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Phylogeny of Calliandra (Leguminosae: Mimosoideae) based on nuclear and plastid molecular markers

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We reconstructed phylogenetic relationships in Leguminosae subfam. Mimosoideae tribe Ingeae using 135 sequences from the nuclear (ITS) and 119 from the plastid (trnL-F) genome, representing 23 of the 36 currently recognized genera in the tribe with newly generated sequences of Blanchetiodendron, Guinetia, Macrosamanea, Thailentadopsis and Viguieranthus and an extensive sampling of Calliandra. Only two of the five Neotropical generic alliances of Barneby & Grimes (1996) were supported as monophyletic. Calliandra is resolved as monophyletic with the inclusion of Guinetia. The five previously proposed sections within Calliandra were not supported by our study. Nevertheless, based on these results, a new infrageneric classifica- tion is proposed for Calliandra, and the African species of the genus are assigned to a new genus, Afrocalliandra. Three new sections are proposed for Calliandra: (1) sect. Tsugoideae based on C. ser. Tsugoideae, with four species from northwestern South America; (2) sect. Septentrionales, with six species distributed in dry areas from the United States to Mexico and (3) sect. Monticola, which consists of species restricted to the Espinhaço range of Brazil; these latter species form a clade with low levels of sequence variation, a potential indicator of the recent diversification of this group.
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INTRODUCTION
Larger genera of Leguminosae subfam. Mimosoideae have
a long history of taxonomic complexity and nomenclatural in-
stability. The attention devoted to unravel the non-monophyly
of Acacia Mill. s.l. (e.g., Miller & Bayer, 2001, 2003; Brown
& al., 2008; Murphy & al., 2010; Miller & Seigler, 2012) is such
an example. Nevertheless, recent studies of the phylogeny of
particular groups demonstrated that several genera, as tradi-
tionally delimited, are not monophyletic and/or require signifi-
cant taxonomic adjustments, for example: Piptadenia Benth.
(Jobson & Luckow, 2007), Prosopis L. (Burghardt & Espert,
2007; Catalano & al., 2008), Mimosa L. (Bessega & al., 2008;
Simon & al., 2011), Albizia Durazz. (Brown & al., 2008), and
Paraserianthes I.C. Nielsen (Brown & al., 2011).
The taxonomic history of Calliandra Benth. (tribe Ingeae)
mirrors that of other large mimosoid genera such as Mimosa
and Acacia. The genus was established by Bentham (1840)
based on the combination of a monadelphous and polystem-
onous androecium and a fruit with thick margins that dehisces
elastically from the apex and is usually held erect. Eighteen
New World species were included in Calliandra in Bentham’s
treatment. Later, Bentham (1844) presented a more detailed ac-
count of the genus, recognizing 60 species in five series (C. ser.
Macrophyllae Benth., ser. Laetevirentes Benth., ser. Pedic-
ellatae Benth., ser. Nitidae Benth., ser. Racemosae Be nth.),
based on characters of the leaves and inflorescences. The geo-
graphic range of the genus was expanded to the Old World
by Bentham (1875) with the inclusion of four Asian species
(C. cynometroides Beddome, C. geminata Benth., C. griffithii
Benth., C. umbrosa Benth.) because of similar fruit mor-
phology. New species were later proposed from Madagascar
(C. amblyphylla Harms; Harms, 1921) and continental Africa
(C. gilbertii Thulin & Asfaw, C. redacta (J.H. Ross) Thulin
& Asfaw; Thulin & al., 1981).
This increase in size of the genus was somewhat coun-
teracted by the work of Hernández (1986) who segregated the
species of C. ser. Laetevirentes and two species of ser. Macro-
phyllae (C. amazonica Benth., C. aculeata Spruce ex Benth.) to
the new genus Zapoteca H.M. Hern. Barneby (1998) published
a monographic account of Calliandra, described 36 new taxa
and recognized a total of 133 species. Calliandra was kept as
distinct from Zapoteca and restricted to the New World. As a
consequence, 18 Old World species were excluded from Cal-
liandra but not ascribed to any other genus by Barneby (1998).
Subsequently, nine species endemic to Madagascar were in-
cluded in the new genus Viguieranthus Villiers (Villiers,
2002); C. geminata Benth., from India, was considered as a
Phylogeny of Calliandra (Leguminosae: Mimosoideae) based on
nuclear and plastid molecular markers
Élvia Rodrigues de Souza,1 Gwilym P. Lewis,2 Félix Forest,2 Alessandra S. Schnadelbach,3
Cássio van den Berg1 & Luciano Paganucci de Queiroz1
1 Universidade Estadual de Feira de Santana, Departamento de Ciências Biológicas, Feira de Santana, Bahia, Brasil
2 Royal Botanic Gardens, Kew,
Richmond, Surrey, TW9 3AB, U.K.
3 Universidade Federal da Bahia, Departamento de Biologia Geral, Instituto de Biologia, Salvador, Bahia, Brasil
Author for correspondence: Élvia Rodrigues de Souza, elviasouza@yahoo.com.br
Abstract
We reconstructed phylogenetic relationships in Leguminosae subfam. Mimosoideae tribe Ingeae using 135 sequences
from the nuclear (ITS) and 119 from the plastid (trnL-F) genome, representing 23 of the 36 currently recognized genera in the
tribe with newly generated sequences of Blanchetiodendron, Guinetia, Macrosamanea, Thailentadopsis and Viguieranthus
and an extensive sampling of Calliandra. Only two of the five Neotropical generic alliances of Barneby & Grimes (1996) were
supported as monophyletic. Calliandra is resolved as monophyletic with the inclusion of Guinetia. The five previously proposed
sections within Calliandra were not supported by our study. Nevertheless, based on these results, a new infrageneric classifica-
tion is proposed for Calliandra, and the African species of the genus are assigned to a new genus, Afrocalliandra. Three new
sections are proposed for Calliandra: (1) sect. Tsugoideae based on C. ser. Tsugoideae, with four species from northwestern
South America; (2) sect. Septentrionales, with six species distributed in dry areas from the United States to Mexico and (3)
sect. Monticola, which consists of species restricted to the Espinhaço range of Brazil; these latter species form a clade with
low levels of sequence variation, a potential indicator of the recent diversification of this group.
Keywords
Ingeae; phylogenetic analyses and dating; pollen morphology; taxonomy
Supplementary Material
The Electronic Supplement (Table S1; Fig. S1) is available in the Supplementary Data section of the
online version of this article (http://www.ingentaconnect.com/content/iapt/tax).
Received: 22 Oct. 2012; revision received: 7 Apr. 2013; accepted: 5 Sep. 2013. DOI: http://dx.doi.org/10.12705/626.2
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synonym of Thailentadopsis nitida (Vahl) G.P. Lewis & Schrire
(Lewis & Schrire, 2003). Six species formerly described as
Calliandra remained without a definite taxonomic position. To
accommodate these different concepts of Calliandra, we here
refer to Calliandra s.l. as representing the widest historical
circumscription of the genus (i.e., including Zapoteca, Viguier-
anthus and Thailentadopsis Koster mans) and Calliandra s.str.
to represent the delimitation proposed by Barneby (1998).
Hernández (1986) highlighted the importance of polyad
structure in the taxonomy of Calliandra and allied genera. He
segregated Zapoteca because it has acalymmate polyads (i.e.,
the constituent pollen grains do not have a common exine). In
contrast, the polyads of Calliandra are calymmate, having a
common exine to all eight pollen grains and a viscous appendix
in the basal cell that adheres the polyad to a stigmatic surface
during pollination (Greissl, 2006). Besides this polyad struc-
ture, Calliandra s.str. has other morphological features atypical
in tribe Ingeae; for example, the basic chromosome number is 8
or 11 (vs. 13 in the remaining Ingeae; Hernández, 1986), calyx
lobes with imbricate aestivation and unidirectional initiation
of the sepals (vs. valvate aestivation and helicoid initiation;
Prenner, 2004; Prenner & Teppner, 2005) and stamens with
helicoid initiation (vs. simultaneous in other Mimosoideae;
Prenner, 2004; Prenner & Teppner, 2005).
The most recent classification of Calliandra was proposed
by Barneby (1998) who recognized five sections and fourteen
series and put strong emphasis on inf lorescence architecture
in defining sections: a terminal pseudoraceme of heads or um-
bels in C. sect. Calliandra (Fig. 1B, F–L) and sect. Microcallis
Barneby (further differentiated by dimension of the perianth
Fig. 1N); isolated heads or umbels arising from lateral special-
ized short branches in C. sect. Androcallis Barneby (Fig. 1A,
C–E, M, O); an isolated terminal umbel in C. sect. Acroscias
Barneby; and lateral inflorescences associated with stipular
spicules in sect. Acistegia Barneby.
Phylogenetic relationships of Calliandra in tribe Ingeae
have not yet been well established. In some phylogenetic
studies based on morphological data (Grimes, 1995; Barneby
& Grimes, 1996) and on the plastid region trnL-F (Luckow
& al., 2000), Zapoteca appeared as sister to Calliandra. A wider
analysis of Mimosoideae, based on trnL-F, trnK introns, and
matK, including five species of Calliandra, found Cedrelinga
Ducke as sister of Calliandra, but with low support (Luckow
& al., 2003). In more recent phylogenetic studies (Brown & al.,
2008) based on the nuclear ITS and ETS regions, Calliandra
appeared in an unresolved position (in the ITS and combined
ITS + ETS data) or as sister group to Zapoteca (in the ETS
analysis). Lewis & Rico-Arce (2005) included Calliandra in
the “Inga Alliance” of Barneby & Grimes (1996) together with
Archidendron F. Muell, Cedrelinga, Cojoba Britton & Rose,
Guinetia L. Rico & M. Sousa, Macrosamanea Britton & Rose,
Marmaroxylon Killip, Inga Mill., Viguieranthus, Zapoteca and
Zygia P. Brown. Viguieranthus, Guinetia and Thailentadopsis
have not been included in any published phylogenetic study of
the group to date.
As currently circumscribed by Barneby (1998), Calliandra
occurs mostly in seasonally dry tropical forests (SDTFs),
savannas and campos rupestres (open rocky fields) and less
commonly in wet forests and subtropical grasslands, known as
Pampas in southern South America. The region of the Chapada
Diamantina in the Brazilian State of Bahia is the main center
of diversity of the genus, with a total of 46 species of which 36
are restricted to this region. The other major centers of diver-
sity are in North America (southern United States and Mexico
to Central America) with 35 species, and northwestern South
America (Colombia, Venezuela) with 29 species (Barneby,
1998; Souza & Queiroz, 2004; Hernández, 2008; Souza, 2010).
All of these centers of diversity occur in areas with strong
climatic seasonality.
In this paper, we present a phylogenetic study of Calliandra
based on the nuclear ribosomal ITS region, the plastid trnL
intron and the trnL-trnF spacer. We also used a wide sampling
from tribe Ingeae in order to (1) test the monophyly of Calli-
andra and its relationship with other ingoid genera, especially
those formerly included in Calliandra; (2) test the monophyly
of the sections and series proposed by Barneby (1998); (3) in-
vestigate the evolution of morphological characters within the
genus and their diagnostic importance within a proposed new
classification system; and (4) investigate the biogeographical
history of the genus.
MATERIALS AND METHODS
Taxon and DNA region sampling. —
Leaf tissues were
dehydrated in silica-gel from field-collected material in five
Brazilian states and in the state of Guerrero in Mexico. Voucher
specimens are housed in the herbaria of Feira de Santana State
University (HUEFS) and the Universidad Nacional Autónoma
do México (MEXU). Additional samples were taken, with per-
mission, from herbarium sheets at BM, BR, HUEFS, INPA,
K, MEXU, P and W.
The dataset includes 95 of the 141 recognised species of
Calliandra s.str. including three undescribed species (Souza,
ined.). All five sections and twelve of the fourteen series pro-
posed by Barneby were included. The ingroup also includes
representatives of the genera segregated from Calliandra s.l.:
Thailentadopsis (2 of 3 species), Viguieranthus (6/23), Zapoteca
(7/17), as well as the two species of Calliandra from continen-
tal Africa (C. redacta, C. gilbertii) excluded from Calliandra
by Barneby (1998) but not yet positioned in any other genus.
It was not possible to include in the analyses some species
(e.g., C. cynometroides and C. umbrosa, both Indo-Burmese
species) formerly classified in Calliandra because we could
not obtain good-quality DNA.
Also included in our study were representatives of all re-
maining genera of the “Inga Alliance” except for Marmar-
oxylon and Archidendron. Genera included were: Cedrelinga
(monospecific), Cojoba (3 of 12 species), Guinetia (1/1), Inga
(2/300), Macrosamanea (1/11) and Zygia (1/50). Because all
published phylogenetic studies of tribe Ingeae did not identify
well-resolved topologies or well-supported clades, we also sam-
pled representatives of other genera of Ingeae not included in
the Ingeae Alliance: Abarema Pittier (2 of 46 species), Balizia
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Fig. 1.
Inflorescences in Calliandra.
A,
C. dolichopoda H.M. Hern.;
B,
C. physocalyx H.M. Hern. & M. Sousa;
C,
C. dysantha Benth.;
D,
C. ses-
silis Benth.;
E,
C. macrocalyx Harms;
F,
C. lanata Benth.;
G,
C. bahiana Renvoize;
H,
C. coccinea Renvoize;
I,
C. semisepulta Barneby;
J,
C. stel-
ligera Barneby;
K,
C. calycina Benth.;
L,
C. longipinna Benth.;
M,
C. depauperata Benth.;
N,
C. leptopoda Benth.;
O,
C. aeschynomenoides
Benth. — Photos: A–L, E.R. Souza; M–O, L.P. Queiroz.
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Barneby & J.W. Grimes (1/3), Blanchetiodendron Barneby
& J.W. Grimes (monospecific), Ebenopsis Britton & Rose
(1/3), Enterolobium Mart. (1/11), Havardia Small (1/5), Hes-
peralbizia Barneby & J.W. Grimes (monospecific), Hydro-
chorea Barneby & J.W. Grimes (1/3), Leucochloron Barneby
& J.W. Grimes (1/5), Pithecellobium Mart. (1/18), Pseudosa-
manea Harms (1/2), Samanea (Benth.) Merr. (1/3) and Sphinga
Barneby & J.W. Grimes (1/3). As outgroup we used Acacia
spinescens Benth. as a taxon phylogenetically distant from the
Inga Alliance (Miller & al. 2003; Brown & al., 2008). Voucher
details and sequences downloaded from GenBank (http://www
.ncbi.nlm.nih.gov) are listed in Appendix 1.
We tested eight potential molecular markers for variation
in the group, following information from previous phylogenetic
studies in Mimosoideae (Luckow & al., 2000, 2003) and those
suggested by Shaw & al. (2005, 2007): the nuclear ITS/5.8S
region (including ITS1 and ITS2 regions, hereafter referred to
as ITS) and the plastid matK, trnL-F, trnS-G, rps16, trnD-T,
psbA-trnH, rpl32-trnL. We selected the ITS and the trnL-F
regions (both trnL intron and trnL-trnF spacer) because they
had higher substitution rates and proved to be more easily
amplified in the study group than the other regions. In total,
254 sequences were used in this study, 247 of which were newly
generated. For ITS, 135 taxa were sampled and 119 for trnL-F,
with 76 covering the trnL intron and the trnL-trnF spacer and
43 for the trnL intron only.
Primers for the ITS region were 17SE and 26SE (Sun & al.,
1994) for most accessions. For the most difficult materials we
used primers ITS4 and ITS5 (White & al., 1990) and ITS75
and ITS92 (Desfeux & Lejeune, 1996). A combination of prim-
ers 17SE and 26SE with ITS2 and ITS3 (White & al., 1990)
was used when it was necessary to amplify this region in two
separate reactions. The trnL intron and trnL-trnF spacer were
amplified in two reactions, using a combination of the universal
primers “c” and “d”, and “e” and “f” (Taberlet & al., 1991),
respectively.
DNA extraction, amplification and sequencing. —
Lab-
oratory procedures were performed at the Plant Molecular
Systematics Laboratory (LAMOL) of Feira de Santana State
University (UEFS) and at the Jodrell Laboratory of the Royal
Botanic Gardens, Kew. Total DNA was extracted from silica-
gel dried leaves and herbarium material using a modified 2×
CTAB protocol (Doyle & Doyle, 1987).
Polymerase chain reactions were carried out using two
different procedures. In the first approach, the reactions con-
sisted of 22.5 µL of ReddyMix Master Mix (ABgene, Surrey,
U.K.), 5 pmol of each primer, 2% DMSO and 1 µL of total
DNA. Amplifications were carried out as follows: 2 min initial
denaturation at 94°C followed by 35 to 40 cycles of 30 s dena-
turation at 94°C, 1 min annealing at 48°C–50°C and 1.5 min
extension at 72°C, and completed by a final extension of 4 min
at 72°C. The second approach used 50 µL reactions comprising
PCR reaction buffer 1×, 2.5 mM MgCl
2
, 1 mM dNTPs, 7.5 pmol
of each primer, 0.5 µM BSA, 2% DMSO, 1 M betaine and 1.25
units of Taq DNA polymerase (Phoneutria Ltda, Belo Hori-
zonte, Brazil). For ITS, the number of cycles and the annealing
temperature were slightly different depending on the primers
used, as follow: 40 cycles at 48°C–50°C for ITS4 and ITS5, 28
cycles at 54°C–56°C for 17SE and 26SE, and 40 cycles at 58°C
for ITS92 and ITS75. All reactions were carried out in a 9700
GeneAmp Thermocycler (Applied Biosystems, Singapore).
PCR products were purified using the QIAquick kit
(Qiagen, Hilden, Germany) or by enzymatic treatment with
Exonuclease I and shrimp phosphatase alcaline (kit ExoSapIT,
GE Healthcare, Buckinghamshire, U.K.). Sequencing reactions
were carried out with the same primers as used for amplifica-
tions and using the Big Dye Terminator kit version 3.1 (Applied
Biosystems, Foster City, California, U.S.A.). Complementary
strands for each region were sequenced using the automatic se-
quencers Spectrumedix SCE9624 and ABI3130XL at LAMOL
and ABI3100 at the Jodrell. All sequences were deposited in
GenBank (Appendix 1). Aligned data matrices are avalilable
in TreeBase (http://treebase.org, study no. S14957).
Alignment and phylogenetic analyses. —
Complemen-
tary strands were combined and base-calling verified with the
Staden package (Staden & al., 2003) or Sequencher v.4.1 (Gene
Codes Corp., Ann Arbor, Michigan, U.S.A.). Alignments were
performed by eye in PAUP* v.4.0b10 (Swofford, 2002). Gaps
were considered as missing data; most gaps were autapomor-
phic and for this reason were not coded as additional characters.
A total of 231 characters at the ends of the sequences and in
regions of ambiguous alignment were excluded (118 from ITS
and 113 from trnL-F).
The combined data matrix was constructed using 130
taxa, for the majority of which both nuclear and plastid mark-
ers (ITS + trnL-F) could be obtained. Taxa with only one
marker were included in order to sample the morphological
variation and full biogeographical range of Calliandra. These
were: C. belizensis Standl., C. californica Benth., C. dolichop-
oda H.M. Hern., C. eriophylla Benth., C. gilbertii, C. hirsuta
Benth., C. humilis Benth., C. palmeri S. Watson, C. physo-
calyx H.M. Hern. & M. Sousa, C. rhodocephala Donn. Sm.,
C. riparia Pittier, C. trinervia Benth., C. tsugoides R.S. Cowan,
and C. tweedii Benth.
Maximum parsimony (MP) analyses were carried out in
PAUP* v.4.0b10 for Windows (Swofford, 2002) using Fitch par-
simony (all characters unordered and equally weighted; Fitch,
1971). The search for the most parsimonious trees (MPTs) was
carried out using a heuristic search, 1000 random taxon-addi-
tion, and tree bisection-reconnection (TBR) branch swapping,
saving 15 trees per replicate. Trees saved in this first round were
used as starting trees in a second search using the same param-
eters, but saving a maximum of 10,000 trees. Clade support
was estimated with non-parametric bootstrapping (Felsenstein,
1985) with 1000 pseudoreplications, simple taxon-addition and
TBR branch swapping, saving 15 trees per pseudoreplicate.
Maximum likelihood (ML) analyses were carried out using
RAxML (Stamatakis, 2006) as implemented on the CIPRES
v.2.0 gateway (htt p://www.phylo.org). We used the model GTR
+ CAT for both the ITS and trnL-F regions; both regions were
treated a separate partitions. Support was assessed using 1000
replicates and the rapid bootstrap option.
Bayesian analyses were carried out using MrBayes v.3.1.2
(Ronquist & Huelsenbeck, 2003). Best-fit substitution models
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were selected using MrModeltest v.2.3 (Nylander, 2004). Model
GTR + Γ was selected for the trnL, trnL-F and 5.8S regions
and model GTR + I + Γ for ITS1 and ITS2. The analyses were
performed with uniform priors and a random starting tree.
Two simultaneous Monte Carlo Markov Chains (MCMC) were
run for 13,000,000 generations sampling one tree each 1000
generations. Stability of the chains was reached near the be-
ginning of the analysis and trees from the initial 25% of the
runs were discarded as burn-in, as assessed in Tracer v.1.5.
(Rambaut & Drummond, 2003). Remaining trees were used to
compute a 50% majority-rule consensus tree in PAUP* v.4.0b10
(Swofford, 2002), and the frequencies of clades were taken as
estimates of posterior probabilities.
Phylogenetic congruence between the ITS and trnL-F re-
gion datasets was assessed using the partition homogeneity test
(PHT; Felsenstein, 1985). Topological conf licts between trees
resulting from different analyses were checked by eye in case of
significant differences in PHT, and by the use of split networks
with the supernetwork algorithm in Splits Tree v.4.11.3 (Huson
& Bryant, 2006) using 50% majority-rule consensus trees of
the BI and ML analyses.
The possible presence of ITS pseudogenes was investi-
gated through comparison of length and substitution rates in
fast-evolving (ITS 1–2) and conserved (5.8S) regions and the
presence of polymorphic specimens, following the recommen-
dation of Bailey & al. (2003).
Molecular divergence time estimates. —
Divergence time
estimates were obtained using an uncorrelated relaxed molecu-
lar clock as implemented in BEAST v.1.7.2. (Drummond & al.,
2012) based on the combined nuclear and plastid data. Two
calibration points were used in the analysis: the crown node of
Ingeae and Acacia s.str. was set to 23.9 ± 3.1 million years ago
(Ma) based on the results of a previous analysis (Lavin & al.,
2005) assuming a normal prior distribution. A second calibra-
tion point assuming a lognormal prior distribution was based
on a fossil polyad from the Miocene of Argentina, consisting
of eight pollen grains in a monoplanar, calymmate arrangement
(Caccavari & Barreda, 2000), unequivocally belonging to Cal-
liandra. This fossil has an estimated age of 16 ± 1 Ma based on
radiometric dating, and this value was used as the minimum age
constraint for the most recent common ancestor (MRCA) which
represents the stem node of Calliandra with calymmate polyads.
The analysis was carried out using three partitions for ITS
and substitution models GTR + Γ for 5.8S, trnL and trnL-F and
GTR + I + Γ for ITS1 and ITS2. Convergence of all parameters
was evaluated in Tracer v.1.5. (Rambaut & Drummond, 2003).
The maximum clade credibility tree with annotation of pos-
terior probability, mean age, substitution rates and respective
standard deviations was compiled using TreeAnnotator v.1.4.8
(Drummond & Rambaut, 2007). The nodes are named accord-
ing to the majority consensus of 10,000 trees derived from the
Bayesian analysis of the combined dataset.
Biogeography and evolution of morphological characters.
Thirteen morphological characters (Table 1) were selected to
assess potential synapomorphies and provide diagnostic char-
acters for well-supported clades recovered in the molecular
phylogenetic reconstruction. Most characters selected were
Table 1.
Geographical distribution and morphological characters
examined.
Characters States
1 Distribution 1 Amazonia
2 Andes
3 Continental Africa
4 Asia
5 Madagascar
6 NE Brazil without Espinhaço
7 Espinhaço mountain range
8 Central Brazil
9 Subtropical South America
10 North/central Mexico & U.S.A.
11 Central America & Caribbean
12 Australia
13 Northern South America without
Amazonia
2 Habitat 1 Dry Forests
2 Wet Forests
3 Savannas
4 Subtropical grasslands
5 “Campos rupestres”
3 Armament 1 absent
2 present
4 Extrafloral nectaries 1 present
2 absent
5 Number of pinnae per leaf 1 1–2
2 3–10
3 >10
6 Number of leaflets per pinna 1 ≤10
2 11–20
3 > 20
7 Leaflet length 1 ≤10 mm
2 11–20 mm
3 > 20 mm
8 Inflorescence position 1 lateral
2 terminal
9 Inflorescence aggregation 1 compound
2 simple
10 Synflorescence type 1 fascicle
2 pseudoraceme
3 pseudopanicle
11 Partial inflorescence 1 globose capitulum
2 spicate
3 umbelliform
4 raceme
12 Corolla length 1 3–7 mm
2 8–10 mm
3 >10 mm
13 Glandular trichomes 1 absent
2 present
14 Fruit dehiscence 1 elastically from apex to base
2 not elastically dehiscent
3 indehiscent
15 Polyad type 1 7-celled, acalymmate
2 16–32-celled, acalymmate
3 8-celled, calymmate
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used by Barneby (1998) as diagnostic traits of infrageneric
groups of Calliandra. In addition, we assessed the evolution of
pollen traits as these have been used previously to differentiate
generic entities. Ancestral character state reconstructions were
performed using the parsimony criterion in Mesquite v.2.01
(Maddison & Maddison, 2007), and using trees derived from
the Bayesian analysis of the combined dataset. All characters
were coded as unordered and optimized using the ACCTRAN
algorithm on the majority consensus tree of 10,000 trees de-
rived from the Bayesian analysis of the combined dataset using
the option “Trace over Trees” to account for topological uncer-
tainty (Electr. Suppl.: Table S1).
Geographical areas and habitat were optimized using the
same parameters as used to reconstruct the evolution of mor-
phological traits. Based on the distribution range of the Ameri-
can species of Calliandra as provided by Barneby (1998), thir-
teen major geographical areas were coded: Amazonia; Andes;
Asia; Australia; continental Africa; Central America & Carib-
bean; central Brazil; Espinhaço mountain range; Madagas-
car; northeast Brazil without Espinhaço; north/central Mexico
& U.S.A.; northern South America without Amazonia; and
subtropical South America. For the Old World taxa, major con
-
tinental areas were used, i.e., continental Africa, Madagascar,
Asia and Australia. Four major habitats were selected based
mostly on the work of Schrire & al. (2005) who identified the
major global biomes relevant for the diversification history of
the legume family: tropical wet forests, savanna (the “grass rich
biome”), seasonally dry tropical forests (hereinafter SDTF, part
of the global “succulent rich biome”) and subtropical grass-
lands (included in the “temperate biome”). Besides these major
biomes, we added another particular habitat where Calliandra
is particularly rich, the campos rupestres (upland rocky fields)
of the Espinhaço mountain range in the eastern Brazilian states
of Bahia and Minas Gerais.
Pollen morphology. —
Pollen samples were obtained
from dried herbarium specimens deposited in the herbaria
HUEFS, K and MEXU. We sampled three species of Cal-
liandra s.str.: C. debilis Renvoize, C. houstoniana (Miller)
Standl. and C. parviflora Benth.; three Old World species tra-
ditionally included in the genus: C. cynometroides, C. gilbertii
and C. umbrosa, and three species of genera segregated from
Calliandra s.l.: Thailentadopsis nitida, Viguieranthus umbilis-
cus Villiers and Zapoteca formosa (Kunth) H.M. Hern. It was
not possible to include a sample of Guinetia because flowers
are available only on the type specimen.
Pollen samples were acetolysed according to Erdtman
(1960) and then dehydrated in an ethanol series of 50%, 70%,
90% and 100%, for five minutes in each solution. The pollen
grains were then placed on “stubs”, dried at room tempera
-
ture and coated with gold (using a Balzers SCD 050). Electron
micrographs were taken on a LEO 1430VP scanning electron
microscope.
Additional data on pollen morphology was taken from the
literature; for Calliandra from Souza (2007), Santos & Romão
(2008), Guinet & Hernandez (1989), Niezgoda & al. (1983), and
Guinet (1965); for Guinetia from Rico Arce & al. (1999); for
Zapoteca from Guinet & Hernandez (1989), Niezgoda & al.
(1983), and Guinet (1965); for Thailentadopsis from Souza
(2007).
RES U LT S
Phylogenetic reconstructions. —
The aligned ITS region
for 135 accessions comprised 970 characters of which 852 were
used in the analyses; 284 were parsimony-informative (33.3%).
The aligned trnL-F region for 119 accessions comprised 1477
characters, of which 1380 were included in the analyses; 169 of
these were parsimony-informative (12.2%). The concatenated
matrix of 130 accessions contained 2430 characters, with 2,170
included in the analyses; 412 were potentially parsimony infor-
mative (19.1%) (Table 2).
The majority consensus of 10,000 trees derived from the
Bayesian analysis of the combined dataset, ITS + trnL-F, is
shown in Fig. 2. The clades with posterior probabilities equal
to or higher than 0.95 (BI, Bayesian inference) and/or bootstrap
values equal to or higher than 0.75 (MP, maximum parsimony;
ML, maximum likelihood) are indicated on the majority con-
sensus tree and are discussed later.
The trees generated from the ITS and trnL-F datasets are
significantly different in the MP analysis based on the PHT
test (P < 0.01). However, the trees generated from the MP,
ML and BI analyses were not significantly different based on
split networks with the supernetwork algorithm. Clades C, E
and F appeared in all analyses of the individual and combined
datasets, with topological differences occurring in clades G to
K, which were recovered only from the nuclear and combined
datasets (Fig. 3).
Relationships within tribe Ingeae. —
The “Inga alliance”
(sensu Barneby & Grimes, 1996; Lewis & Rico Arce, 2005)
was not recovered as monophyletic in any analysis (e.g., Fig. 2).
Interestingly, with the exception of Calliandra and Abarema,
all genera represented by more than one species were strongly
supported as monophyletic (Fig. 2). Inga, Macro samanea,
Table 2.
Characteristics of each DNA sequence region used.
DNA region
Alignment
length
Variable
characters
Parsimony-
informative
characters MP tree length
Consistency
index
Retention
index
trnL-F 1477 405 169 594 0.77 0.90
ITS 970 422 284 1378 0.50 0.83
Combined data 2430 745 412 1866 0.56 0.84
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• Phylogeny of Calliandra
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Zygia and Leucochloron formed one clade (PP 0.98). The re-
maining genera of the “Inga alliance” (Calliandra, Cojoba,
Guinetia, Viguieranthus, Zapoteca) were placed together in
clade B with Thailentadopsis and with high support only in the
Bayesian analysis based on combined nuclear and plastid data
(PP 0.98, Fig. 2). The monophyly of the “Abarema alliance” and
of the “Pithecellobium alliance” is supported by our analyses
(PP 1.0, BS ML 1.0, BS MP 1.0 and PP 1.0, BS ML 1.0, BS MP
< 0.75, respectively; Fig. 2).
Infrageneric classification of Calliandra s. str.
Callian-
dra s.str., as circumscribed by Barneby (1998), was paraphyletic
because of the inclusion of Guinetia tehuantepecensis L. Rico
& M. Sousa. The sections of Calliandra proposed by Barneby
(1998) were not supported as monophyletic with the exception
of C. sect. Acistegia, which includes only two species, C. hae-
matomma (D C.) B enth ., C. pedicellata Benth. (Fig. 2). Species
of Barneby’s C. sect. Calliandra appeared in four clades: (1)
in clade F, composed of species restricted to the Espinhaço
Mountain range in eastern Brazil; (2) in clade G that includes
species from the southern United States to Central America
(including C. houstoniana (Miller) Standley, the type species of
the genus) and species of C. sect. Acistegia; (3) in clade H com-
prising C. vaupesiana and C. tsugoides only, and (4) in clade K,
which includes only one species of C. sect. Cal liandra, C. vir-
gata, and this species was nested in the large C. sect. Andro-
callis (plus sect. Acroscias and Guinetia tehuantepecensis).
Clade I (PP 1.0; BS ML 1.0; BS MP 1.0) comprised species from
the United States to Mexico of Barneby’s C. sect. Androcallis.
Clade J (PP 0.99; BS ML 0.79; BS MP < 0.75) was a mixture of
four species of Barneby’s sect. Androcallis and two species of
sect. Microcallis (C. parviflora Benth., C. leptopoda Bent h.).
Clade K (PP 1.0; BS ML 0.85; BS MP < 0.75), which is widely
distributed from the southern United States to northern Argen-
tina, includes most representatives of Barneby’s C. sect. Andro-
callis together with Guinetia tehuantepecensis, C. brevicaulis
(sect. Acroscias) and C. virgata (sect. Calliandra).
Of the twelve series (of a total of fourteen) proposed by
Barneby (1998) included in this study, seven are monospecific
(C. ser. Biflorae, ser. Chilensis, ser. Hymenaeoides, ser. Lep-
topodae, ser. Longipedes, ser. Microcallis, ser. Virgatae), four
were shown to be non-monophyletic (C. ser. Ambivalente, ser.
Androcallis, ser. Calliandra, ser. Macrophyllae) and only ser
Tsugoideae was recovered as monophyletic.
Relationships of Calliandra s.str. to other groups of Ingeae
were not well resolved. A well-supported group of two species
from continental Africa (Calliandra gilbertii and C. redacta)
was recovered as sister to Calliandra s.str. (Fig. 2) with Co-
joba arborea as sister group of this clade, but always with low
Zapoteca_formosa
Samanea_saman
Macrosamanea_pubiramea
Zapoteca_lambertiana
Viguieranthus_ambongensis
Balizia_pedicellaris
Blanchetiodendron_blanchetii
Zapoteca_filipes
Hesperalbizia_occidentalis
Zygia_racemosa
Leucochloron_limae
Viguieranthus_subauriculatus
Cojoba_arborea
Archidendron_hirsutum
Pithecellobium_diversifolium
Viguieranthus_megalophyllus
Hydrochorea_corymbosa
Zapoteca_tetragona
Abarema_floribunda
Zapoteca_media
Enterolobium_timbouva
Thailentadopsis_tenuis
Acacia_spinescens
Thailentadopsis_nitida
Viguieranthus_kony
Viguieranthus_glaber
Inga_thibaudiana
Cedrelinga_cateniformis
Pseudosamanea_guachapele
Viguieranthus_densinervus
Abarema_piresii
Albizia_polycephala
Ebenopsis_ebano
Inga_edulis
Zapoteca_sousae
Zapoteca_alinae
Havardia_mexicana
Sphinga_acatlensis
0.75/-
0.99/0.97
1/-
0.85/0.90
0.92/0.93
0.82/-
1/1
1/0.97 0.97/0.81
0.94/0.91
B
C
A
“Pithecellobium
alliance”
“Abarema
alliance”
Viguieranthus
Zapoteca
Thailentadopsis
see next page, Fig. 2B
1/1
Fig. 2A–B.
Majority-rule (50%) consensus tree of 10,000 trees sampled at stationarity from the Bayesian analysis of the combined data (ITS + trnL/
trnL-F) of Calliandra and related genera. Thick lines indicate clades supported by posterior probabilities (PP) ≥ 0.90. Numbers on the branches
indicate bootstrap values (≥ 0.75) of the maximum li kelihood (ML) and of the maximum parsimony (MP) analyses, respectively. Color of names
of taxa indicate sectional assignation of species in Calliandra sensu Barneby (1998). The new infrageneric classification presented in this study
is represented by gray boxes. Letters on nodes refer to clades discussed in the text. Taxa in bold belong to the “Inga alliance” (sensu Barneby &
Grimes, 1996; Lewis & Rico-Arce, 2005). In the inset in Fig. 2B is the same tree depicted as a phylogram to show the branch lengths.
1207
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support. Most of the morphological characters used by Ben-
tham (1844) and Barneby (1998) to characterize infrageneric
groups of Calliandra were recovered as homoplastic (e.g., in-
florescence architecture, number of pairs of pinnae and number
of leaflets per pinna; Electr. Suppl.: Fig. S1).
Molecular divergence time estimates. — All estimated
parameters had sufficient effective sample size, in most cases
well above the minimum of 200. Age estimates for relevant
crown nodes (mean and 95% credibility intervals) are shown in
Table 3. The mean ages of stem and crown group of Calliandra
Calliandra_laxa
Calliandra_leptopoda
Calliandra_harrisii
Calliandra_goldmanii
Calliandra_virgata
Calliandra_vaupesiana
Calliandra_tumbeziana
Calliandra_guildingii
Calliandra_tsugoides
Calliandra_parvifolia
Calliandra_haematocephala
Calliandra_feioana
Calliandra_glomerulata
Calliandra_viscidula
Calliandra_sp. FS9972
Calliandra_brevipes
Calliandra_erubescens
Calliandra_bella
Calliandra_ulei
Calliandra_molinae
Calliandra_sp. FS9982
Calliandra_purdiei
Calliandra_humilis
Calliandra_aeschynomenoides
Calliandra_purpurea
Calliandra_sessilis
Calliandra_cumbucana
Calliandra_luetzelburgii
Calliandra_debilis
Calliandra_redacta
Calliandra_paterna
Calliandra_hirsuta
Calliandra_cruegeri
Calliandra_caeciliae
Calliandra_calycina
Calliandra_sp. FS10531
Calliandra_spinosa
Calliandra_laevis
Calliandra_dolichopoda
Calliandra_mollissima
Calliandra_fasciculata
Calliandra_lintea
Calliandra_belizensis
Calliandra_hirtiflora
Calliandra_tweedii
Calliandra_trinervia
Calliandra_chilensis
Calliandra_eriophylla
Calliandra_semisepulta
Calliandra_longipinna
Calliandra_magdalenae
Calliandra_rhodocephala
Calliandra_iligna
Calliandra_angustifolia
Calliandra_macrocalyx
Calliandra_longipes
Calliandra_riparia
Calliandra_rubescens
Calliandra_pittieri
Calliandra_hygrophila
Calliandra_nebulosa
Calliandra_surinamensis
Calliandra_gilbertii
Calliandra_houstoniana
Calliandra_depauperata
Calliandra_haematomma
Calliandra_silvicola
Calliandra_coriacea
Calliandra_bahiana
Calliandra_taxifolia
Calliandra_pedicellata
Calliandra_californica
Calliandra_lanata
Calliandra_renvoizeana
Calliandra_sincorana
Calliandra_dysantha
Calliandra_hintonii
Calliandra_blanchetii
Calliandra_coccinea
Calliandra_parviflora
Calliandra_mucugeana
Calliandra_tergemina
Calliandra_pilgerana
Calliandra_physocalyx
Calliandra_palmeri
Guinetia_tehuantepecensis
Calliandra_brenesii
Calliandra_crassipes
Calliandra_asplenioides
Calliandra_umbellifera
Calliandra_biflora
C
D
E
F
G
H
I
J
K
sect.
Microcallis
sect.
Androcallis
sect.
Septentrionales
sect. Tsugoideae
sect.
Calliandra
sect.
Monticola
Afrocalliandra
1/1
1/0.99 1/1
1/1
0.99 /1
0.96/0.93
0.99/
0.99
1/1
0.91/
0.93
0.79/- 0.82/
0.89
0.99/
0.92
0.80/0.80
1/1
0.98/0.96
0.85/-
0.98/
0.94
1/1
0.99/
0.99
1/0.91
1/0.98
0.94 /
0.98 0.92/
0.96
0.99/
0.99
Calliandra_brevicaulis
Sect. Calliandra
Sect. Acistegia
Sect. Acroscias
Sect. Androcallis
Sect. Microcallis
C
B
F
E
G
H
I
J
K
Calliandra
Afrocalliandra
Zapoteca
Viguieranthus
Thailentadopsis
“Abarema alliance”
“Pithecellobium alliance”
A
D
1/1
1/1
1/0.90
see previous
page, Fig. 2A
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• Phylogeny of Calliandra
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were estimated at 14.74 Ma (clade C) and 11.36 Ma (clade E),
respectively (Fig. 4). Crown ages of the major clades are pre-
sented in Table 3.
The topological differences found in the tree obtained in
the dating analysis with BEAST were: (1) clade G sister group
of clade F and (2) a clade composed of Cojoba, Thailentadopsis,
Viguieranthus and Zapoteca. These differences (in comparison
with the Bayesian analysis of MrBayes) are not supported and
probably reflect differences in the model used, since BEAST
estimates molecular rates for each branch with a more complex
model than MrBayes (probably at the expense of topological
precision) (Drummond & al., 2012).
Pollen morphology. —
Palynological studies carried out
on the two African species (Guinet, 1965; Thulin & al., 1981;
Souza, 2007; Souza & al., in prep.), two Asian species (Guinet,
1965; Souza, 2007; Souza & al., in prep.) and 66 American
species (Guinet, 1965; Niezgoda & al., 1983; Guinet & Hernán-
dez, 1989; Souza, 2007; Santos & Romão, 2008; Souza & al.,
in prep.), representing all sections and series recognized by
Barneby (1998), showed that calymmate and ellipsoid poly-
ads are an exclusive trait of the American taxa of Calliandra,
whereas, in contrast, the paleotropical species have acalymmate
polyads. Calliandra cynometroides (Fig. 5B) and C. umbrosa
(Fig. 5C), both Asian, have radially symmetrical, 16-celled
polyads, where as C. redacta and C. gilbertii (Fig. 5A), the two
African species, have bilateral, 7-celled polyads.
DISCUSSION
Most phylogenetic studies in Mimosoideae have revealed
a relatively low substitution rate in plastid markers (e.g., Lavin
& al., 2005) which resulted in a persistent lack of resolution
in many areas of the mimosoid phylogeny (Luckow & al,
2000, 2003; Lavin & al, 2005; Jobson & Luckow, 2007). One
Fig. 3.
Supernetwork obtained
from the majority-rule consen-
sus tree of the Bayesian analysis
illustrating the incongruence be-
tween ITS and trnL trees. Clades
are named according as in Fig. 2.
0.01
Other Ingeae
D
F
J
K
Calliandra sect
Androcallis
(in part)
+Guinetia
Table 3.
Molecular divergence time (crown age) estimates (for names
of nodes see Fig. 4).
Most recent common
ancestor of
Mean
[Ma]
Minimum
[Ma]
Maximum
[Ma]
Clade A (Ingeae + Acacieae) 20.98 17.18 24.54
Ingeae 18.76 16.27 21.29
Clade C 14.74 11.75 17.52
Clade D (Afrocalliandra) 7.94 3.44 11.87
Clade E (Calliandra s.str.) 11.36 8.90 13.42
Clade F (sect. Monticola) 2.88 1.65 3.78
Clade G (sect. Calliandra) 4.77 2.41 6.88
Clade H (sect. Tsugoideae) 4.34 1.62 6.67
Clade I (sect. Septentrionales) 3.47 1.47 5.30
Clade J (sect. Microcallis) 6.31 4.17 8.07
Clade K (sect. Androcallis) 7.21 5.56 8.51
Thailentadopsis 3.64 1.05 6.12
Viguieranthus 3.51 1.49 5.55
Zapoteca 5.75 3.42 7.73
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Fig. 4.
Maximum clade credibility
chronogram of Calliandra and
related genera. Node bars indicate
95% highest posterior density
date ranges (95% HPDs). Clades
are named as in Fig. 2. Diamonds
represent the calibration points.
0 Ma5101520
Calliandra_dysantha
Calliandra_laxa
Calliandra_houstoniana
Calliandra_semisepulta
Thailentadopsis_nitida
Balizia_pedicellaris
Zapoteca_media
Calliandra_aeschynomenoides
Calliandra_laevis
Sphinga_acatlensis
Calliandra_belizensis
Zapoteca_alinae
Macrosamanea_pubiramea
Calliandra_brevipes
Calliandra_hirsuta
Hydrochorea_corymbosa
Calliandra_coccinea
Calliandra_parviflora
Blanchetiodendron_blanchetii
Archidendron_hirsutum
Afrocalliandra_gilbertii
Calliandra_longipes
Calliandra_parvifolia
Guinetia_tehuantepecensis
Calliandra_hirtiflora
Inga_edulis
Calliandra_cumbucana
Samanea_saman
Zapoteca_lambertiana
Thailentadopsis_tenuis
Calliandra_chilensis
Calliandra_depauperata
Calliandra_purpurea
Calliandra_leptopoda
Calliandra_brenesii
Calliandra_physocalyx
Pseudosamanea_guachapele
Calliandra_paterna
Calliandra_taxifolia
Calliandra_rubescens
Ebenopsis_ebano
Calliandra_debilis
Calliandra_lanata
Calliandra_sp. FS9972
Calliandra_trinervia
Calliandra_calycina
Calliandra_coriacea
Calliandra_macrocalyx
Calliandra_renvoizeana
Calliandra_fasciculata
Calliandra_hygrophila
Viguieranthus_megalophyllus
Calliandra_cruegeri
Calliandra_sp. FS10531
Calliandra_palmeri
Viguieranthus_densinervus
Calliandra_dolichopoda
Enterolobium_timbouva
Viguieranthus_kony
Albizia_polycephala
Calliandra_californica
Calliandra_virgata
Calliandra_iligna
Calliandra_sp. FS9982
Calliandra_ulei
Calliandra_feioana
Cojoba_arborea
Calliandra_molinae
Calliandra_harrisii
Calliandra_blanchetii
Calliandra_purdiei
Havardia_mexicana
Calliandra_umbellifera
Abarema_floribunda
Calliandra_tweedii
Calliandra_erubescens
Zapoteca_formosa
Zapoteca_sousae
Calliandra_bahiana
Calliandra_lintea
Calliandra_guildingii
Calliandra_sessilis
Calliandra_spinosa
Calliandra_silvicola
Calliandra_goldmanii
Viguieranthus_subauriculatus
Calliandra_pittieri
Calliandra_surinamensis
Inga_thibaudiana
Calliandra_hintonii
Calliandra_angustifolia
Calliandra_magdalenae
Calliandra_brevicaulis
Calliandra_crassipes
Zapoteca_filipes
Abarema_piresii
Calliandra_tsugoides
Calliandra_haematocephala
Calliandra_nebulosa
Calliandra_caeciliae
Calliandra_rhodocephala
Viguieranthus_ambongensis
Calliandra_bella
Calliandra_haematomma
Calliandra_pilgeriana
Calliandra_viscidula
Calliandra_sincorana
Calliandra_longipinna
Calliandra_mollissima
Calliandra_riparia
Pithecellobium_diversifolium
Zapoteca_tetragona
Calliandra_luetzelburgii
Calliandra_pedicellata
Calliandra_eriophylla
Calliandra_mucugeana
Afrocalliandra_redacta
Cedrelinga_cateniformis
Calliandra_asplenioides
Calliandra_tumbeziana
Acacia_spinescens
Calliandra_humilis
Leucochloron_limae
Zygia_racemosa
Calliandra_tergemina
Calliandra_vaupesiana
Calliandra_glomerulata
Hesperalbizia_occidentalis
Viguieranthus_glaber
Calliandra_biflora
Pliocene Pleistocene
Miocene
Holocene
Oligocene
A
D
C
E
G
F
H
I
J
K
sect.
Androcallis
sect.
Microcallis
sect.
Septentrionales
sect. Tsugoideae
sect.
Monticola
sect.
Calliandra
Afrocalliandra
Zapoteca
Viguieranthus
Thailentadopsis
Ingeae
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exception is the trnD-trnT region that contained enough varia-
tion to uncover major clades in Mimosa (Simon & al., 2011).
The evolutionary rates of both the ITS and trnL-F regions
observed in our study are similar to those found in other Mi-
mosoideae (Murphy & al., 2003; Ariati & al., 2006; Brown
& al., 2008; Govindarajulu & al., 2011). However, potentially
non-functional pseudogene copies of ITS have been identified
in some mimosoid groups (Bailey & al., 2003), including Leu-
caena (Hughes & al., 2002) and Inga (Richardson & al., 2001).
ITS pseudogenes, unlike functional copies, are not subject to
functional constraints and, therefore, can have similar substitu-
tion rates in the 5.8S gene region and the ITS spacers (Bailey
Fig. 5.
SEM micrographs of
polyads.
A,
Afrocalliandra
gilbertii (Thulin & Hunde)
E.R. Souza & L.P. Queiroz
(Powys 493, K) with detail
showing polyad with only one
central grain (Tardelli 161, K);
B,
Calliandra cynometroides
Bedd. (Sasidharan 10003, K);
C,
C. umbrosa Benth. (Clarke
44932, K);
D,
Viguieranthus
umbiliscus Villiers (Capuro 796,
P);
E,
Zapoteca formosa (Kunth)
H.M. Hern. (Wood 8782, K);
F,
C. houstoniana (Mill.) Standl.
(Colín 16765, MEXU);
G,
C. debi-
lis Renvoize, basal grain showing
the appendix (Harley 18676,
HUEFS);
H,
C. parviflora (Hook.
& Arn.) Speg. (Wood 19934, K).
— Scale bars: A–F, H = 10 µm;
G = 20 µm.
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& al., 2003). We did not find evidence for pseudogenes in our
data because the 5.8S gene region did not contain indels and
had a much lower substitution rate than the two ITS regions
across the sampled taxa. Also, taxa represented by multiple
accessions did not reveal polymorphic sites in ITS sequences.
The topological conflicts between trees generated from
the ITS and trnL-F data probably arose from: (1) different
taxonomic sampling between the two datasets: Calliandra
belizensis, C. californica, C. chilensis, C. dolichopoda, C. erio-
phylla, C. hirsuta, C. humilis, C. palmeri, C. tsugoides are present
only in the nuclear dataset, whereas C. gardnerii, C. glyphoxy-
lon, C. juzepczukii, C. peninsularis, C. trinervia, and Thailen-
tadopsis tenuis were included only in the plastid dataset; (2)
lack of inclusion of the plastid spacer (trnL-F) in some taxa
such as C. brevicaulis, C. goldmanii, C. guildingii, C. hintoni
and C. houstoniana.
Relationships within tribe Ingeae. —
The “Inga alliance”
was not recovered as monophyletic in any analysis. This group
was proposed by Grimes (1995, 1999) and Barneby & Grimes
(1996) based on a morphological phylogenetic analysis and
characterized by persistent axillary reproductive meristems
(ramiflory). It is heterogeneous with respect to habit and habitat
since it includes arboreal genera typical of humid and riparian
forests (e.g., Archidendron, Cedrelinga, Cojoba, Inga, Macro-
samanea, Marmaroxylon, Zygia), as well as small trees, shrubs,
and subshrubs typical of STDFs (e.g., Calliandra, Guinetia,
Viguieranthus, Zapoteca). Relationships amongst these genera
were not well resolved in our study, except within the clade
comprising Inga, Macrosamanea and Zygia with Leucochlo-
ron (“Chloroleucon alliance”) nested within it, and the clade
containing Calliandra, with Guinetia nested within it, Co-
joba, Thailentadopsis, Viguieranthus and Zapoteca. In previ-
ous molecular analyses (Luckow & al., 2000, 2003; Brown
& al., 2008), the “Inga alliance” also was not supported as
monophyletic.
The “Abarema alliance” as circumscribed by Barneby
& Grimes (1996) and Lewis & Rico-Arce (2005) was re-
covered as monophyletic in all analyses. It includes genera
typical of humid forests that are differentiated mainly by fruit
type (Barneby & Grimes, 1996). Rico Arce (1999) consid-
ered Balizia as a synonym of Albizia, which was maintained
by Lewis & Rico Arce (2005). However, our study indicated
that Balizia is independent of Albizia and placed within the
Abarema alliance” as proposed by Barneby & Grimes (1996).
The “Pithecellobium alliance” comprises genera typical
of SDTFs: Havardia, Sphinga, Pithecellobium, Ebenopsis and
Painteria, distributed in Mexico, the Caribbean region and
surrounding areas (e.g., Honduras and Nicaragua in Central
America; Colombia and Venezuela in South America), with
only Pithecellobium occurring in eastern South America. Of
the genera belonging to this alliance, only Painteria was not
included in our analyses, and so far has not been included in
any other molecular study. The group is highly supported as
monophyletic in all analyses except the maximum parsimony
analysis and is diagnosed by new growth developing from
both standard vegetative branches and brachyblasts, the pres-
ence of separate vegetative and reproductive brachyblasts, and
spinescent stipules as morphological synapomorphies (Grimes,
1995; Barneby & Grimes, 1996).
Monophyly and generic relationships of Calliandra. —
The
phylogenetic position of the two African species of Calliandra
had not been evaluated until now. According to palynological
studies, the two species were deemed to be early diverging
lineages that probably represent a genus distinct from Callian-
dra (Thulin & al., 1981; Guinet & Hernandez, 1989). Barneby
(1998) subsequently circumscribed Calliandra to be restricted
to the New World. The two African species differ from Cal-
liandra s.str. by their acalymmate polyads (Fig. 5A) and the
presence of extrafloral nectaries. Our results strongly support
the two African species as a monophyletic group sister to an
American Calliandra s.str. clade, itself also strongly supported.
Based on the reciprocal monophyly of these sister clades, dif-
ferent taxonomic status could be ascribed to the African clade
without violating the principle of monophyly. We have cho-
sen to recognize the African clade as a new genus, sister to
Calliandra, based on the criterion of morphological diagnos-
ability. If we had chosen to include the species of the African
clade in a more broadly circumscribed Calliandra, this would
have rendered Calliandra to lack any clear-cut synapomor-
phy and virtually lacking diagnostic characters with respect
to Zapoteca, Viguieranthus and Thailentadopsis. Recognizing
the two African species as a distinct genus is supported by their
different pollen characters (8-celled polyads with a calym-
mate exine in Calliandra vs. 7-celled acalymmate polyads in
Afrocalliandra), the absence of extrafloral nectaries (vs. absent
or present in Afrocalliandra), and spines or thorns which are
absent in Calliandra, in addition to the continental disjunction.
The Asian C. cynometroides and C. umbrosa (Fig. 5B, C,
respectively) also have polyad morphologies different from
those found in Calliandra s.str. and might be better placed in a
new genus, but such an action would be premature because these
two species have not yet been included in any molecular study.
Higher-level relationships of the Calliandra s.str.–Afrocal-
liandra clade with other genera formerly included in Calliandra
s.l., as well as with other genera of Ingeae, were unresolved, al-
though each genus (Zapoteca, Viguieranthus, Thailentadopsis)
is supported as monophyletic both in the ITS and the combined
ITS + trnL-F analyses and each has a pollen morphology dis-
tinct from Calliandra (Fig. 5). These results add support to the
current generic circumscriptions in the Calliandra s.l. group,
that is, keeping Calliandra s.str. (with the inclusion of Guinetia)
as distinct from Zapoteca, Viguieranthus and Thailentadopsis
as well as supporting each of these as distinct genera, as pro-
posed by several authors (Hernández, 1986; Barneby, 1998;
Villiers, 2002; Lewis & Schrire, 2003).
The transfer of Guinetia to Calliandra s.str. renders the
latter monophyletic with robust support in all analyses (Fig. 2).
Guinetia is placed in the clade of Neotropical Calliandra spe-
cies along with the species of C. sect. Androcallis (Fig. 2,
clade K). These species and Guinetia have in common the axil-
lary inflorescences arising from brachyblasts, and the majority
of them have heteromorphic inflorescences, although this char-
acter is not mentioned in the original description of Guinetia
(Rico Arce & al., 1999). This clade (Calliandra s.str. + Guinetia)
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is diagnosed by the following morphological synapomorphies:
absence of a petiolar nectary (Electr. Suppl.: Fig. S1D) and ca-
lymmate polyads composed of eight pollen grains (Fig. 5F–H;
Electr. Suppl.: Fig. S1K).
The clade (Zapoteca (Afrocalliandra + [Calliandra s.str
+ Guinetia])) is characterized by fruits elastically dehiscent
from the apex (with a reversal in Guinetia that does not possess
this kind of dehiscence but instead opens along one margin).
Zapoteca was regarded as the sister group of Calliandra s.str.
in the analyses of Grimes (1995), Barneby & Grimes (1996),
Luckow & al. (2000) and the ETS analysis of Brown & al.
(2008), although there was low support for this relationship
in our analyses.
In the molecular analyses of Luckow & al. (2003), Cedrel-
inga was supported as the probable sister group to Callian-
dra s.str, but in our study this position was not confirmed and
Cedrelinga was placed as sister to Pseudosamanea guachapele.
Cedrelinga was not included in the analyses of Brown & al.
(2008).
Habitat evolut ion in Calliandra. —
Divergence time analy-
ses indicated that Calliandra s.str. and Afrocalliandra split
from each other at about 14.74 Ma (mean age; clade C) in the
Miocene (Fig. 4; Table 3). Modern Calliandra s.str. diversified
from 11.36 Ma (clade E) forming two major groups: (1) The
radiation of the first group seems to have started at about 10
Ma in the Miocene, and contains the majority of the species
included in this study. These species are resolved in four dis-
tinct clades: clade H, from 4.34 Ma, which contains only two
species distributed in the Guianas, Venezuela, the Colombian
Amazon and the northern state of Amazonas, Brazil; clade I,
from 3.47 Ma, which includes species that grow in the desert
and semi-desert regions of the Mexican highlands, extending to
the southern United States; clade J, 6.31 Ma, which comprises
species restricted to the arid and semi-arid regions of north-
eastern Brazil, Chile, southwestern United States (Arizona) to
Mexico and extra-Amazonian Brazil, Paraguay and Bolivia,
and clade K, from 7.21 Ma, which includes species widely dis-
tributed from the southern United States to Argentina; (2) The
second group may have split about 8 Ma. These species are
resolved into two distinct clades: clade G, which diversified
from 4.77 Ma, includes species distributed from Mexico to
Central America; clade F, which diversified within the past 2.88
Ma, in the Pleistocene. This clade comprises species restricted
to the Espinhaço mountain range in Brazil.
Calliandra is more diverse in STDFs, savannas and cam-
pos rupestres with a few species in wet forests and subtropical
grasslands (Electr. Suppl.: Fig. S1B). Our results indicate that the
SDTF is the most probable ancestral habitat of the genus and the
stage of the major diversification events. As in other dry forest
specialists (e.g., Coursetia, Lavin & al., 2001; Queiroz & Lavin,
2011; Indigofera, Schrire & al., 2009; Mimosa, Simon & al.,
2011), the SDTF clades of Calliandra show strong geographical
and phylogenetic coherence, as exemplified by the dry forest
clades G, I and some subclades of clade K distributed from
Mexico to northwestern South America, and the C. aeschynom-
enoides–C. parviflora clade of clade J, distributed only in the
Caatinga vegetation of northeastern Brazil. This suggests niche
conservatism and limited dispersal in SDTF lineages (Lavin,
2006, Queiroz & Lavin, 2011).
Habitat shifts to savanna vegetation have occurred several
times. Most of these transitions occurred independently to the
Cerrado vegetation of central Brazil corroborating the find-
ing of Simon & al. (2009) that most of the Cerrado flora had a
recent origin and evolved from different surrounding biomes.
In sharp contrast with this Cerrado diversification pattern,
the campos rupestres, another area also dominated by simi-
lar fire-prone savanna-like vegetation, harbours a spectacular
radiation of Calliandra, comprising 46 of the 142 species of
the genus. These 46 species are concentrated in the northern
part of the Chapada Diamantina mountain range, and 36 of
them are narrowly restricted to this region, paralleling the
rapid species diversification also observed in other montane
regions for other legume genera, such as the Andean clade of
Lupinus L. (Hughes & Eastwood, 2006).
One important aspect of this endemism in the Chapada
Diamantina is that it is not distributed uniformly among the
infrageneric groups of Calliandra (Souza, 2001). Of the 36 spe
-
cies of Calliandra restricted to the Chapada, one belongs to the
Androcallis clade (C. pilgerana Harms) and 35 to the Monticola
clade. In addition, we observed no habitat shifts between Cer-
rado and campos rupestres clades of Calliandra despite striking
environmental similarities and the geographical proximity of
these two vegetation types. This pattern suggests that there
is strong dispersal barrier between the Chapada Diamantina
region and the remaining areas of campos rupestres of the Es-
pinhaço range, as well as to other areas of Cerrado in central
Brazil. This high level of taxonomically unbalanced endemism
may indicate that much of the f loristic diversity observed in the
campos rupestres vegetation may be the result of a relatively re-
cent and rapid adaptive radiation, as suggested by Harley (1988)
for Eriope Humb. & Bonpl. ex Benth. (Labiatae). This hypoth-
esis predicts that relatively isolated areas should have floras that
are composed of similar taxa, but with distinct local patterns of
diversity (high beta diversity). This is exactly the pattern seen
in the distribution of Calliandra, which is concentrated in the
southern region of the Chapada Diamantina. This recent and
rapid radiation can be observed in an analysis of the diversity
of the two main blocks of the Espinhaço mountain range: the
Espinhaço Mountains (in Minas Gerais State) and the Chapada
Diamantina (in Bahia). While some groups show an explosive
diversification in Minas Gerais, with relatively few species in
Bahia (e.g. Leiothrix Ruhland (Eriocaulaceae), Pseudotrimezia
R.C. Foster (Irid aceae), Senna Mill. (Leguminosae), Barbace-
nioideae (Velloziaceae); Giulietti & Pirani, 1988 and Minaria
T.U.P. Konno & Rapini (Apocynaceae); Rapini & al., 2002,
2007; Ribeiro & al., 2012), other groups show the exact oppo-
site, with their greatest diversity in the Chapada Diamantina
(e.g. Calliandra, Marcetia DC. (Melastomataceae); Giulietti
& al., 1996; Santos, 2009).
Apart from the proposed taxonomic changes presented
below, our results also demonstrate the importance of delimit-
ing conservation areas within the main centers of diversity of
Calliandra where the largest number of species and the greatest
number of endemics occur. On the one hand, the significant
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diversity and endemism encountered in a number of areas rep-
resents a high level of beta diversity, while on the other hand it
raises the question of the fragility of these ecosystems and the
urgent need for their conservation, for example, in the Chapada
Diamantina where the endemic species are narrowly restricted,
often with populations composed of very few individuals.
TAXONOMIC TREATMENT
Based on the analyses presented here, we propose a new
circumscription of Calliandra with the inclusion of the Mexi-
can genus Guinetia. We also propose a new infrageneric clas-
sification for Calliandra based on the well-supported clades
identified in our study, describe two new sections and give
sectional status to C. ser. Tsugoideae. Optimization of mor-
phological traits defines Calliandra by three uniquely derived
apomorphic characters: the 8-celled calymmate polyads, with
an entire exine covering all grains (Fig. 5F–H; Electr. Suppl.:
Fig. S1K), and the loss of foliar nectaries. The two African
species excluded from Calliandra by Barneby (1998) are here
assigned to a new genus. Besides its wide geographical disjunc-
tion, this new genus is defined by the 7-celled acalymmate
polyads (Fig. 5A; Electr. Suppl.: Fig. S1K) and the presence
of thorns derived from axillary branches or modified stipules.
Afrocalliandra E.R. Souza & L.P. Queiroz, gen. nov. – Type:
Afrocalliandra redacta (J.H. Ross) E.R. Souza & L.P.
Queiroz.
Similar to Calliandra in having elastically dehiscent pods
with thick margins and ellipsoid polyads, but differing by the
presence of thorns derived from axillary branches or modified
stipules, acalymmate polyads which are 7-celled with each cell
provided with internal proximal pores.
Densely branched subshrubs, branches with brachy-
blasts from which leaves and inflorescences emerge, axillary
branches modified (or not) into thorns. Stipules herbaceous or
modified into thorns. Leaves bipinnate with one pair of pinnae,
extrafloral nectaries present or absent on the petiole. Inflo-
rescences lateral, pedunculate, few-flowered heads. Flowers
homomorphic, small, 8–15 mm long, sessile or with a short
pedicel, filaments whitish cream, fused at the base into an
included (within the corolla) or slightly exserted tube, pollen
grains in 7-celled acalymmate polyads. Pods erect, oblanceo-
late, compressed, margins thickened, elastically dehiscent from
the apex.
Two species in tropical Africa.
Afrocalliandra gilbertii (Thulin & Asfaw) E.R. Souza & L.P.
Queiroz, comb. nov. Calliandra gilbertii Thulin &
Asfaw in Nordic J. Bot. 1: 27. 1981 – Holotype: KENYA.
Mandera District, War Gedud, 1 May 1978, M.G. Gilbert
& M. Thulin 1288 (UPS; isotypes: BR!, C, EA, FT, K!,
MO, P!, PRE!, WAG).
Afrocalliandra redacta (J.H. Ross) E.R. Souza & L.P. Queiroz,
comb. nov. Acacia redacta J.H. Ross in Bothalia 11: 231.
1974 ≡ Calliandra redacta (J.H. Ross) Thulin & Asfaw in
Nordic J. Bot. 1: 29. 1981 – Holotype: SOUTH AFRICA.
Cape Province, 22.4 km N of Sunkfontein on the way to
Jenkinskop, 15 Nov. 1971, M.J.A. Werger 1518 (PRE!; iso -
type: K!).
Calliandra Benth. in J. Bot. (Hooker) 2(11): 138. 1840, nom.
cons. – Type: C. houstoniana (Mill.) Standl. [≡ Mimosa
houstoniana Mill. ≡ C. houstonii Benth. (“houstoni”), nom.
superf l. et illeg. ≡ M. houstonii L’He r . ( houstoni”) nom.
superf l. et illeg.], typ. cons. (see Hernández & Nicolson in
Taxon 35: 747–748. 1986).
= ? Anneslia Salisb., Parad. Lond.: ad t. 64. 1807, nom. rej.,
non Anneslea Wall., Pl. Asiat. Rar. 1: 5. 1829, nom. cons. –
Type: A. falcifolia Salisb., nom. superfl. et illeg. [≡ Gledit-
sia inermis L. ≡ Calliandra inermis (L.) Dr uce].
= Clelia Casar., Nov. Stirp. Bras.: 83. 1845 – Type: C. ornata
Casar.
= Codonandra H. Karst., Fl. Columb. 2: 43. 1863 – Type:
Codonandra purpurea H. Karst. ≡ Calliandra codonandra
Benth.
Shrubs, treelets or subshrubs, branches with or without
lateral brachyblasts. Stipules herbaceous, rarely modified into
thorns. Leaves bipinnate with one to many pairs of pinnae,
extrafloral nectaries absent. Inflorescences pedunculate or
sessile obconical heads, lateral on brachyblasts or terminal in
pseudoracemes. Flowers homomorphic or heteromorphic, ses-
sile or with a short pedicel, filaments white, red or bicolored,
rarely yellow, fused at the base into an included (within the
corolla) to exserted tube, pollen grains in 8-celled calymmate
polyads. Pods erect, oblanceolate, compressed, margins thick-
ened, elastically dehiscent from the apex.
142 species (three undescribed) from America.
Anneslia and Calliandra were treated as homotypic syn-
onyms (e.g., Barneby, 1998), based on C. houstoniana. How-
ever, Salisbury (1807) cited Gleditsia inermis L. as a synonym
of Anneslia falcifolia Salisb., which makes it a superfluous
and illegitimate name. The basis for the name Gleditsia iner-
mis L. is a Plukenet illustration of a single leaf, the identi-
fication of which is uncertain but that is possibly a species
of Acacia (Jarvis, 2007). Thus, Calliandra and Anneslia are
heterotypic and it is not sure that they should be synonyms.
Calliandra sect. Calliandra
= Calliandra ser. Comosae Barneby in Mem. New York Bot.
Gard. 74(3): 196. 1998 – Type: C. comosa (Sw.) Benth .
= Calliandra sect. Acistegia Barneby in Mem. New York Bot.
Gard. 74(3): 139. 1998 – Type: C. haematomma (DC.)
Benth.
Shrubs or subshrubs, armed or not; heads grouped in elon-
gate, exserted, terminal pseudoracemes or a panicle of pseu-
doracemes or in axillary fascicles. Mexico, Guatemala, Cuba,
Bahamas, Haiti, Jamaica, Porto Rico and Dominican Republic.
1. C. comosa (Sw.) Benth.
2. C. houstoniana (Mill.) Standl.
3. C. haematomma (DC.) Bent h.
4. C. juzepczukii Standl.
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5. C. palmeri S. Watson
6. C. paniculata C.D. Adams
7. C. pedicellata Benth.
8. C. physocalyx H.M. Hern. & M. Sousa (Fig. 1B)
9. C. quetzal (Donn. Sm.) Donn. Sm.
10. C. wendlandii Benth.
Calliandra sect. Septentrionales E.R. Souza & L.P. Queiroz,
sect. nov. – Type: C. californica Benth., Bot. Voy. Sulphur:
14, t. 11. 1844.
= Calliandra ser. Biflorae Barneby in Mem. New York Bot.
Gard. 74(3): 98. 1998 – Type: C. biflora Tharp.
Shrubs or densely branched subshrubs; heads grouped in
axillary fascicles. United States to Mexico.
11. C. biflora Tharp
12. C. californica Benth.
13. C. cualensis H.M. Hern.
14. C. dolichopoda H.M. Hern. (Fig. 1A)
15. C. eriophylla Benth.
16. C. hirsuta Benth.
Calliandra sect. Androcallis Barneby in Mem. New York Bot.
Gard. 74(3): 21. 1998 – Type: C. laxa (Willd.) Benth.
= Calliandra ser. Macrophyllae (Benth.) Barneby in Mem.
New York Bot. Gard. 74(3): 111. 1998 – Type: C. trinervia
Benth.
= Calliandra ser. Pauciflorae Barneby in Mem. New York Bot.
Gard. 74(3): 101. 1998 – Type: C. pauciflora (A. R ich.)
Griseb.
= Calliandra ser. Ambivalentes Barneby in Mem. New York
Bot. Gard. 74(3): 103. 1998 – Type: C. guildingii Benth.
= Calliandra ser. Hymenaeodeae Barneby in Mem. New York
Bot. Gard. 74(3): 134. 1998 – Type: C. hymenaeodes ( Pers.)
Benth.
= Calliandra ser. Longipedes Barneby in Mem. New York Bot.
Gard. 74(3): 137. 1998 – Type: C. longipes Benth.
= Calliandra ser. Virgatae Barneby in Mem. New York Bot.
Gard. 74(3): 189. 1998 – Type: C. virgata Benth.
= Calliandra sect. Acroscias Barneby in Mem. New York Bot.
Gard. 74(3): 146. 1998 – Type: C. brevicaulis Micheli.
= Guinetia L. Rico & M. Sousa in Kew Bull. 54: 977. 1999,
syn. nov. – Type: G. tehuantepecensis L. Rico & M. Sousa.
Shrubs, treelets or subshrubs, sometimes rhizomatous;
inflorescences lateral on brachyblasts or in terminal umbels
(C. brevicaulis), the units never assembled into a terminal efo-
liate pseudoraceme. Distribution almost the same as for the
genus, United States to Uruguay.
17. C. angustifolia Spruce ex Benth.
18. C. antioquiae Barneby
19. C. belizensis (Britton & Rose) Standl.
20. C. bella Benth.
21. C. bijuga Rose
22. C. blanchetii Benth.
23. C. bombycina Spruce ex Benth.
24. C. brenesii Standl.
25. C. brevicaulis Micheli
26. C. brevipes Benth.
27. C. caeciliae Harms
28. C. carcerea Standl. & Steyerm.
29. C. carrascana Barneby
30. C. chulumania Barneby
31. C. colimae Barneby
32. C. conferta Benth.
33. C. coriacea (Humb. & Bonpl. ex Willd.) Benth.
34. C. cruegeri Griseb.
35. C. duckei Barneby
36. C. dysantha Benth. (Fig. 1C)
37. C. enervis (Britton) Urb.
38. C. erythrocephala H.M. Hern. & M. Sousa
39. C. falcata Benth.
40. C. fernandesii Barneby
41. C. foliolosa Benth.
42. C. gardneri Benth.
43. C. glaziovii Taub.
44. C. glomerulata H. Karst.
45. C. glyphoxylon Spruce ex Benth.
46. C. goldmanii Rose ex Barneby
47. C. guildingii Benth.
48. C. haematocephala Hassk.
49. C. harrisii (Lindl.) Benth.
50. C. hintonii Barneby
51. C. hymenaeodes (Pers.) Benth.
52. C. imperialis Barneby
53. C. jariensis Barneby
54. C. laevis Rose
55. C. laxa (Willd.) Barneby
56. C. longipes Benth.
57. C. macqueenii Barneby
58. C. macrocalyx Harms
59. C. magdalenae ( DC.) Bent h.
60. C. medellinensis Britton & Rose ex Britton & Killip
61. C. molinae Standl.
62. C. mollissima (Humb. & Bonpl. ex Willd.) Benth.
63. C. parvifolia (Hook. & Arn.) Speg.
64. C. pauciflora (A. Rich.) Griseb.
65. C. peninsularis Rose
66. C. pilgerana Harms
67. C. pittieri Standl.
68. C. pityophila Barneby
69. C. purdiei Benth.
70. C. purpurea (L.) B enth.
71. C. rhodocephala Donn. Sm.
72. C. riparia Pittier
73. C. rubescens (Martens & Galeotti) Standl.
74. C. samik Barneby
75. C. sesquipedalis McVaug h
76. C. sessilis Benth. (Fig. 1D)
77. C. silvicola Taub.
78. C. spinosa Ducke
79. C. squarrosa Benth.
80. C. staminea (Thunb.) Barneby
81. C. subspicata Benth.
82. C. surinamensis Benth.
83. C. taxifolia (Kunth) Benth.
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84. Calliandra tehuantepecensis (L. Rico & M. Sousa) E.R.
Souza & L.P. Queiroz, comb. nov. Guinetia tehuan-
tepecensis L. Rico & M. Sousa in Kew Bull. 54: 977.
1999 – Holotype: MEXICO. Oaxaca, 5 km W of Salina
Cruz, M. Sousa & al. 9117 (MEXU!; isotype K!).
85. C. tergemina (L.) Bent h.
86. C. tolimensis Tau b.
87. C. trinervia Benth.
88. C. tumbeziana J.F. M a c b r
89. C. tweedii Benth.
90. C. ulei Harms
91. C. umbellifera Benth.
92. C. virgata Benth.
Calliandra sect. Microcallis Barneby in Mem. New York Bot.
Gard. 74(3): 197. 1998 – Type: C. parviflora Benth.
= Calliandra ser. Leptopodae Barneby in Mem. New York Bot.
Gard. 74(3): 199. 1998 – Type: C. leptopoda Benth.
= Calliandra ser. Chilensis Barneby in Mem. New York Bot.
Gard. 74(3): 100. 1998 – Type: C. chilensis Benth.
Scandent to erect shrubs or subshrubs up to 2 m in height;
phyllotaxy distichous (or exceptionally spiral in C. chilensis);
small flowers in obconical heads or umbels terminal or in
brachyblasts; perianth 3–7 mm; androecium small (from 7
to 23 mm in C. aeschynomenoides). The section comprises
a small number of species restricted to the arid regions of
northeastern Brazil: C. aeschynomenoides, C. depauperata
and C. leptopoda; Chile: C. chilensis, northwestern United
States (Arizona) to Mexico: C. humilis, and one widely dis-
tributed species in extra-Amazonian Brazil, Paraguay and
Bolivia: C. parviflora.
93. C. aeschynomenoides Benth. (Fig. 1O)
94. C. chilensis Benth.
95. C. depauperata Benth. (Fig. 1M)
96. C. humilis Benth.
97. C. leptopoda Benth. (Fig. 1N)
98. C. parviflora Benth.
Calliandra sect. Monticola E.R. Souza & L.P. Queiroz, sect.
nov. Ty pe: C. calycina Benth.
Treelets to densely branched shrubs or rhizomatous sub-
shrubs; inflorescences of terminal pseudoracemes, never axil
-
lary, mostly inserted amongst the foliage; brachyblasts absent.
Distributed in the Espinhaço mountain range (Bahia and Minas
Gerais, Brazil), in mountainous regions, especially rocky fields
(campos rupestres).
99. C. asplenioides (Nees) Renvoize
100. C. bahiana Renvoize (Fig. 1G)
101. C. calycina Benth. (Fig. 1K)
102. C. coccinea Renvoize (Fig. 1H)
103. C. concinna Barneby
104. C. crassipes Benth.
105. C. cumbucana Renvoize
106. C. debilis Renvoize
107. C. elegans Renvoize
108. C. erubescens Renvoize
109. C. fasciculata Benth.
110. C. feioana Renvoize
111. C. fuscipila Harms
112. C. ganevii Barneby
113. C. geraisensis E.R. Souza & L.P. Queiroz
114. C. germana Barneby
115. C. hirsuticaulis Harms
116. C. hirtiflora Benth.
117. C. hygrophila Mackinder & G.P. Lewis
118. C. iligna Barneby
119. C. imbricata E.R. Souza & L.P. Queiroz
120. C. involuta Mackinder & G.P. Lewis
121. C. lanata Benth. (Fig. 1F)
122. C. linearis Benth.
123. C. lintea Barneby
124. C. longipinna Benth. (Fig. 1L)
125. C. luetzelburgii Harms
126. C. mucugeana Renvoize
127. C. nebulosa Barneby
128. C. paganuccii E.R. Souza
129. C. paterna Barneby
130. C. renvoizeana Barneby
131. C. santosiana Glaz. ex Barneby
132. C. semisepulta Barneby (Fig. 1I)
133. C. sincorana Harms
134. C. stelligera Barneby (Fig. 1J)
135. C. viscidula Benth.
Calliandra sect. Tsugoideae (Bar neby) E.R. Souza & L.P.
Queiroz, stat . nov.C. ser. Tsugoideae Barneby in Mem.
New York Bot. Gard. 74(3): 190. 1998 – Type: C. tsugoides
R.S. Cowan.
Treelets or shrubs, similar to C. sect. Calliandra in having
terminal (never axillary) pseudoracemose inf lorescences (these
sometimes only shortly exserted from the foliage), but distin-
guished from other species of the genus by the parallel primary
venation of the leaflets; brachyblasts absent. Guayana Highland
and sand savannas in the Guianas, Venezuela, the Colombian
Amazon and the northern state of Amazonas, Brazil.
136. C. pakaraimensis R.S. Cowan
137. C. rigida Benth.
138. C. tsugoides R.S. Cowan
139. C. vaupesiana R.S. Cowan
ACKNOWLEDGEMENTS
We thank all the people who provided plant material for this
study, especially the directors and curators of the following herbaria
who loaned specimens and gave permission to take tissue samples:
BM, BR, HUEFS, INPA, MEXU, K, P and W; the Kew Latin Ameri-
can Research Fellowship (KLARF) Programme that facilitated the
visit of ERS to European herbaria and the Jodrell Laboratory of the
Royal Botanic Gardens, Kew; Laszlo Csiba for assistance at Kew;
Adelina Vitória F. Lima, Bárbara M. Mota, Priscilla G.C. de Almeida,
Adonilson A. de Menezes Neto, Evandro Ancelmo dos Santos for
assistance in LAMOL; Ricardo Vilas-Bôas helped with figures and
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Souza, E.R. de 2001. Aspectos taxonômicos e biogeográficos do gênero
Calliandra Benth. (Leguminosae—Mimosoideae) na Chapada
Diamantina, Bahia, Brasil. Dissertation, Universidade Estadual
de Feira de Santana, Brazil.
Souza, E.R. de 2007. Estudos filogenéticos na tribo Ingeae (Legumi-
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Appendix 1.
Species names and GenBank accession numbers of DNA sequences used in this study. Voucher data is given for accessions for which DNA
sequences were newly obtained, using the following format: Taxon name, country, largest political subdivision, collector and colletor number, herbarium
acronym, ITS, trnL-trnF GenBank accession numbers. –, missing data; *, newly generated sequences.
Abarema floribunda (Benth.) Barneby & J.W. Grimes, Brazil, Bahia, L.P. de Queiroz 13930 (HUEFS), JX870654*, JX870786*; Abarema piresii Barneby &
J.W. Grimes, Brazil, Amazonas, P.A.C.L. Assunção 411 (INPA), JX870655*, –; Abarema piresii Barneby & J.W. Grimes, Brazil, Amazonas, L.P. de Queiroz
13911 (H UEFS), –, JX870787*; Acacia spinescens Benth., AF360700, AF19706; Afrocalliandra gilbertii (Thulin &Asfaw) E.R. Souza & L.P. Queiroz , Kenya,
Mandera, M. Tardelli 67 (K), JX870690*, –; Afrocalliandra redacta (J.H. Ross) E.R. Souza & L .P. Queiroz, Afr ica, Cape Province, Oliver 338 (K), JX870732*,
JX870853*; Albizia polycephala (Kunth) Killip, Brazil, Bahia, R.M. Harley 54554 (K), JX870656*, –; Albizia polycephala (Kunth) Killip, Brazil, Bahia,
D. Cardoso 253 (HUEFS), –, JX870788*; Archidendron hirsutum I.C. Nielsen, –, AF365042.1; Balizia pedicellaris (DC.) Barneby & J.W. Grimes, Brazil,
Bahia, E.R. de Souza 358 (HUEFS), JX870657*, JX870799*; Blanchetiodendron blanchetii (Benth.) Barneby & J.W. Grimes, Brazil, Bahia, L.P. de Queiroz
7085 (HUEFS), JX870658*, JX870790*; Calliandra aeschynomenoides Benth., Brazil, Ba hia, E.R. de Souza 390 (HU EFS), JX870659*, JX870790*; Callian-
dra angustifolia Spruce ex. Benth., Bolivia, Cochabamba, J. R. I. Wood 16132 (K), JX870660*, JX870792*; Calliandra asplenioides (Nees) Renvoize, Brazil,
Bahia, E .R. de Souza 601 (H UEFS), JX870661*, JX870793*; Calliandra bahiana Renvoize, Brazi l, Bahia, E.R. de Souza 562 (HUEFS), JX870664*, JX870796*;
Calliandra bahiana Renvoize, Brazil, Bahia, L .P. de Queiro z 14550 (HU EFS), JX870662*, JX870795*; Calliandra bahiana Re nvoize, Bra zil, Bahia, A. Rapini
1047 (HUEFS), JX870663*, JX870794*; Calliandra belizensis (Britton & Rose) Standl., Honduras, Belize, C.L. Lundell 148 (K), JX870665*, –; Calliandra
bella (Spreng.) Benth., Brazil, Bahia, M.L.C. Neves 16 (HUEFS), JX870666*, JX870797*; Calliandra biflora Tharp, Mexico, J.M. Aguilar P. 1111 (MEXU),
JX870667*, JX870798*; Calliandra blanchetii Benth., Br azil, Bahia, E .R. de Souza 813 (HUEFS), JX870668*, JX870799*; Calliandra brenesii Standl., Costa
Rica, Guanacaste, D.J. Macqueen 122 (K), –, JX870800*; Calliandra brenesii Standl., Costa Rica, Alajuelo, A. Estrada 2394 (K), JX870669*, –; Calliandra
brevicaulis M. Micheli, S. Caceres 362 (K), JX870670*, JX870801*; Calliandra brevipes Benth., Brazil, Bahia, L.P. de Queiroz 12630 (HUEFS), JX870671*,
JX870802*; Calliandra caeciliae Harms, Mexico, T.S. Cochrane 13160 (MEXU), JX870674*, JX870803*; Calliandra californica Benth., Mexico, Baja cali-
fornia, M.E. Jones 22440 (MEXU), JX870672*, –; Calliandra calycina Benth., Brazil, Bahia, E.R. de Souza 333 (HUEFS), JX870673*, JX870804*; Callian-
dra chilensis Benth., Chile, Huasco, M. Acosta BB 018 (K), JX870675*, –; Calliandra coccinea Renvoize, Brazil, Bahia , A. Rapini 1046 (HUEFS), JX870676*,
JX870805*; Calliandra coriacea (Humb. & Bonpl. ex Willd.) Benth., Panama, D.J. Macqueen 623 (K), JX870677*, JX870806*; Calliandra crassipes Benth.,
Brazil, Bahia, E.R. de Souza 378 (HUEFS), JX870678*, JX870807*; Calliandra cruegeri Griseb., Trindad, W. Johnson 927 (K), JX870679*, JX870808*;
Calliandra cumbucana Renvoize, Brazil, Bahia, E.R. de Souza 361 (HUEFS), JX870680*, JX870809*; Calliandra debilis Renvoize, Brazil, Bahia, L.P. de
Queiroz 13734 (HUEFS), JX870681*, JX870810*; Calliandra depauperata Benth., Brazil, Bahia, E.R. de Souza 412 (HUEFS), JX870682*, JX870811*;
Calliandra dolichopoda H.M. Hern., Mexico, Guerrero, R.T. Colín 16771 (MEXU), JX870683*, –; Calliandra dysantha Benth., Brazil, Bahia, E.R. de Souza
344 (HUEFS), JX870684*, JX870813*; Calliandra eriophylla Benth., Mexico, R.T. Colín 14773 (MEXU), JX870685*, –; Calliandra erubescens Renvoize,
Brazil, Bahia, E.R. de Souza 338 (HUEFS), JX870686*, JX870812*; Calliandra fasciculata Benth., Brazil, Minas Gerais, E.R. de Souza 346 (HUEFS),
JX870687*, JX870814*; Calliandra feioana Renvoize, Brazil, Bahia, E.R. de Souza 637 (HUEFS), JX870688*, –; Calliandra gardneri Benth., Brazil, Goiás,
G. Hatschbach 60415 (HUEFS), –, JX870816*; Calliandra glomerulata H. Karst., Panama, Coclé, M.N. Stapf 368 (HUEFS), JX870691*, JX870817*;
Souza, E.R. de & Queiroz, L.P. 2004. Duas novas espécies de Callian-
dra Benth. (Legumi nosae - Mimosoideae) da Chapada Diamantina,
Bahia, Brasil. Revista Brasil. Bot. 27: 615 –619.
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in continental Africa. Nordic J. Bot. 1: 27–34.
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Villiers, J.F. 2002. Viguieranthus Villiers. Pp. 271–285 in: Du Puy, D.J.,
Labat, J.-N., Rabevohitra, R., Villiers, J.-F., Bosser, J. & Moat, J.
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1219Version of Record (identical to print version).
Calliandra glyphoxylon Spruce ex Benth., Ecuador, Chimborazo, W.H. Camp 3177 (K), –, JX870819*; Calliandra goldmanii Rose ex Barneby, Mexico,
Chiapas, C.E. Hughes 1493 (K), JX870692*, JX870818*; Calliandra guildingii Benth., Trindad, Northen Hills, D. Hollis M48 (K), JX870693*, JX870820*;
Calliandra haematocephala Hassk., Bolivia, Santa Cr uz, D. Soto 1235 (USZ), JX870694*, J X870 821*; Calliandra haematomma Benth., Domin ican Republic,
M. Fuertes 1927, P, JX870695*, JX870822*; Calliandra harrisii (Lindl.) Benth., Brazil, Bahia, J.R.I. Wood 17334 (K), JX870696*, JX870823*; Calliandra
hintoni i Barneby, Mexico, Temascaltepec, G.B. Hinton 4099 (K), JX870697*, JX870824*; Calliandra hirsuta Benth., Mexico, Guerrero, A. Salinas T. 8203
(MEXU), JX870698*, –; Calliandra hirtiflora Benth., Brazil, Bahia, E.R. de Souza 360 (HUEFS) JX870699*, JX870825*; Calliandra houstoniana (Mil l.)
Standl., Mexico, Guerrero, R.T. Colín 16765 (MEX U), J X870700*, JX870826*; Calliandra humilis Benth., P. Tenório L. 5970 (MEXU), JX870701*, –;
Calliandra hygrophila Mackinder & G.P. Lewis, Brazil, Bahia, E.R. de Souza 331 (HUEFS), JX870702*, JX870827*; Calliandra iligna Barneby, Brazil,
Minas Gerais, J.R. Pirani 4163 (HUEFS), JX870703*, JX870828*; Calliandra juzepczukii Standl., Mexico, A. Saynes V. 2354 (MEXU), –, J X870829*;
Calliandra laevis Rose, Mexico, Jalisco, D.J. Macqueen 617 (K), JX870704*, JX870830*; Calliandra lanata Benth., Brazil, Bahia, A. Rapini 1045 (HUEFS),
JX870705*, JX870831*; Calliandra laxa (Willd.) Benth., S.M. Souza 13374 (MEXU), J X870707*, –; Calliandra la xa (Willd.) Benth., G.T. Prance 29534
(MEXU), JX870706*, JX870832*; Calliandra leptopoda Benth., Brazil, Bahia, G.P. Lewis 1884 (K), JX870708*, JX870833*; Calliandra lintea Barneby,
Brazil, Bahia, E.R. de Souza 350 (HUEFS), JX870709*, JX870834*; Calliandra longipes Benth., Brazil, Goiás, B.M.T. Walter 2675 (HUEFS), JX870710*,
JX870835*; Calliandra longipinna Benth., Brazil, Bahia, E.R. de Souza 376 (HUEFS), JX870711*, JX870836*; Calliandra luetzelburgii Harms, Brazil,
Bahia, E.R. de Souza 340 (HUEFS), JX870712*, JX870837*; Calliandra macrocalyx Harms, Brazil, Bahia, L.P. de Queiroz 9111 (HUEFS), JX870713*, –;
Calliandra macrocalyx Harms, Brazil, Bahia, E.R. de Souza 413 (HUEFS), –, JX870838*; Calliandra magdalenae (Bertero ex DC.) Benth., Costa Rica, San
Jose, Q. Jimenez 1883 (K), JX870714*, JX870839*; Calliandra molinae Standl., Honduras, Francisco Morazan, M. Chorley 1 (BM), JX870715*, JX870840*;
Calliandra mollissima (Humb. & Bonpl. ex Willd.) Benth., Peru, Amazonas, T.D. Pennington 16851 (K), JX870716*, JX870841*; Calliandra mucugeana
Renvoize, Brazil, Bahia, E.R. de Souza 329 (HUEFS), JX870717*, JX870842*; Calliandra nebulosa Barneby, Brazil, Bahia, E.R. de Souza 342 (HUEFS),
JX870718*, JX870843*; Calliandra paganuccii E.R. Souza, Brazil, Bahia, S. Leython 854 (HUEFS), JX870720*, –; Calliandra paganuccii E.R. Souza,
Brazil, Bahia, E.R. de Souza 524 (HUEFS), JX870719*, –; Calliandra palmeri S. Watson, Mexico, Jalisco, D.J. Macqueen 200 (K), JX870721*, –; Calliandra
parviflora Benth., Bolivia, Santa Cruz, D. Soto 1195 (USZ), JX870723*, –; Calliandra parviflora Benth., Brazil, Bahia, J.R.I. Wood 19934 (K), JX870722*,
JX870844*; Calliandra parvifolia (Hook & Arn.) Speg., Brazil, Bahia, E.R. de Souza 357 (HUEFS), JX870724*, JX870845*; Calliandra paterna Barn eby,
Brazil, Bahia, E.R. de Souza 353 (HUEFS), JX870725*, JX870846*; Calliandra pedicellata Benth., Haiti, E.L. Ekman 985 (K), JX870726*, JX870847*;
Calliandra peninsularis Rose, Mexico, Baja California Sur, C.E. Hughes 1493 (K), –, JX870848*; Calliandra physocalyx H.M. Hern. & M. Sousa, Mexico,
Guerrero, R.T. Colín 16773 (MEXU), JX870727*, –; Calliandra pilgerana Harms, Brazil, Bahia, T.S. Nunes 980 (HUEFS), JX870728*, JX870849*; Callian-
dra pittieri Standl., B.B. Klitgaard 649 (K), JX870729*, JX870850*; Calliandra purdiei Benth., Ecuador, Napo, Spruce (K), JX870730*, JX870851*; Callian-
dra purpurea (L.) Benth., Martinique, Cap Salomon, D.C. Daly 5310 (K), JX870731*, JX870852*; Calliandra renvoizeana Barneby, Brazil, Bahia, E.R. de
Souza 383 (HUEFS), JX870733*, JX870854*; Calliandra rhodocephala Donn. Sm., Costa Rica, Alajuela, W. Haber 11246 (K), JX870734*, –; Calliandra
riparia Pittier, Brazil, Bahia, J.L. Hage 1860 (HUEFS), JX870735*, –; Calliandra rubescens (M. Martens & Galeotti) Standl., M. Sousa 8600 (MEXU),
JX870736*, JX870855*; Calliandra semisepulta Benth., Brazil, Bahia, E.R. de Souza 688 (HUEFS), –, JX870856*; Calliandra semisepulta Barneby, Brazil,
Bahia, E.R. de Souza 544 (HUEFS), JX870737*, –; Calliandra sessilis Benth., Brazil, Bahia, C. Correia 105 (HUEFS), JX870738*, JX870857*; Calliandra
silvicola Taub., Brazil, DF – Brasília, H.S. Irwin 6204 (K), JX870739*, JX870858*; Calliandra sincorana Harms, Brazil, Bahia, E.R. de Souza 359 (HUEFS),
JX870740*, –; Calliandra sincorana Harms, Brazil, Bahia, E.R. de Souza 355 (HUEFS), –, JX870859*; Calliandra sp., Brazil, Bahia, M.L.S. Guedes 14602
(ALCB), JX870742*, JX870861*; Calliandra sp., Brazil, Bahia, E.R. de Souza 548 (HUEFS), JX870743*, –; Calliandra sp., Brazil, Bahia, E.R. de Souza 558
(HU EFS), JX870744*, JX870863*; Calliandra sp., Brazil, Bahia, L.P. de Queiroz 9281 (HU EFS), JX870746*, JX870864*; Calliandra sp., Brazil, Bahia, E.R.
de Souza 514 (H UEFS), JX870745*, JX870862*; Calliandra spinosa Ducke, Brazil, Bahia, E.R. de Souza 138 (HUEFS), JX870741*, JX870860*; Calliandra
surinamensis Benth., Bra zil, Pará, J. Jardim 4524 (HU EFS), JX870747*, JX870865*; Calliandra taxifolia (Kunth) Benth., Ecuador, Loja, J.E. Mad sen 8368-B
(K), JX870748*, JX870866*; Calliandra tehuantepecensis (L. Rico & M. Sousa) E.R. Souza & L.P. Queiroz, Mexico, Oaxaca, M. Sousa 7433 (K), JX870761*,
JX870877*; Calliandra tergemina (L.) Benth., D. Neiel 5513 (MEXU), JX870749*, JX870867*; Calliandra trinervia Benth., –, AF365044.1; Calliandra
trinervia Benth., –, AF278516; Calliandra tsugoides R.S. Cowan, G.T. Prance 28958 (MEXU ), JX870750*, –; Calliandra tumbeziana J.F. Macbr., Peru, Piura,
R.J. Eastwood 119 (K), JX870751*, JX870868*; Calliandra tweedii Benth., Brazil, Rio Grande do Sul, G. Hatschbach 61367 (HUEFS), JX870752*, –; Calliandra
ulei Har ms, Brazil, Piauí, L.P. de Queiroz 14769 (HUEFS), JX870689*, JX870815*; Calliandra umbellifera Benth., Brazil, Piauí, L.P. Félix 7825 (HUEFS),
JX870753*, JX870869*; Calliandra vaupesiana R.S. Cowan, Colombia, Caquetá, J. Duivenvoorden 271 (K), JX870754*, JX870870*; Calliandra virgata
Benth., Brazil, Goiás, Luziânia, G. Hatschbach 54373 (HUEFS), JX870755*, –; Calliandra virgata Benth., Brazil, Distrito Federal, Planaltina, F.H.F. O lden -
burger 1879 (K), –, JX870871*; Calliandra viscidula Benth., Brazil, Bahia, E.R. de Souza 327 (HUEFS), –, JX870872*; Calliandra viscidula Benth., Brazil,
Bahia, E.R. de Souza 332 (HUEFS), JX870756*, –; Cedrelinga cateniformis (Ducke) Ducke, Brazil, Manaus, J.R. Nascimento 674 (INPA), JX870757*,
JX870873*; Cojoba arborea (L.) Britton & Rose, M. Chase 8244 (K), JX870758*, JX870874*; Cojoba catenata (Donn.Sm.) Britton & Rose, –, AY944538.1;
Cojoba rufescens (Benth.) Britton & Rose, EF638187, –; Ebenopsis ebano (Berland.) Barneby & J.W. Grimes, Mexico, Q.B.A.F. Ku 358 (MEXU), JX870759*,
JX870875*; Enterolobium timbouva Mart., Brazil, Bahia, L.P. de Queiroz 7973 (HUEFS), JX870760*, JX870876*; Havardia mexicana Britton & Rose,
Mexico, E. Joyal 2019 (MEXU), JX870762*, JX870878*; Hydrochorea corymbosa (Rich.) Barneby & J.W. Grimes, Brazil, Pará, G.C. Ferreira 571 (K),
JX870763*, JX870879*; Inga edulis Mart., Brazil, Bahia, L.P. de Queiroz 13797 (HUEFS), JX870764*, JX870880*; Inga thibaudiana DC., Brazil, Manaus,
M.A.S. Costa 1001 (INPA), JX870765*, JX870881*; Leucochloron limae Barneby & J.W. Grimes, Brazil, Bahia, M. Chase 8250 (K), JX870766*, JX870882*;
Macrosamanea pubiramea (Steud.) Barneby & J.W. Grimes, Venezuela, Amazonas, J. Jardim 4595 (HUEFS), JX870767*, JX870883*; Pithecellobium di-
versifolium Benth., Braz il, Bahia, L.P. de Queiroz 3740 (K), JX870768*, JX8708 84*; Pseudosamanea guachapele Ha rms, Ecuador, Gu ayas, J.E. Madsen 83914
(K), JX870769*, JX870885*; Samanea saman (Jacq.) Merr., Brazil, Bahia, E.R. de Souza 386 (HUEFS), JX870770*, JX870886*; Sphinga acatlensis (Be nth.)
Barneby & J.W. Grimes, Mexico, A. Martinez B. 339 (MEXU), J X870771*, JX870887*; Thailentadopsis nitida (Vahl) G.P. Lewis & Schrire, Sri Lanka,
Ceylon, A. Kostermans 28234 (K), JX870772*, JX870888*; Thailentadopsis tenuis (Craib) Kosterm., Thailand, Kanchanaburi, K & S.S. Larsen 33960 (K), –,
JX870889*; Viguieranthus ambongensis (R. Vig.) Villiers, Africa, Madagascar, J.N. Labat 2197 (K), JX870773*, JX870890*; Viguieranthus densinervus
Villiers, Africa, Madagascar, SF 12564 (K), JX870774*, JX870891*; Viguieranthus glaber Villiers, Africa, Madagascar, D.J. Du Puy M247 (K), JX870775*,
JX870892*; Viguieranthus kony (R. Vig.) Villiers, Africa, Madagascar, R. Rakoto 296 (P), JX870776*, –; Viguieranthus megalophyllus (R. Vig.) Villiers,
Africa, Madagascar, R. Rabevohitra 2354 (P), JX870777*, –; Viguieranthus subauriculatus Villiers, Africa, Madagascar, D. Turk 107 (P), JX870778*, –;
Zapoteca alinae H.M. Hern., Mexico, G. Manzanero M. 1137 (MEXU), JX870779*, JX870893*; Zapoteca f ilipes (Benth.) H.M. Hern., Brazil, Minas Gerails,
E.R. de Souza 324 (HUEFS), J X870780*, JX870896*; Zapoteca formosa (Kunth) H.M. Hern., Mexico, M. Sousa 9491 (HUEFS), JX870781*, JX870897*;
Zapoteca lambertiana (G. Don) H.M. Hern., Mexico, A.L.H. Mayfield 854 (MEXU), JX870782*, JX870894*; Zapoteca media (M. Martens & Galeotti)
H.M. Hern., Mexico, E. Torrecillas 68 (MEXU), –, JX870895*; Zapoteca sousae H.M. Hern. & A. Campos, Mexico, A. Campos 5224 (MEXU), JX870783*,
JX870898*; Zapoteca tetragona (Willd.) H.M. Hern., Mexico, G. Flores F. 669 (MEXU), JX870784*, JX870899*; Zygia racemosa (Ducke) Barneby &
J.W. Grimes, Brazil, Manaus, J.E.L.S. Ribeiro 1383 (I NPA), JX870785*, JX870900*.
Appendix 1.
Continued.
... The African genus Afrocalliandra (sensu Souza & al. 2013) and the Neotropical genus Calliandra s.s. (sensu Barneby 1998) are sisters (clade 1, Fig. 2-3) and together they represent the earliest diverging lineage within the Ingeae+Acacia clade ( Fig. 2-3). ...
... have 8-grained, asymmetrical, calymmate polyads including a tail cell (Hernández 1986), and Afrocalliandra is variably reported to have 7-10 grains in their acalymmate polyads. According to Souza & al. (2013), Afrocalliandra has 7-grained, asymmetrical, acalymmate polyads including a tail cell. Uneven numbers of pollen grains in polyads are not uncommon within Ingeae (Barneby & Grimes 1997). ...
... leaf morphology shows large variation between species and they can have one to many pairs of pinnae with one to many pairs of leaflets per pinna (Barneby 1998). The two species of Afrocalliandra have leaves with one pair of pinnae only, with several pairs of leaflets (Souza & al. 2013). Large variation of leaf morphology is also seen within Acaciella. ...
Preprint
We investigated generic relationships in the ingoid clade (Fabaceae) (sensu Koenen & al. 2020a), with main focus on genera with a taxonomic history in Calliandra s.l. of the tribe Ingeae (i.e. Afrocalliandra, Calliandra s.s., Sanjappa, Thailentadopsis, Viguieranthus, Zapoteca), and three genera of the tribe Acacieae (i.e., Acacia, Acaciella, Senegalia). The nuclear ribosomal ETS and ITS, and the plastid matK, trnL-trnF and ycf1 DNA-regions were analysed for 246 representatives from 36 genera using maximum likelihood as implemented in IQ-tree. The results show an Ingeae-Acacia clade within the ingoid clade, resolved in three major clades. Clade 1 (Calliandra s.s. and Afrocalliandra) is sister to clades 2 and 3. Clade 2 comprises Faidherbia, Sanjappa, Thailentadopsis, Viguieranthus and Zapoteca. Clade 3 comprises the remaining genera of the Ingeae, plus Acacia. The ingoid genus Senegalia is excluded from the Ingeae-Acacia clade. Acaciella is sister to the remaining ingoid clade when nuclear ribosomal data is included in the analyses, but included in the Ingeae-Acacia clade based on plastid data. Acacia and perhaps also Acaciella are thus nested within Ingeae. Species traditionally referred to Calliandra (Calliandra s.l.) are resolved in two clades, and the Calliandra-pod has apparently evolved independently several times.
... Calliandra is a large legume genus within the tribe Ingeae (mimosoid clade, subfamily Caesalpinioideae [1,2]) mainly used for ornamentation, soil restoration, forage, soil erosion control and as a medicinal plant [3][4][5]. The genus is considered to be exclusively neotropical [4] with three diversity centres: North-Central America (including the South of USA, Mexico and other countries of Central America; termed henceforth as North-Central America) wherein 35 species occur; Eastern Brazil (mainly in the Chapada Diamantina region in Bahia State, Brazil) wherein 46 species are known, including 36 endemics; and species widespread in South America, with 29 species occurring in various countries (e.g. ...
... The genus is considered to be exclusively neotropical [4] with three diversity centres: North-Central America (including the South of USA, Mexico and other countries of Central America; termed henceforth as North-Central America) wherein 35 species occur; Eastern Brazil (mainly in the Chapada Diamantina region in Bahia State, Brazil) wherein 46 species are known, including 36 endemics; and species widespread in South America, with 29 species occurring in various countries (e.g. Bolivia, Peru, Brazil) [1,4,6]. ...
... Most of the species from Eastern Brazil are endemic to the Chapada Diamantina in the state of Bahia; it is dominated by a rocky, open-field vegetation type common in Brazilian highland regions, denoted Campo Rupestre, and is a significant biodiversity centre for legumes. Our sampling included members of four out of the six infrageneric sections of Calliandra [1,4], hence comprising a broad phylogenetic sampling across the genus (Table S1). ...
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The neotropical genus Calliandra is of great importance to ecology and agroforestry, but little is known about its nodulation or its rhizobia. The nodulation of several species from two restricted diversity centres with native/endemic species (Eastern Brazil and North-Central America) and species widespread in South America, as well as their nodule structure and the molecular characterization of their rhizobial symbionts based on phylogeny of the 16S rRNA, recA and nodC gene, is reported herein. Species representative of different regions were grown in Brazilian soil, their nodulation observed, and their symbionts characterized. Calliandra nodules have anatomy that is typical of mimosoid nodules regardless of the microsymbiont type. The rhizobial symbionts differed according to the geographical origin of the species, i.e. Alphaproteobacteria (Rhizobium) were the exclusive symbionts from North-Central America, Betaproteobacteria (Paraburkholderia) from Eastern Brazil, and a mixture of both nodulated the widespread species. The symbiont preferences of Calliandra species are the result of the host co-evolving with the “local” symbiotic bacteria that thrive in the different edaphoclimatic conditions, e.g. the acidic soils of NE Brazil are rich in acid-tolerant Paraburkholderia, whereas those of North-Central America are typically neutral-alkaline and harbour Rhizobium. It is hypothesized that the flexibility of widespread species in symbiont choice has assisted in their wider dispersal across the neotropics.
... The biomes surrounding campos rupestres, such as the Cerrado, Amazon, Atlantic Forest, and SDTF, might be the source of plant lineages that colonised there. For example, the genus Calliandra Benth., common in campos rupestres, seems to have a SDTF origin(de Souza et al. 2013). However, unlike the Cerrado, colonisation of campos rupestres from surrounding biomes may not be evolutionarily recent. ...
... However, unlike the Cerrado, colonisation of campos rupestres from surrounding biomes may not be evolutionarily recent. The stem nodes of Calliandra species occurring in campos rupestres are dated to the Miocene(de Souza et al. 2013). Our phylogenetic tree shows low support values in backbone of the clade containing C. jasminodora ...
... Calliandra is commonly found throughout Brazil and is represented by 74 species, 46 of which are recorded from Chapada Diamantina, Bahia state (Northeast Region), the area with the highest diversity of this genus in the country (Souza et al., 2013;Flora do Brasil, 2020). A recent study revealed several Fabaceae in the Cariri region of Paraíba state (Rodrigues et al., 2020). ...
... We followed the Leguminosae Phylogeny Working Group (LPWG, 2017) in classifying the subfamilies, and Queiroz (2009) and Souza et al. (2013) for genus and species classifications. Type of habit was defined on the basis of field observations. ...
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Abstract. Calliandra subspicata (Fabaceae) hitherto had been reported from Pernambuco and Bahia, states of the Northeast Region of Brazil. Here we report this species from Paraíba state, the third state of this region. It was observed and collected at the Pico do Jabre State Park, a conservation unit situated at the residual massif of the Depression Sertaneja on the Borborema Plateau, which reaches an altitude of 1197 m. The identification was made on the basis of current literature. A morphological description, images, information about the area where the taxon was collected, and a key for identification of the species of Calliandra recorded in Paraíba state are provided.
... DNA Sampling, Extraction, Amplification, and Sequencing-The two datasets comprise four molecular regions, which have been successfully used in previous phylogenetic studies of mimosoid lineages (Luckow et al. 2003;Miller et al. 2003;Jobson and Luckow 2007;Souza 2007;Brown et al. 2008;Souza et al. 2013;Ferm 2019;Ferm et al. 2019). We sampled two nuclear regions, the internal transcribed spacer (ITS) and the external transcribed spacer (ETS), and two plastid regions, trnL-F (encompassing the trnL intron and the trnL-trnF spacer) and trnD-T. ...
... This group is mainly from the Brazilian cerrado and campo rupestre vegetation and appears to have had a recent and rapid diversification in these vegetation types, as hypothesized in studies of time divergence for series Rigidulae and Paniculatae (Souza et al., 2019a, andMendes et al., 2020, respectively). This is a common pattern in other genera of Fabaceae diverse in these two vegetation types (Simon et al., 2009;Souza et al., 2013;Queiroz et al., 2015;Alcantara, Ree & Mello-Silva, 2018;Inglis & Cavalcanti, 2018;Vaconcelos et al., 2020). ...
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Chamaecrista with > 330 species, six sections, three subsections and 39 series has had a long and complex taxonomic history. The genus is monophyletic, but most of its traditional infrageneric categories are not. To test the monophyly of sections, subsections and series of Chamaecrista, we used two molecular phylogenetic approaches. The first (Broad) based on two DNA regions (ITS and trnL-F) includes a comprehensive sampling of Chamaecrista spp. and infrageneric taxa. The second (Multilocus) is based on four molecular regions (ITS, ETS, trnL-F and trnE-T) for a smaller but representative sampling. We performed ancestral character reconstructions to identify morphological characters that could serve as synapomorphies for major clades. Both molecular approaches support Chamaecrista and sections Apoucouita, Grimaldia and Xerocalyx as monophyletic, but sections Chamaecrista, Caliciopsis and Absus and most of the series are not monophyletic. The four main clades recovered are all characterized by a combination of morphological characters: a clade of tree species with cauliflorous inflorescences (including species of section Apoucouita); a mostly Brazilian campo rupestre clade (including all species of subsections Adenophyllum, Baseophyllum and Otophyllum); a clade of mostly herbaceous/shrubby species with solitary flowers or fascicles (including sections Chamaecrista, Caliciopsis and Xerocalyx and extra-American species) and a clade (with three main subclades) of species with viscous indumentum (including section Grimaldia and section Absus subsection Absus). We propose a new infrageneric classification for Chamaecrista supported by molecular phylogenetic analyses and morphology, recognizing the four main clades as sections Apoucouita, Baseophyllum, Chamaecrista and Absus, the last with three subsections (Absus, Viscosa and Zygophyllum), but we do not recognize any previously circumscribed series. Our taxonomic treatment includes descriptions of and a key to the newly defined infrageneric taxa and an updated species list for the genus under the new classification.
... In a more general context, three previous phylogenetic analyses have been published with abundant accessions of ITS, and/or ETS Rodriguez de Souza et al., 2013;Iganci et al., 2015). In concordance with those, our large (rDNA-ETS, Fig. 2) analysis supports a basal position for the segregates of Acacia, namely Acaciella, Mariosousa, Senegalia, and Vachellia as well as for the Lysilo-ma+Hesperalbizia clade. ...
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Background and Aims: Lysiloma is a Neotropical genus in the Fabaceae family that comprises eight species, six of which are widely distributed in Mexico, and two more that occur in the Antilles and Florida. Lysiloma is frequent in Megamexico’s dry forests. A previous phylogenetic study included three species of Lysiloma and Hesperalbizia occidentalis. Both genera are closely related, but their divergence has weak support. Our objectives were to test the monophyly of the genus, evaluate the sister relationships within the genus, and estimate the divergence times. Methods: A phylogenetic analysis based on morphological characters, molecular markers (ETS, matK, and trnK), as well as a combined analysis (morphology + molecules) was performed. The data matrices were analyzed both individually and concatenated (total evidence approach) with Bayesian inference and Maximum Parsimony. In addition, molecular divergence times were estimated from the ETS dataset with a Bayesian uncorrelated lognormal relaxed clock. Key results: The morphological analysis supports the monophyly of Lysiloma with Hesperalbizia as sister group. However, the individual and the combined molecular analyses do not provide resolution to clarify the relationships between Hesperalbizia occidentalis, Lysiloma sabicu, and core Lysiloma. The total evidence analysis (including morphology) supports the monophyly of Lysiloma, yet with low support. According to our molecular clock model, the clade Lysiloma+Hesperalbizia diverged from other members of the tribe Acacieae+Ingeae about 32 million years ago, and the diversification of the core of Lysiloma occurred during the Miocene. Conclusions: Lysiloma+Hesperalbizia is an early divergent clade of tribes Acacieae+Ingeae. There are enough morphological differences to recognize both linages. Morphological characters informally used for taxonomic delimitation seem to have evolved homoplasiously. The clade Lysiloma and Hesperalbizia separated from other members of the tribe Acacieae+Ingeae in the Oligocene, but the diversification of the core of the genus coincides with the expansion of the dry forest at the beginning of the Miocene.