliance and core
Melastomeae) have not traditionally been used for
taxonomic purposes and are shown here as a taxonomically important characters. Tibouchina, as currently defined, is not resolved as a monophyletic
group, mostly because it is defined by characters that
are plesiomorphic in core Melastomeae: pentamerous
flowers with anthers with developed pedoconnectives
and shortly bilobed ventral anther appendages.
HABITAT
AND DISTRIBUTION
As shown for other groups of Melastomataceae (Fritsch
et al., 2004; Renner, 2004a; Penneys & Judd, 2005;
Michelangeli et al., 2008), even if the generic or tribal
classification does not closely match phylogenetic
results, there is a close correspondence between most
clades recovered and the geographical distribution or
type of environment in which the plants live (Fig. 2).
Although a minority of outlying taxa are native to
areas north of South America, most species of the
Marcetia and allies clade are distributed in central
and north-eastern South America. Most are found
in open habitats, in either successional or ruderal
environments, savannas, campo rupestres and the
Guayana highlands. Some, mostly widespread,
species reach the Antilles and the Andes.
Microlicieae are almost exclusively found in eastern
and central Brazil in campos rupestres. A few Rhynchanthera spp. are found farther to the north and
south-west and in wetter environments, and one
Microlicia sp. is found in the Guayana Highlands.
The geographical distribution of this group has
already been examined in detail by Fritsch et al.
(2004) and Simon et al. (2009).
The Rhexia clade as a whole deviates from this
pattern of geographical integrity, but each genus is
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NEW WORLD MELASTOMEAE (MELASTOMATACEAE)
geographically restricted. Pachyloma, a genus of four
species, is restricted to north-western Amazonia,
whereas Arthrostemma, also with four species, is
found along the Andes, from Bolivia to Venezuela and
northen Brazil, and in Central America, Mexico
and the Antilles. This widespread distribution of
Arthrostemma is attributable only to one species,
A. ciliatum Pav. ex D.Don, which is a tetraploid
(N = 30), probably derived from A. primaevum
Almeda, a diploid species (N = 15) restricted to southern Mexico (Almeda & Chuang, 1992; Almeda, 1994).
Rhexia is the only genus of Melastomataceae found in
subtropical and temperate North America, with most
species being distributed from Texas to Nova Scotia.
One widespread species is also found in Cuba, Hispaniola and Puerto Rico (Kral & Bostick, 1969;
Liogier, 2000; Ionta et al., 2007). Even although these
species are found in three different regions, all three
genera are found in poorly drained, usually acidic
soils. Fossil seeds from the early to mid-Miocene that
have been collected throughout Eurasia (Dorofeev,
1960, 1963, 1988; Collinson & Pingen, 1992; Dyjor
et al., 1992; Mai, 2000) closely match those of this
clade with a cochleate shape and multicellular tubercles (Renner, Clausing & Meyer, 2001b; Renner &
Meyer, 2001). This is especially relevant considering
that these fossils have been used as calibration points
in molecular dating and biogeographical studies
(Renner et al., 2001b; Renner & Meyer, 2001; Morley
& Dick, 2003; Fritsch et al., 2004; Renner, 2004a, b),
and the fossil is found well outside the modern distribution of these three extant genera.
Pterolepis (with 14 species) and Pterogastra (with
two species) grow almost exclusively in different types
of grasslands in the Neotropics. Most species of Pterolepis are endemic to cerrado vegetation in central
and eastern Brazil, with one widespread species
reaching into the Caribbean and a second into
Central America and Southern Mexico (Renner,
1994a). One Pterogastra sp. is only found in savannas
in south-west Venezuela and Colombia, and a second
is widespread on the eastern slopes of the Andes from
sea level to 2600 m (Renner, 1994b).
The Palaeotropical Melastomeae clade includes
species of open and forested areas. Sampling in this
group is far from adequate to answer biogeographical
questions with a high level of certainty, but, based on
morphology, it is almost certain that all Palaeotropical Melastomeae do indeed fall into this group. This
preliminary sampling shows that Madagascan and
Asian lineages are derived from within Africa, and
not from the Neotropics.
In the group formed by Tibouchina and allied
genera, Desmoscelis and Tibouchina sections
Tibouchina and Barbigerae are also found in open
habitats in the savannas and the lower portion of the
49
Andean slopes of South America. Heterocentron, Centradenia and Pilocosta are mostly found on the edges
of mid-elevation and cloud forest from north-western
Colombia to Mexico (with one Pilocosta sp. extending
into Ecuador), constituting a predominantly Mexican/
Central American clade. The other group with tetramerous species, Monochaetum and allies, is mostly
distributed at high elevation in paramos and cloud
forests. Castratella and Bucquetia are restricted to
paramos in western Venezuela and eastern Colombia.
Chaetolepis is mostly found in South American
paramos, with one species endemic to the highest
elevations in Costa Rica and one species in the
Guayana
highlands.
Chaetolepis
gentianoides
(Naudin) Jacq.-Fél., a species restricted to the sandstone highlands of western Africa, renders Chaetolepis the only genus in Melastomatoideae disjunct
between the Neotropics and Paleotropics. Unfortunately, material of this species was not available for
sequencing during the course of this study. A morphological cladistic analysis (Grimm, 2009) found that
this species grouped with New World Chaetolepis, but
most of the anther morphology in this group is highly
reduced, and, because of the presence of intercalycine
projections at the apex of the hypanthium, a placement in the Old World Melastomeae cannot be discounted. Monochaetum is the most species-rich genus
in the clade with c. 30 species distributed in South
America and 20 in Mexico and Central America. Most
Central American species are found in cloud forests in
Costa Rica and Panama, and a second, smaller group
in the mountains of southern Mexico. Most South
American species are found in the paramos and cloud
forests of Venezuela and Colombia, with a few species
extending as far south as central Peru and one widespread species in the Guayana Highlands (Almeda,
1978, 2009; Alvear, 2010).
All Brachyotum spp. are found at high elevations in
the Andes from Colombia to Argentina (but not in
Chile), either in paramo or puna vegetation, or in the
surrounding cloud forests (Wurdack, 1953). The
majority of the members of Tibouchina in this clade
(Tibouchina sections Diotanthera and Lepidotae) are
also found at high elevations in the Andes and mountains of southern Central America. A small group of
species in this clade [see clade with T. clinopodifolia
(DC.) Cogn.] is found in the forests of the Mata
Atlantica, which may provide evidence of a dispersal
event from the Andes to Eastern Brazil. This connection between the Andes and high elevation floras in
eastern Brazil has been reported for other plant
groups (e.g. Berry et al., 2004; Perret, Chautems &
Spichiger, 2006; Struwe et al., 2009; Vasco, 2011). A
connection through favourable habitats in southern
Brazil during cool periods, rather than long distance
dispersal, seems to be the most likely explanation for
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50
F. A. MICHELANGELI ET AL.
this pattern (Safford, 2007). The distribution pattern
of species in the T. clinopodifolia clade would also
favour this hypothesis. One species, T. longifolia
(Vahl) Baill., is widespread from Mexico and the Antilles to Bolivia, and a close relative T. geitneriana
(Schltdl) Cogn. is also widely distributed, but usually
found at slightly higher elevations.
Tibouchina sections Pleroma, Diplostegia, Involucrales and the remainder of sections Diotanthera and
Purpurella, along with the genera Itatiaia, Microlepis, Svitramia and Tibouchinopsis are all found in
eastern Brazil, mostly in Mata Atlantica vegetation,
but some also grow on the exposed summits of rocky
outcrops and campos rupestres, cerrados and coastal
vegetation.
NICHE
CONSERVATISM AND HABITAT SHIFTS
The strong geographical structuring found in the
pedoconnective clade of Melastomataceae can be
attributed to phylogenetic niche conservatism
(Harvey & Pagel, 1991; Wiens, 2004; Donoghue,
2008), coupled with limited colonization of new environments and/or dispersal and with in situ speciation
(Pennington, Richardson & Lavin, 2006; Pennington,
Lavin & Oliveira, 2009; Schrire et al., 2009; Pennington et al., 2010). Not only are many groups restricted
to the same geographical area, but the vast majority
of the species are found in open habitats, regardless of
soil, temperature or elevation. Thus, even in cases of
habitat shift or colonization of new environments (e.g.
with the uplift of the Andes or the appearance of the
cerrado and Mata Atlantica biomes), this has occurred
through habitats that share some characteristics that
have allowed the incoming group to be successful.
These types of habitat shifts to similar, but not identical environments have been shown to occur at
higher phylogenetic levels and broader biome types
for several plant groups (see review by Crisp et al.,
2009, and references therein).
Phylogenetic niche conservatism has also been
invoked to explain the presence of closely related
groups in disjunct areas with similar environmental
conditions (Donoghue, 2008). Several plant groups in
the high Andes seem to follow this pattern, but in
many cases they have originated in temperate environments outside South America (von Hagen & Kadereit, 2001, 2003; Bell & Donoghue, 2005; Hughes &
Eastwood, 2006; Fritsch et al., 2008). A lowland, tropical origin for Andean groups, as shown here for some
members of the pedoconnective clade of Melastomataceae, can also be inferred in tribe Miconieae
(Michelangeli et al., 2008), and recently has been
shown for other groups of angiosperms (Antonelli
et al., 2009; Jabaily & Sytsma, 2011; Luebert, Hilger
& Weigend, 2011; Simon et al., 2011). In the pedoconnective clade, this situation is seen in Monochaetum
(found at high elevations in the northern Andes and
mountains of Central America), Chaetolepis (paramos
or northern South America, mountains in Costa Rica
and summits of tepuis in the Guayana shield), and
representatives of Tibouchina from the southern
Andes and high elevations of the Mata Atlantica (see
Fig. 2b clades Iiv and Iv).
When viewed as a whole, the pedoconnective clade
is found in a wide variety of environments from sea
level to 4000 m, in both tropical and subtropical climates (with some species of Rhexia and Melastoma
extending through temperate climates). This distribution of taxa across such different environments
may at first contradict our claim of phylogenetic
niche conservatism in the group. However, it is
important to note that habitat distribution is phylogenetically clustered, and the widespread distribution of our study group is only attributable to the
broad phylogenetic scope of the study. Moreover, if
we look at any two taxa in the same or closely
related clades and with extremely different habitats
(e.g. lowland savannas vs. mid-elevation cloud
forests of Mata Atlantica in clade J), we can see
how other closely related taxa of the second group
are found in intermediate environments (i.e. open
habitats at high elevations). Thus, the widespread
Neotropical distribution of the pedoconnective clade
could have been accomplished through successive
colonization of neighbouring or similar environments
(as described by Crisp et al., 2009) and by ‘niche
crawling’ from one environment to another, and the
ultimate result would be a broad distribution.
Unfortunately, the current level of phylogenetic
resolution between clades F–J, and, in some of these
clades, is insufficient to test this hypothesis. A more
resolved phylogenetic tree will also help address
questions about multiple colonizations of Central
America (clades G and Ii and some members of
clade H), the Andes (clades H and Iv) or the cerrado
biome (Microlicieae and some members of clades C,
D and J).
In summary, the pedoconnective clade of Melastomataceae appears to have radiated and speciated
mostly through open habitats, with wind dispersal of
seeds produced in capsular fruits playing an important role. Competition for pollinators (mostly bees),
and pollen economy (through heteranthery), may
have driven the evolution and diversification of
stamen morphology in this group (Gross, 1993;
Larson & Barrett, 1999; Luo & Zhang, 2005; VallejoMarin et al., 2010), These hypotheses were already
advanced by Renner & Meyer (2001) and would be
in agreement with the predictions of the niche conservatism hypothesis and colonization of similar or
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 38–60
NEW WORLD MELASTOMEAE (MELASTOMATACEAE)
adjacent environments and are supported here with
increased taxon and character sampling.
ACKNOWLEDGEMENTS
We thank wish to thank M. Alford, J. F. Baumgratz,
I. Capote, R. Goldenberg, W. Judd, L. Kelly,
L. Kollman, A. Lobao, C. V. Martin, H. Mendoza,
R. Naczi, M. Nee, K. Redden, A. K dos Santos,
K. Steiner and K. Wurdack for providing leaf and/or
herbarium material. Antoine Nicolas provided invaluable help in the laboratory. This research was supported by a grant from CAPES, Brazil to P.J.F.G.
(Scholarship Process Number BEX 2128/09-8). Partial
support was also provided by the Cullman Program
for Molecular Systematics and the structural botany
laboratory at The New York Botanical Garden and
grant DEB- 0818399 from NSF to F.A.M. R.K. was
supported by the Oliver Hazard Perry Graduate Fellowship at The New York Botanical Garden and
D.S.P. was partially supported by the John J. Rose
Postdoctoral Fellowship at the California Academy of
Sciences. Susanne Renner, an anonymous reviewer
and Toby Pennington provided valuable comments
that greatly improved this article.
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APPENDIX
List of species, voucher information, provenance and GenBank accession data included in this study [nuclear
ribosomal internal transcribed spacer (nrITS), accD-psaI, psbK-psbL). Voucher information only provided for
species newly sequenced for this study; all others taken from GenBank. Additional vouchers may be deposited
at other herbaria (acronyms following Thiers, 2012).
Species
Acanthella sprucei Hook.f.
Aciotis acuminifolila (Mart. ex DC.)
Triana
Aciotis circaeifolia (Bonpl.) Triana
Aciotis indecora (Bonpl.) Triana
Aciotis paludosa (Mart. ex DC.)
Triana
Aciotis purpurascens (Aubl.) Triana
Aciotis rubricaulis (Mart. ex DC.)
Triana
Acisanthera alsinaefolia (DC.) Triana
Acisanthera hedyotidea (C.Presl.)
Triana
Acisanthera quadrata Pers.
Amphorocalyx multiflorus Baker
Amphorocalyx rupestris H.Perrier
Antherotoma naudinii Hook.f.
Appendicularia thymifolia (Bonpl.)
Triana
Arthrostemma ciliatum 1 Pav. ex
D.Don
Arthrostemma ciliatum 2 Pav. ex
D.Don
Arthrostemma primaevum Almeda
Brachyotum benthamianum Triana
Brachyotum confertum (Bonpl.)
Triana
Brachyotum fictum Wurdack
Brachyotum fraternum Wurdack
Brachyotum harlingii Wurdack
Brachyotum incrassatum E.Cotton
Brachyotum ledifolium (Desr.) Triana
Brachyotum lindenii Cogn.
Brachyotum microdon (Naudin)
Triana
Brachyotum rostratum (Naudin)
Triana
Bucquetia glutinosa (L.f.) DC.
Cambessedesia espora (A.St.Hil. ex
Bonpl.) DC.
Cambessedesia hilariana (A.St.Hil. ex
Bonpl.) DC.
Castratella piloseloides (Bonpl.)
Naudin
Centradenia grandifolia (Schltdl.)
Endl. ex Walp.
Centradenia inaequilateralis (Schltdl.
& Cham.) G.Don
Chaetolepis cufodontisii Standl.
Chaetolepis microphylla (Bonpl.) Miq.
Chaetostoma armatum (Spreng.)
Cogn.
Collector, number
(herbarium)
Provenance
nrITS
accd-psaI
psbK-psbL
Diaz, W., 4538 (NY)
Martin, C. V., 487 (NY)
Brazil
French Guiana
JQ730036
JQ730037
JQ730247
JQ730248
JQ730456
JQ730457
Caddah, M.K., 621 (NY)
Martin, C. V., 411 (NY)
Guimarães, P., 317 (RB)
Brazil
French Guiana
Brazil
JQ730038
JQ730039
JQ730040
JQ730249
JQ730250
JQ730251
JQ730458
JQ730459
JQ730460
Martin, C. V., 422 (NY)
Goldenberg, R., 850 (NY)
French Guiana
Brazil
JQ730041
JQ730042
JQ730252
JQ730253
JQ730461
JQ730462
Goldenberg, R., 826 (NY)
Wurdack, K. J., 4145 (NY)
Brazil
Guyana
JQ730043
JQ730044
JQ730254
JQ730255
JQ730463
JQ730464
Michelangeli, F. A., 826 (BH)
Almeda, F., 8669 (CAS)
Almeda, F., 8723 (CAS)
Almeda, F., 8624 (CAS)
Martin, C. V., 441 (NY)
Venezuela
Madagascar
Madagascar
Madagascar
French Guiana
JQ730045
JQ730046
JQ730047
JQ730048
JQ730049
JQ730256
JQ730257
JQ730258
JQ730259
JQ730260
JQ730465
JQ730466
JQ730467
–
JQ730468
DQ985619
–
–
AY460429
–
–
Penneys, D. S., 1429 (FLAS)
Alford, M., 3083 (BH)
Penneys, D. S., 1603 (FLAS)
Mexico
Ecuador
Ecuador
JQ730050
JQ730051
JQ730052
JQ730261
JQ730262
JQ730263
JQ730469
JQ730470
JQ730471
Penneys, D. S., 1594 (FLAS)
Penneys, D. S., 1604 (FLAS)
Penneys, D. S., 1593 (FLAS)
Clark, J. L., 8896 (NY)
Penneys, D. S., 1554 (FLAS)
Penneys, D. S., 1555 (FLAS)
Nee, M., 55327 (NY)
Ecuador
Ecuador
Ecuador
Ecuador
Ecuador
Ecuador
Bolivia
JQ730053
JQ730054
JQ730055
JQ730056
JQ730057
JQ730058
JQ730059
JQ730264
JQ730265
JQ730266
JQ730267
JQ730268
JQ730269
JQ730270
JQ730472
JQ730473
JQ730474
JQ730475
JQ730476
JQ730477
JQ730478
Penneys, D. S., 1586 (FLAS)
Ecuador
JQ730060
JQ730271
JQ730479
Alvear, M., 1398 (CAS)
Guimarães, P., 397 (RB)
Colombia
Brazil
JQ730061
JQ730062
JQ730272
JQ730273
JQ730480
JQ730481
Guimarães, P., 405 (RB)
Brazil
JQ730063
JQ730274
JQ730482
Gonzalez, F., 3830 (COL)
Colombia
JQ730064
JQ730275
JQ730483
Penneys, D. S., 1544 (FLAS)
Costa Rica
JQ730065
JQ730276
–
Michelangeli, F. A., 838-a (NY)
Costa Rica
JQ730066
JQ730277
JQ730484
Michelangeli, F. A., 1160 (NY)
Michelangeli, F. A., 1268 (NY)
Guimarães, P., 396 (RB)
Costa Rica
Brazil
Brazil
JQ730067
JQ730068
JQ730069
JQ730278
JQ730279
JQ730280
JQ730485
JQ730486
JQ730487
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 38–60
56
F. A. MICHELANGELI ET AL.
APPENDIX Continued
Species
Comolia microphylla Benth.
Comolia sertularia (DC.) Triana
Comolia vernicosa (Benth.) Triana
Desmocelis villosa (Aubl.) Naudin
Dichaetanthera africana Jacq.-Fél.
Dichaetanthera oblongifolia Baker
Dionycha bojeri Naudin
Dissotis cf. phaeotricha Harv.
Dissotis multiflora (Sm.) Triana
Eriocnema fulva Naudin
Ernestia confertiflora Wurdack
Ernestia glandulosa Gleason
Ernestia pullei Gleason
Ernestia tenella (Bonpl.) DC.
Fritzchia erecta Cham.
Graffenrieda latifolia (Naudin)
Triana
Graffenrieda moritziana Triana
Guyonia ciliata Hook.f.
Heterocentron elegans (Schltdl.)
Kuntze
Heterocentron muricatum Gleason
Heterocentron subtriplinervium (Link
& Otto) A.Braun & C.D.Bouché
Heterotis decumbens (P.Beauv.) Trian
Heterotis rotundifolia (Sm.) Jacq.-Fél.
Itatiaia cleistopetala Ule
Lavoisiera imbricata (Thunb.) DC.
Lavoisiera mucorifera Mart. ex
Schrank ex DC.
Lavoisiera pulchella Cham.
Macairea pachyphylla Benth.
Macairea radula (Bonpl.) DC.
Macairea thyrsiflora DC.
Marcetia acerosa DC.
Marcetia eimeriana A.B.Martins &
E.M.Woodgyer
Marcetia ericoides Cogn.
Marcetia harleyii Wurdack
Marcetia latifolia Naudin
Marcetia taxifolia (A.St.Hil.) DC.
Melastoma affine D.Don
Melastoma candidum D.Don
Melastoma denticulatum Labill.
Melastoma dodecandrum Desr.
Melastoma intermedium Dunn
Melastoma malabathrichum L.
Melastoma sanguineum Sims
Meriania longifolia (Naudin) Cogn.
Miconia dodecandra (Desr.) Cogn.
Miconia tomentosa (Rich.) D.Don ex
DC.
Microlepis oleaefolia (DC.) Triana
Monochaetum bonplandii (Kunth.)
Naudin
Collector, number
(herbarium)
Provenance
nrITS
accd-psaI
psbK-psbL
Redden, K. M., 1454 (NY)
Almeda, F., 7724 (CAS)
Wurdack, K. J., 4181 (NY)
Michelangeli, F. A., 827 (BH)
Smith, S., 1885 (US)
Almeda, F., 7926a (CAS)
Almeda, F., 8626 (CAS)
Steiner, K., 3561 (NBG)
Smith, S., 1886 (US)
Almeda, F., 8414 (CAS)
Penneys, D. S., 1913 (FLAS)
Martin, C. V., 471 (NY)
Martin, C. V., 460 (NY)
Michelangeli, F. A., 386 (BH)
Guimarães, P., 406 (RB)
Michelangeli, F. A., 794 (BH)
Guyana
Brazil
Guyana
Venezuela
Gabon
Madagascar
Madagascar
Madagascar
Gabon
Brazil
French Guiana
French Guiana
French Guiana
Venezuela
Brazil
Venezuela
JQ730070
JQ730071
JQ730072
JQ730073
JQ730074
JQ730075
JQ730076
JQ730078
JQ730077
EF418811
JQ730079
JQ730080
JQ730081
JQ730082
JQ730083
AY460450
JQ730281
JQ730282
JQ730283
JQ730284
JQ730285
JQ730286
JQ730287
JQ730289
JQ730288
JQ730291
JQ730292
JQ730293
JQ730294
JQ730295
JQ730296
JQ730297
JQ730488
JQ730489
JQ730490
JQ730491
JQ730492
JQ730493
JQ730494
JQ730496
JQ730495
JQ730497
JQ730498
JQ730499
JQ730500
JQ730501
JQ730502
JQ730503
Michelangeli, F. A., 832 (BH)
Mambo, P., 248 (NY)
Cultivated NY, (NY)
Venezuela
Cameroon
USA*
AY460451
JQ730084
JQ730085
JQ730298
–
JQ730299
JQ730504
JQ730505
JQ730506
Penneys, D. S., 1949 (FLAS)
Penneys, D. S., 1430 (FLAS)
USA*
Mexico
JQ730086
JQ730087
JQ730300
JQ730301
JQ730507
JQ730508
Smith, S., 1705 (US)
Penneys, D. S., 1304 (FLAS)
Baumgratz, J. F. A, 1138b (R)
Goldenberg, R., 820 (NY)
Guimarães, P., 345 (RB)
Gabon
Dominica*
Brazil
Brazil
Brazil
JQ730088
JQ730089
JQ730090
JQ730091
JQ730092
JQ730302
JQ730290
JQ730303
JQ730304
JQ730305
JQ730509
–
JQ730510
JQ730511
JQ730512
Goldenberg, R., 814 (NY)
Redden, K. M., 3869 (NY)
Lima, J., 715 (UPCB)
Wurdack, K. J., 4153 (NY)
Santos, A. K. A., 681 (UFB)
Santos, A. K. A., 832 (UFB)
Brazil
Guyana
Brazil
Guyana
Brazil
Brazil
JQ730093
JQ730094
JQ730095
JQ730096
JQ730097
JQ730098
JQ730306
–
JQ730307
JQ730308
–
JQ730309
JQ730513
–
JQ730514
JQ730515
JQ730516
JQ730517
Santos, A. K.
Santos, A. K.
Santos, A. K.
Michelangeli,
Brazil
Brazil
Brazil
Venezuela
JQ730099
JQ730100
JQ730101
JQ730102
GQ265878
JQ730103
JQ730104
JQ730310
–
–
JQ730311
–
JQ730312
JQ730313
JQ730518
JQ730519
JQ730520
JQ730521
–
JQ730522
JQ730523
GQ265883
GQ265879
JQ730105
JQ730106
AY460454
AY460506
–
–
JQ730314
JQ730315
JQ730316
JQ730317
–
–
JQ730524
JQ730525
JQ730526
JQ730527
EF418905
JQ730318
JQ730528
JQ730107
JQ730108
JQ730319
JQ730320
JQ730529
JQ730530
A., 532 (UFB)
A., 558 (UFB)
A., 366 (UFB)
F. A., 680 (BH)
Chen, C. H., 6443 (TAIE)
Simmons, M. P., 1842 (BH)
Penneys, D. S., 1998 (CAS)
Penneys, D. S., 2000 (CAS)
Michelangeli, F. A., 610 (BH)
Judd, W. S., 8093 (FLAS)
Taiwan
New
Caledonia
Michelangeli, F. A., 1344 (NY)
China
China
Venezuela
Dominican
Republic
Brazil
Goldenberg, R., 1036 (NY)
Michelangeli, F. A., 1239 (NY)
Brazil
Venezuela
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 38–60
NEW WORLD MELASTOMEAE (MELASTOMATACEAE)
57
APPENDIX Continued
Species
Monochaetum discolor H. Karst. ex
Triana
Monochaetum humboldtianum
(Kunth & Boché) Kunth ex Walp.
Monochaetum meridense (Klotzsch ex
H.Karst.) Naudin
Monochaetum polyneuron Triana
Monochaetum tenellum Naudin
Monochaetum uribei Wurdack
Monochaetum volcanicum Cogn.
Nepsera aquatica (Aubl.) Naudin
Osbeckia australiana Naudin
Osbeckia courtalensis Gamble
Osbeckia nepalensis Hook.
Osbeckia stellata Buch.-Ham. ex Ker
Gawl.
Pachyloma huberioides (Naudin)
Triana
Physeterostemon tomasii Amorim,
Michelangeli & Goldenb.
Pilocosta campanensis (Almeda &
Whiffin) Almeda
Pilocosta nana (Standl.) Almeda &
Whiffin
Pilocosta nubicola Almeda
Pilocosta oerstedii (Triana) Almeda &
Whiffin
Pterogastra divaricata (Bonpl.)
Naudin
Pterogastra minor Naudin
Pterolepis sp.
Pterolepis alpestris (DC.) Triana
Pterolepis glomerata (Rottb.) Miq.
Pterolepis parnasiifolia (DC.) Triana
Pterolepis repanda (DC.) Triana
Pterolepis rotundifolia Wurdack
Rhexia alifanus Walter
Rhexia aristosa Britton
Rhexia cubensis Griseb.
Rhexia lutea Walter
Rhexia mariana L.
Rhexia nashii Small
Rhexia nutallii C.W.James
Rhexia parviflora Chapm.
Rhexia petiolata Walter
Rhexia salicifolia Kral & Bostick
Rhexia virginica L.
Rhynchanthera bracteata Triana
Rhynchanthera grandiflora (Aubl.)
DC.
Rhynchanthera serrulata (Rich.) DC.
Rousseauxia andringitrensis
(H.Perrier) Jacq.-Fél.
Rousseauxia minimifolia (Jum. &
H.Perrier) Jacq.-Fél.
Collector, number
(herbarium)
Provenance
nrITS
accd-psaI
psbK-psbL
Capote I., 811 (NY)
Venezuela
JQ730109
JQ730321
JQ730531
Michelangeli, F. A., 796 (BH)
Venezuela
JQ730110
JQ730322
JQ730532
Capote I., 862 (NY)
Venezuela
JQ730111
JQ730323
JQ730533
Michelangeli, F. A., 1267 (NY)
Venezuela
Mendoza, H., 17593 (FMB)
Michelangeli, F. A., 718 (BH)
Struwe, L., 1158 (NY)
Brennan, K. G., 7008 (NY)
Klackenberg, 376 (NY)
Penneys, D. S., 1986 (CAS)
Penneys, D. S., 1969 (CAS)
Colombia
Costa Rica
Puerto Rico
Australia
India
China
China
JQ730112
AY460432
JQ730113
JQ730114
JQ730115
JQ730116
JQ730117
JQ730118
JQ730119
JQ730324
–
JQ730325
JQ730326
JQ730327
JQ730328
–
JQ730329
JQ730330
JQ730534
–
JQ730535
JQ730536
JQ730537
JQ730538
–
JQ730539
JQ730540
Caddah, M.K., 558 (NY)
Brazil
JQ730120
JQ730331
JQ730541
Amorim, A., 5054 (NY)
Brazil
JQ730121
JQ730332
JQ730542
Penneys, D. S., 1647 (FLAS)
Panama
JQ730122
JQ730333
JQ730543
Moran, R. C., 6928 (NY)
Costa Rica
JQ730123
JQ730334
JQ730544
Penneys, D. S., 1775 (FLAS)
Kriebel, R., 5412 (NY)
Costa Rica
Costa Rica
JQ730124
JQ730125
JQ730335
JQ730336
JQ730545
JQ730546
Michelangeli, F. A., 540 (BH)
Venezuela
JQ730126
JQ730337
JQ730547
Romero, G. A., 1682 (CAS)
Nee, M., 55383 (NY)
Almeda, F., 8469 (CAS)
Martin, C. V., 419 (NY)
Almeda, F., 8306 (CAS)
Almeda, F., 7731 (CAS)
Almeda, F., 8290 (CAS)
Brazil
Bolivia
Brazil
French Guiana
Brazil
Brazil
Brazil
Naczi, R. F. C., 12065 (NY)
USA
Longbottom, W. D., 11730
(NY)
USA
JQ730127
JQ730133
JQ730128
JQ730129
JQ730130
JQ730131
JQ730132
DQ985623
JQ730134
DQ985627
DQ985628
JQ730135
JQ730338
JQ730344
JQ730339
JQ730340
JQ730341
JQ730342
JQ730343
–
JQ730345
–
–
–
JQ730548
JQ730554
JQ730549
JQ730550
JQ730551
JQ730552
JQ730553
–
JQ730555
–
–
JQ730556
Michelangeli, F. A., 1448 (NY)
Zenteno, F., 8801 (NY)
Michelangeli, F. A., 541 (BH)
USA
Bolivia
Venezuela
DQ985662
DQ985634
DQ985636
DQ985637
DQ985639
JQ730136
JQ730137
JQ730138
–
–
–
–
–
JQ730346
JQ730347
JQ730348
–
–
–
–
–
JQ730557
JQ730558
JQ730559
Michelangeli, F. A., 828 (BH)
Almeda, F., 9390 (CAS)
Venezuela
Madagascar
AY460435
JQ730139
JQ730349
JQ730350
JQ730560
JQ730561
Almeda, F., 8704 (CAS)
Madagascar
JQ730140
JQ730351
JQ730562
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 38–60
58
F. A. MICHELANGELI ET AL.
APPENDIX Continued
Species
Sandemania hoehnei (Cogn.)
Wurdack
Siphanthera hostmanii Cogn.
Svitramia hatschbachii Wurdack
Svitramia minor R.Romero &
A.B.Martins
Svitramia pulchra Cham.
Svitramia sp. ined. 1
Svitramia sp. ined. 2
Svitramia wurdackiana R.Romero &
A.B.Martins
Tibouchina aegopogon (Naud.) Cogn.
Tibouchina aemula (Triana) Cogn.
Tibouchina alpestris Cogn.
Tibouchina angustifolia (Naudin)
Cogn.
Tibouchina arborea (Gardn.) Cogn.
Tibouchina arenaria Cogn.
Tibouchina aspera Aubl.
Tibouchina aspera var asperima
Cogn.
Tibouchina axillaris Cogn.
Tibouchina barnebyana Wurdack
Tibouchina benthamiana (Gardn.)
Cogn.
Tibouchina bicolor (Naudin) Cogn.
Tibouchina bipenicillata (Naudin)
Cogn.
Tibouchina blanchetiana Cogn.
Tibouchina boudetii P.J.F.Guim. &
Goldenb.
Tibouchina breedlovei Wurdack
Tibouchina candolleana (DC.) Cogn.
Tibouchina cardinalis (Bonpl.) Cogn.
Tibouchina castellensis Brade
Tibouchina cerastifolia (Naudin)
Cogn.
Tibouchina chamaecistus (Naudin)
Cogn.
Tibouchina ciliaris (Vent.) Cogn.
Tibouchina cinerea Cogn.
Tibouchina citrina (Naudin) Cogn.
Tibouchina clavata (Pers.) Wurdack
Tibouchina clidemiodes (O.Berg ex
Triana) Cogn.
Tibouchina clinopodifolia (DC.) Cogn.
Tibouchina confertiflora (Naudin)
Cogn.
Tibouchina corymbosa (Raddi) Cogn.
Tibouchina cristata Brade
Tibouchina cryptadena Gleason
Tibouchina dubia (Cham.) Cogn.
Tibouchina estrellensis (Raddi) Cogn.
Tibouchina fissinervia DC.
Tibouchina fothergillae (Schrank &
Mart. ex DC.) Cogn.
Tibouchina foveolata Cogn.
Collector, number
(herbarium)
Provenance
nrITS
accd-psaI
psbK-psbL
Goldenberg, R., 1007 (NY)
Brazil
JQ730141
JQ730352
JQ730563
Wurdack, K. J., 4142 (NY)
Guimarães, P., 391 (RB)
Guimarães, P., 390 (RB)
Guyana
Brazil
Brazil
JQ730142
JQ730143
JQ730144
JQ730353
JQ730354
JQ730355
JQ730564
JQ730565
JQ730566
Guimarães,
Guimarães,
Guimarães,
Guimarães,
Brazil
Brazil
Brazil
Brazil
JQ730145
JQ730146
JQ730147
JQ730148
JQ730356
JQ730357
JQ730358
JQ730359
JQ730567
JQ730568
JQ730569
JQ730570
Almeda, F., 9523 (CAS)
Guimarães, P., 313 (RB)
Nee, M., 55379 (NY)
Almeda, F., 9568 (CAS)
Brazil
Brazil
Bolivia
Brazil
–
JQ730149
JQ730150
JQ730151
–
JQ730360
JQ730361
JQ730362
JQ730571
JQ730572
JQ730573
JQ730574
Guimarães, P., 324 (RB)
Guimarães, P., 352 (RB)
Martin, C. V., 409 (NY)
Martin, C. V., 423 (NY)
Brazil
Brazil
French Guiana
French Guiana
JQ730152
JQ730153
JQ730154
JQ730155
JQ730363
JQ730364
JQ730365
JQ730366
JQ730575
JQ730576
JQ730577
JQ730578
Guimarães, P., 338 (RB)
Almeda, F., 8262 (CAS)
Almeda, F., 9759 (CAS)
Brazil
Brazil
Brazil
JQ730156
JQ730157
JQ730158
JQ730367
JQ730368
JQ730369
JQ730579
–
JQ730580
Nee, M., 55307 (NY)
Michelangeli, F. A., 735 (BH)
Bolivia
Venezuela
JQ730159
JQ730160
JQ730370
JQ730371
JQ730581
JQ730582
Santos, A. K. A., 332 (UFB)
Kollman & Goldenberg, 8563
(NY)
Kelly, L., 1361 (CAS)
Lima, J., 711 (UPCB)
Guimarães, P., 407 (RB)
Goldenberg, R., 1071 (NY)
Varassin, I. G., 96 (UPCB)
Brazil
Brazil
JQ730161
JQ730162
JQ730372
JQ730373
–
JQ730583
Mexico
Brazil
Brazil
Brazil
Brazil
JQ730163
JQ730164
JQ730165
JQ730166
JQ730167
JQ730374
JQ730375
JQ730376
JQ730377
–
JQ730584
JQ730585
JQ730586
JQ730587
JQ730588
Penneys, D. S., 1276 (FLAS)
Martinique
JQ730168
JQ730378
JQ730589
Kriebel, R., 5461 (NY)
Almeda, F., 9843 (CAS)
Nee, M., 55308 (NY)
Santos, A. K. A., 696 (UFB)
Goldenberg, R., 1439 (NY)
Costa Rica
Brazil
Bolivia
Brazil
Brazil
JQ730169
JQ730170
JQ730171
JQ730172
JQ730173
–
JQ730379
JQ730380
JQ730381
JQ730382
JQ730590
JQ730591
JQ730592
JQ730593
–
Goldenberg, R., 774 (NY)
Nee, M., 55377 (NY)
Brazil
Bolivia
JQ730174
JQ730175
JQ730383
JQ730384
JQ730594
JQ730595
Guimarães, P., 327 (RB)
Baumgratz, J. F. A, 819 (R)
Michelangeli, F. A., 708 (BH)
Varassin, I. G., 101 (UPCB)
Guimarães, P., 340 (RB)
Guimarães, P., 351 (RB)
Guimarães, P., 314 (RB)
Brazil
Brazil
Venezuela
Brazil
Brazil
Brazil
Brazil
JQ730176
JQ730177
JQ730178
JQ730179
JQ730180
JQ730181
JQ730182
JQ730385
JQ730386
JQ730387
JQ730388
JQ730389
JQ730390
JQ730391
JQ730596
JQ730597
JQ730598
JQ730599
JQ730600
JQ730601
JQ730602
Guimarães, P., 350 (RB)
Brazil
JQ730183
JQ730392
JQ730603
P.,
P.,
P.,
P.,
388
402
400
395
(RB)
(RB)
(RB)
(RB)
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 38–60
NEW WORLD MELASTOMEAE (MELASTOMATACEAE)
59
APPENDIX Continued
Species
Tibouchina fraterna N.E.Br.
Tibouchina frigidula (DC.) Cogn.
Tibouchina gardneriana (Triana)
Cogn.
Tibouchina gayana (Naudin) Cogn.
Tibouchina geitneriana (Schltdl.)
Cogn.
Tibouchina gleasoniana Wurdack
Tibouchina gracilis (Bonpl.) Cogn.
Tibouchina granulosa (Desr.) Cogn.
Tibouchina grossa (L.f.) Cogn.
Tibouchina heteromalla (D.Don)
Cogn.
Tibouchina hieracioides (DC.) Cogn.
Tibouchina hospita (DC.) Cogn.
Tibouchina inopinata Wurdack
Tibouchina itatiaiae Cogn.
Tibouchina kleinii Wurdack
Tibouchina laevicaulis Wurdack
Tibouchina laxa (Desr.) Cogn.
Tibouchina lepidota (Bonpl.) Baill.
Tibouchina lindeniana Cogn.
Tibouchina llanorum Wurdack
Tibouchina longifolia (Vahl) Baill.
Tibouchina macrochiton (Mart. ex
DC.) Cogn.
Tibouchina manicata Cogn.
Tibouchina martialis (Cham.) Cogn.
Tibouchina martiusiana (DC.) Cogn.
Tibouchina melanocalyx R. Romero,
P. J. F. Guimaraes & Leoni
Tibouchina microphylla Cogn. ex
Schwacke
Tibouchina minor Cogn.
Tibouchina mollis (Bonpl.) Cogn.
Tibouchina mutabilis Cogn.
Tibouchina naudiniana (Decne)
Cogn.
Tibouchina nodosa Wurdack
Tibouchina octopetala Cogn.
Tibouchina oreophilla Wurdack
Tibouchina ornata (Sw.) Baill.
Tibouchina papyrus (Pohl) Toledo
Tibouchina pendula Cogn.
Tibouchina pereirae Brade & Markgr.
Tibouchina pulchra (Cham.) Cogn.
Tibouchina radula Markgr.
Tibouchina ramboi Brade
Tibouchina salviaefolia Cogn.
Tibouchina sebastianopolitana
(Raddi) Cogn.
Tibouchina sellowiana Cogn.
Tibouchina semidecandra (Schrank &
Mart. ex DC.) Cogn.
Tibouchina sp.
Tibouchina sp. ined. 1
Tibouchina sp. ined. 2
Collector, number
(herbarium)
Provenance
nrITS
accd-psaI
psbK-psbL
Michelangeli, F. A., 512 (BH)
Guimarães, P., 394 (RB)
Guimarães, P., 305 (RB)
Venezuela
Brazil
Brazil
JQ730184
JQ730185
JQ730186
JQ730393
JQ730394
JQ730395
JQ730604
JQ730605
JQ730606
Nee, M., 55380 (NY)
Capote I., 852 (NY)
Bolivia
Venezuela
JQ730187
JQ730188
JQ730396
JQ730397
JQ730607
JQ730608
Jaramillo, J., 7985 (NY)
Guimarães, P., 336 (RB)
Guimarães, P., 378 (RB)
Zabala, J. C., 1 (NY)
Guimarães, P., 339 (RB)
Colombia
Brazil
Brazil
Colombia
Brazil
JQ730189
JQ730190
JQ730191
JQ730192
JQ730193
–
JQ730398
JQ730399
JQ730400
JQ730401
JQ730609
JQ730610
JQ730611
JQ730612
JQ730613
Almeda, F., 8380 (CAS)
Baumgratz, J. F. A, 1008 (R)
Kriebel, R., 5342 (NY)
Guimarães, P., 310 (RB)
Almeda, F., 9868 (CAS)
Guimarães, P., 412 (RB)
Harling, G., 23570 (NY)
Morales, M. E., sn (UPTC)
Michelangeli, F. A., 1269 (NY)
Michelangeli, F. A., 736 (BH)
Michelangeli, F. A., 816 (BH)
Guimarães, P., 320 (RB)
Brazil
Brazil
Costa Rica
Brazil
Brazil
Brazil
Ecuador
Colombia
Brazil
Venezuela
Venezuela
Brazil
JQ730194
JQ730195
JQ730196
JQ730197
JQ730198
JQ730199
JQ730200
JQ730201
JQ730202
JQ730203
JQ730204
JQ730205
JQ730402
JQ730403
JQ730404
JQ730405
JQ730406
JQ730407
JQ730408
JQ730409
JQ730410
JQ730411
JQ730412
JQ730413
JQ730614
JQ730615
JQ730616
JQ730617
JQ730618
JQ730619
JQ730620
JQ730621
JQ730622
JQ730623
JQ730624
JQ730625
Guimarães, P., 328 (RB)
Goldenberg, R., 821 (NY)
Guimarães, P., 335 (RB)
Guimarães, P., 341 (RB)
Brazil
Brazil
Brazil
Brazil
JQ730206
JQ730207
JQ730208
JQ730209
JQ730414
JQ730415
JQ730416
JQ730417
JQ730626
JQ730627
JQ730628
JQ730629
Guimarães, P., 344 (RB)
Brazil
JQ730210
JQ730418
JQ730630
Guimarães, P., 393 (RB)
Penneys, D. S., 1895 (FLAS)
Lobão, A, 1450 (RB)
CULTIVATED NY, (NY)
Brazil
Ecuador
Brazil
USA*
JQ730211
JQ730212
JQ730213
JQ730214
JQ730419
JQ730420
JQ730421
JQ730422
JQ730631
JQ730632
JQ730633
JQ730634
Santos, A. K. A., 1049 (UFB)
Salomon, J. C., 14934 (CAS)
Santos, A. K. A., 829 (UFB)
Penneys, D. S., 1298 (FLAS)
Guimarães, P., 380 (RB)
Penneys, D. S., 1893 (FLAS)
Santos, A. K. A., 302 (UFB)
Baumgratz, J. F. A, 1068 (R)
Goldenberg, R., 1281 (NY)
Almeda, F., 9889 (CAS)
Guimarães, P., 322 (RB)
Guimarães, P., 330 (RB)
Brazil
Brazil
Brazil
Dominica
Brazil
Ecuador
Brazil
Brazil
Brazil
Brazil
Brazil
Brazil
JQ730215
JQ730216
JQ730217
JQ730218
JQ730219
JQ730220
JQ730221
JQ730222
JQ730223
JQ730224
JQ730225
JQ730226
JQ730423
JQ730424
JQ730425
JQ730426
JQ730427
JQ730428
JQ730429
JQ730430
JQ730431
JQ730432
JQ730433
JQ730434
JQ730635
JQ730636
JQ730637
JQ730638
JQ730639
JQ730640
JQ730641
JQ730642
JQ730643
JQ730644
JQ730645
JQ730646
Guimarães, P., 331 (RB)
Goldenberg, R., 765 (NY)
Brazil
Brazil
JQ730227
JQ730228
JQ730435
JQ730436
JQ730647
JQ730648
Nee, M., 55287 (RB)
Goldenberg, R., 1143 (NY)
Goldenberg, R., 1150 (NY)
Brazil
Brazil
Brazil
JQ730230
JQ730231
JQ730232
JQ730438
JQ730439
JQ730440
JQ730650
JQ730651
JQ730652
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 38–60
60
F. A. MICHELANGELI ET AL.
APPENDIX Continued
Species
Tibouchina sp. ined. 3
Tibouchina stenocarpa (DC.) Cogn.
Tibouchina striphnocalyx (DC.)
Pittier
Tibouchina trichopoda (DC.) Baill.
Tibouchina trinervia Cogn.
Tibouchina urceolaris (DC.) Cogn.
Tibouchina ursina (Cham.) Cogn.
Tibouchina valtheri Cogn.
Tibouchina velutina (Naudin) Cogn.
Tibouchina wurdackii Almeda &
Todzia
Tibouchinopsis mirabilis Brade &
Markgr.
Trembleya laniflora Cogn.
Trembleya parviflora Cogn.
Trembleya pentagona Naudin
Tristemma coronatum Benth.
Tristemma hirtum P. Beauv.
Tristemma littorale Benth.
Tristemma mauritianum J. F. Gmel.
Collector, number
(herbarium)
Provenance
nrITS
accd-psaI
psbK-psbL
Guimarães, P., 377 (NY)
Nee, M., 55386 (NY)
Michelangeli, F. A., 379 (BH)
Bolivia
Bolivia
Venezuela
JQ730229
JQ730233
JQ730234
JQ730437
JQ730441
JQ730442
JQ730649
JQ730653
JQ730654
Lobão, A, 1437 (RB)
Almeda, F., 9682 (CAS)
Guimarães, P., 321 (RB)
Almeda, F., 9859 (CAS)
Almeda, F., 8443 (CAS)
Santos, A. K. A., 349 (UFB)
Penneys, D. S., 1749 (FLAS)
Brazil
Brazil
Brazil
Brazil
Brazil
Brazil
Panama
JQ730235
–
JQ730236
JQ730237
JQ730238
JQ730239
JQ730240
JQ730443
JQ730444
JQ730445
JQ730446
JQ730447
JQ730448
JQ730449
JQ730655
JQ730656
JQ730657
JQ730658
JQ730659
JQ730660
JQ730661
Santos, A. K. A., 338 (UFB)
Brazil
JQ730241
JQ730450
JQ730662
Goldenberg, R., 824 (NY)
Brazil
Schmidt, H. H., 3386 (CAS)
Smith, S., 1879 (US)
Smith, S., 1725 (US)
Almeda, F., 8021 (CAS)
Ghana
Gabon
Gabon
Madagascar
AY553744
JQ730242
AY553745
JQ730243
JQ730244
JQ730245
JQ730246
–
JQ730451
–
JQ730452
JQ730453
JQ730454
JQ730455
–
JQ730663
–
JQ730664
JQ730665
JQ730666
JQ730667
*Collected in cultivation outside native range.
–, locus not sequenced.
© 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 38–60