Reconstructing the deep-branching relationships of the papilionoid legumes

Abstract

Resolving the phylogenetic relationships of the deep nodes of papilionoid legumes (Papilionoideae) is essential to understanding the evolutionary history and diversification of this economically and ecologically important legume subfamily. The early-branching papilionoids include mostly Neotropical trees traditionally circumscribed in the tribes Sophoreae and Swartzieae. They are more highly diverse in floral morphology than other groups of Papilionoideae. For many years, phylogenetic analyses of the Papilionoideae could not clearly resolve the relationships of the early-branching lineages due to limited sampling. In the eight years since the publication of Legumes of the World, we have seen an extraordinary wealth of new molecular data for the study of Papilionoideae phylogeny, enabling increasingly greater resolution and many surprises. This study draws on recent molecular phylogenetic studies and a new comprehensive Bayesian phylogenetic analysis of 668 plastid matK sequences. The present matK phylogeny resolves the deep-branching relationships of the papilionoids with increased support for many clades, and suggests that taxonomic realignments of some genera and of numerous tribes are necessary. The potentially earliest-branching papilionoids fall within an ADA clade, which includes the recircumscribed monophyletic tribes Angylocalyceae, Dipterygeae, and Amburanae. The genera Aldina and Amphimas represent two of the nine main but as yet unresolved lineages comprising the large 50-kb inversion clade. The quinolizidine-alkaloid-accumulating Genistoid s.l. clade is expanded to include Dermatophyllum and a strongly supported and newly circumscribed tribe Ormosieae. Sophoreae and Swartzieae are dramatically reorganized so as to comprise monophyletic groups within the Core Genistoid clade and outside the 50-kb inversion clade, respectively. Acosmium is excluded from the Genistoids s.l. and strongly resolved within the newly circumscribed tribe Dalbergieae. By providing a better resolved phylogeny of the earliest-branching papilionoids, this study, in combination with other recent evidence, will lead to a more stable phylogenetic classification of the Papilionoideae.

Full text

Reconstructing the deep-branching relationships of the papilionoid legumes
D. Cardoso
a,
⁎, R.T. Pennington
b
, L.P. de Queiroz
a
, J.S. Boatwright
c
, B.-E. Van Wyk
d
,
M.F. Wojciechowski
e
, M. Lavin
f
a
Herbário da Universidade Estadual de Feira de Santana (HUEFS), Av. Transnordestina, s/n, Novo Horizonte, 44036-900 Feira de Santana, Bahia, Brazil
b
Royal Botanic Garden Edinburgh, 20A Inverleith Row, EH5 3LR Edinburgh, UK
c
Department of Biodiversity and Conservation Biology, University of the Western Cape, Modderdam Road, \ Bellville, South Africa
d
Department of Botany and Plant Biotechnology, University of Johannesburg, P. O. Box 524, 2006 Auckland Park, Johannesburg, South Africa
e
School of Life Sciences, Arizona State University, Tempe, AZ 85287-4501, USA
f
Department of Plant Sciences and Plant Pathology, Montana State University, Bozeman, MT 59717, USA
abstractarticle info
Available online 4 July 2013
Edited by J Van Staden
Keywords:
Leguminosae
matK
Papilionoideae
Phylogenetic classification
Sophoreae
Swartzieae
Resolving the phylogenetic relationships of the deep nodes of papilionoid legumes (Papilionoideae) is essential to
understanding the evolutionary history and diversification of this economically and ecologically important legume
subfamily. The early-branching papilionoids include mostly Neotropical trees traditionally circumscribed in the
tribes Sophoreae and Swartzieae. They are more highly diverse in floral morphology than other groups of
Papilionoideae. For many years, phylogenetic analyses of the Papilionoideae could not clearly resolve the relation-
ships of the early-branching lineages due to limited sampling. In the eight years since the publication of Legumes of
the World, we have seen an extraordinary wealth of new molecular data for the study of Papilionoideae phylogeny,
enabling increasingly greater resolution and many surprises.Thisstudydrawsonrecent molecular phylogenetic
studies and a new comprehensive Bayesian phylogenetic analysis of 668 plastid matK sequences. The present
matK phylogeny resolves the deep-branching relationships of the papilionoids with increased support for many
clades, and suggests that taxonomic realignments of some genera and of numerous tribes are necessary. The poten-
tially earliest-branching papilionoids fall within an ADA clade, which includes the recircumscribed monophyletic
tribes Angylocalyceae, Dipterygeae, and Amburanae. The genera Aldina and Amphimas represent two of the nine
main but as yet unresolved lineages comprising the large 50-kb inversion clade. The quinolizidine-alkaloid-
accumulating Genistoid s.l. clade is expanded to include Dermatophyllum and a strongly supported and newly
circumscribed tribe Ormosieae. Sophoreae and Swartzieae are dramatically reorganized so as to comprise mono-
phyletic groups within the Core Genistoid clade and outside the 50-kb inversion clade, respectively. Acosmium is
excluded from the Genistoids s.l. and strongly resolved within the newly circumscribed tribe Dalbergieae. By pro-
viding a better resolved phylogeny of the earliest-branching papilionoids, this study, in combination with other
recent evidence, will lead to a more stable phylogenetic classification of the Papilionoideae.
© 2013 SAAB. Published by Elsevier B.V. All rights reserved.
1. Introduction
The spectacular radiation of the papilionoid legumes (Papilionoideae)
across an estimated 13 800 species, 478 genera, and 28 tribes is a legacy of
their extraordinarily broad ecological and biogeographical range largely
associated with diversifications in tropical rain forests, savannas, season-
ally dry forests, and temperate regions worldwide (Lavin et al., 2005;
Lewis et al., 2005; Schrire et al., 2005). Papilionoids are also well known
for their unprecedented economic importance to agriculture and the
food industry, as they include pulse legume crops such as soybean
[Glycine max (L.) Merr.], culinary beans (Phaseolus L. spp. and Vicia
faba L.), groundnut (Arachis hypogaea L.), lentil (Lens culinarius Medik.),
pea (Pisum sativum L.), and the important forage crop alfalfa (Medicago
sativa L.).
A highly specialized papilionate flower is the most distinctive
morphological feature used to characterize and common to nearly
all Papilionoideae. It is typically distinguished from the mostly
radially symmetrical mimosoid and the generally bilateral but
non-papilionate caesalpinioid flowers by having petals clearly differ-
entiated into a standard (or banner), wings, and a keel, and partially
fused stamens enveloping the ovary. This floral organization in-
volves a strong bilateral symmetry and three-dimensional depth
that often limit access to the nectar and pollen, and is intimately
associated with bee pollination (Arroyo, 1981; Westerkamp and
Claßen-Bockhoff, 2007). Variation in this floral architecture has
greatly influenced the taxonomy of the Papilionoideae. A high degree
of floral connation, especially of the staminal filaments, and keel and
wing petals, has traditionally marked the putative “advanced”
papilionoid tribes (e.g., Polhill, 1981a). Genera exhibiting flowers
with greater radial symmetry than bilateral symmetry, or with in-
completely differentiated petals and free stamens, in contrast, have
South African Journal of Botany 89 (2013) 58–75
⁎Corresponding author. Tel.: +55 7531618132.
E-mail address: cardosobot@gmail.com (D. Cardoso).
0254-6299/$ –see front matter © 2013 SAAB. Published by Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.sajb.2013.05.001
Contents lists available at ScienceDirect
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been classified into the “primitive”or “basal”tribes Sophoreae and
Swartzieae (e.g., Cowan, 1981; Polhill, 1981a, 1994).
The monophyly of the Papilionoideae has been consistently re-
solved in family-wide molecular phylogenetic analyses (Doyle, 1995;
Käss and Wink, 1995, 1996, 1997; Doyle et al., 1997, 2000; Kajita
et al., 2001; Wojciechowski et al., 2004; Lavin et al., 2005; McMahon
and Sanderson, 2006; Cardoso et al., 2012a; LPWG, 2013). Perhaps
the most unexpected finding stemming from the increasing interest
in the Papilionoideae phylogeny was the broad polyphyly of the pu-
tatively “primitive”tribes, with elements of each scattered widely
across the tree (Pennington et al., 2001; Wojciechowski, 2003;
Wojciechowski et al., 2004; Cardoso et al., 2012a, 2012b). The land-
mark publication of Legumes of the World (Lewis et al., 2005)that
summarized taxonomic and molecular phylogenetic advances to
date represented a big step towards a phylogeny-based classification
of the whole legume family. Radical shifts in inter and intra-tribal re-
lationships within Papilionoideae were suggested, but the majority
of the tribes remained defined in the traditional sense (Polhill,
1981a, 1981b, 1981c; Polhill, 1994), recognizing the need for more
robustly supported phylogenies and better taxon sampling (Lewis
et al., 2005). This was particularly true for the relationships among
the earliest-branching papilionoids, where resolution was poor, and
where phylogenies failed to sample several unusual, non-papilionate-
flowered genera traditionally classified in Sophoreae and Swartzieae
(Cardoso et al., 2012a). Indeed, that the early-branching papilionoids
were problematic in this, and other ways, was emphasized earlier by
the prominent legume taxonomist Roger Polhill of the Royal Botanic
Gardens, Kew. In 1981 Polhill recognized the heterogeneous nature of
the Sophoreae: “The Sophoreae s.l. is a tribe of convenience between
the Caesalpinioideaeand the bulk of the Papilionoideae, sharply defined
from neither”(Polhill, 1981a: 213). Then later in 1994 he pointed out
in his revised legume classification that “Considerable emphasis has
been made on the analysis of basal groups in the Caesalpinioideae and
Papilionoideae, but further studies here are critical if groups with
derived features are to be defined clearly”(Polhill, 1994: xlii).
The molecular phylogenies derived from the trnL intron (Pennington
et al., 2001)andmatK (Wojciechowski et al., 2004) sequences were
the first to focus on the unusual lineages of papilionoid legumes marked
by radial floral symmetry or non-papilionate flowers. These studies
provided a starting point for subsequent clade-specific phylogenetic
studies involving non-papilionate flowered lineages, such as the
Amorpheae (McMahon and Hufford, 2004), Lecointeoids (Mansano
et al., 2004), Vataireoids (Cardoso et al., 2013a), Dalbergioids (Lavin
et al., 2001; Cardoso et al., 2012b), and Genistoids (Boatwright et al.,
2008a; Cardoso et al., 2012c). Recently, a renewed interest in the
early-branching papilionoid phylogeny involving the most comprehen-
sive sampling from within Sophoreae and Swartzieae has shed more
light on the obscure position of several genera and relationships of
many clades (Cardoso et al., 2012a). A recurrent result emerging from
phylogenetic studies of the early-branching papilionoids is the evolu-
tionary reversions from a papilionate flower to one with radial or undif-
ferentiated architecture (Pennington et al., 2000; McMahon and
Hufford, 2004; Cardosoet al., 2012a, 2012b, 2012c, 2013a). The high in-
tegration of floral parts in the papilionate flower has clearly been evolu-
tionarily labile, thus rejecting the traditional view that non-papilionate
flowers marked the “primitive”groups of Papilionoideae or in some
manner represented signatures of antiquity (e.g., Arroyo, 1981; Polhill,
1981a, 1994; Tucker and Douglas, 1994). The taxon sampling of
Cardoso et al. (2012a) was, however, intentionally sparse within the
non-protein–amino-acid-accumulating (NPAAA) papilionoid lineages,
and so they left significant implications with regard to the systematics
of several early-branching clades to be further investigated in a more
complete phylogeny.
To gain more insights into the evolution and phylogenetic classifi-
cation of the Papilionoideae requires a robust taxon sampling that in-
tegrates the wealth of available molecular data (e.g., Hu et al., 2000;
Lavin et al., 2001, 2003; Steele and Wojciechowski, 2003; McMahon
and Hufford, 2004; Wojciechowski et al., 2004; Bruneau et al., 2008;
Egan and Crandall, 2008; Stefanovićet al., 2009; Delgado-Salinas
et al., 2011; Cardoso et al., 2012a, 2012b, 2013a; Sirichamorn et al.,
2012). A more comprehensive phylogeny of the Papilionoideae is
pivotal for understanding the evolution of the dramatic floral diversi-
ty among the early-branching clades (Figs. 2–5;Pennington et al.,
2000), the timing of diversification (Lavin et al., 2005), biogeography
(Schrire et al., 2005), and the origin of the complex symbiotic associ-
ation with root-nodulating bacteria in the whole subfamily (Doyle
et al., 1997; Doyle and Luckow, 2003; Doyle, 2011). A better sampled
phylogeny can also lead to a new opportunity to address the question of
why the deep-nodes of the papilionoids are so poorly resolved (Lavin
et al., 2005; Cardoso et al., 2012a). Why are the early-branching genera
so prone to changes in floral symmetry (Pennington et al., 2000;
Cardoso et al., 2012a, 2012b) or to the lack of the ability to nodulate
(Sprent, 2001; J. Sprent, pers. comm.)? In the present study, however,
we focus on questions related to a new phylogeny-based classification
of the Papilionoideae to set the stage for future taxonomic, biogeo-
graphical, evolutionary, and ecological research. The most densely-
sampled matK phylogeny at generic level of the Papilionoideae is ana-
lyzed to review the systematics of the early-branching clades. We set
out to facilitate the formalization of a new phylogenetic classification
of the Papilionoideae, where most informally named clades (sensu
Wojciechowski et al., 2004; Cardoso et al., 2012a)arereportedas
potential candidates to be recognized at tribal rank. Finally, we address
some key challenges for the path toward reconstructing the deep-
branching relationships of the Papilionoideae.
2. Materials and methods
Taxon sampling and molecular data
The complete plastid matK protein-coding gene (Hilu and Liang,
1997) was selected because it has been widely used in legume phylo-
genetics and revealed excellent resolution at many taxonomic levels
(e.g., Hu et al., 2000; Lavin et al., 2001; Steele and Wojciechowski,
2003; McMahon and Hufford, 2004; Wojciechowski et al., 2004;
Bruneau et al., 2008; Pennington et al., 2010; Delgado-Salinas et al.,
2011; Cardoso et al., 2012a, 2013a). Comparative analyses of the
matK and rbcL genes have shown levels of sequence divergence up
to ninefold higher for matK than for rbcL, and substitutions are dis-
tributed more uniformly among the three codon positions in matK
(Lavin et al., 2005). We screened GenBank for all available matK se-
quences of legumes. Our strategy was aimed at sampling as many
genera as possible across all major lineages of the Papilionoideae as
guided by the previous phylogenies of Wojciechowski et al. (2004)
and Cardoso et al. (2012a). Because the phylogenetic analysis of
Cardoso et al. (2012a) focusing on the early-branching clades used a
too sparse taxon sampling from within the NPAAA clade, the present
more densely-sampled analysis can validate the clades that emerged
from that study. Also, a comprehensive taxon sampling potentially
improves phylogenetic accuracy because of the increased probability
of subdividing long branches (e.g., Graybeal, 1998; Pollock et al.,
2002; Zwickl and Hillis, 2002; Heath et al., 2008).
Our matK data set includes 668 accessions, of which 535 are from
Papilionoideae, representing 507 species and 323 of the 478 currently
recognized genera within the subfamily (Lewis et al., 2005). The
early-branching clades accounted for 352 accessions from 325 species
and 145 genera. Some early-branching genera are for the first
time evaluated in a matK family-level phylogeny: Ammopiptanthus
S.H.Cheng, Aspalathus L., Argyrolobium Eckl. & Zeyh., Bocoa Aubl.,
Bolusia Benth., Dichilus DC., Euchlora Eckl. & Zeyh., Laburnum Fabr.,
Lebeckia Thunb., Rafnia Thunb., and Steinbachiella Harms. Nearly all
genera (49 out of 62) of the traditionally circumscribed tribes Sophoreae
and Swartzieae have been sampled, except for representatives of the
59D. Cardoso et al. / South African Journal of Botany 89 (2013) 58–75

following: Ammothamnus Bunge, Dalhousiea Wall. ex Benth., Fairchildia
Britton & Rose, Haplormosia Harms, Leucomphalos Benth. ex Planch.,
Mildbraediodendron Harms, Neoharmsia R.Vig., Pericopsis Thwaites,
Petaladenium Ducke, Platycelyphium Harms, Sakoanala R.Vig., Salweenia
Baker, and Uleanthus Harms. Nevertheless, we can tentatively place
most of these genera in some major branch of the papilionoid tree
based on different DNA sequence data, chemistry or morphology.
Most sequences used in the present data set are from our ongoing phy-
logenetic studies on the early-branching papilionoids (de Queiroz et al.,
2010; Cardoso et al., 2012a, 2012b, 2013a; Le Roux et al., in press;
Wojciechowski, 2013), which provided 181 accessions. Significant ef-
forts of others added considerably to our broad taxon coverage (e.g.,
Hu et al., 2000; Lavin et al., 2001, 2003; Steele and Wojciechowski,
2003; McMahon and Hufford, 2004; Wojciechowski et al., 2004;
Bruneau et al., 2008; Egan and Crandall, 2008; Stefanovićet al., 2009;
Delgado-Salinas et al., 2011; Lewis et al., 2012; Sirichamorn et al.,
2012; L.P. de Queiroz et al., unpubl.; M.F. Wojciechowski, unpubl.).
We selected seven taxa from Polygalaceae, Surianaceae, and
Quillajaceae, and 84 caesalpinioid and 42 mimosoid taxa representing
all constituent main lineages as the outgroups (Luckow et al., 2003;
Lewis et al., 2005; Bruneau et al., 2008; Bello et al., 2009, 2012).
Alignment and phylogenetic analysis
The matK sequences were aligned manually in Se-Al v2.0a11
(Rambaut, 1996) using the similarity criterion of Simmons (2004) and
following the suggestions of Wojciechowski et al. (2004) in order to
avoid inconsistencies derived from automated multiple alignments.
These involved translating the DNA sequences to their corresponding
amino acid sequences to accurately align the DNAsequences with inser-
tions and deletions (indels) at equivalent positions. This procedure
resulted in numerous, but unambiguous, indels with respect to their
placement in the aligned data set. All sequences were complete except
for 60 accessions that had 100 or more missing nucleotides at one of the
ends, most of these however from the mimosoids or the NPAAA
papilionoids. The matK data set of 668 aligned sequences of 1785 nucle-
otide characters is publicly available at http://www.montana.edu/
mlavin/data/papilionoid6ilc.txt.
The matK phylogenetic tree was inferred using Bayesian inference
(Yang and Rannala, 1997; Lewis, 2001) as implemented in MrBayes
v3.1.2 (Ronquist and Huelsenbeck, 2003) using the Cyberinfrastructure
for Phylogenetic Research (CIPRES) Portal 2.0 (Miller et al., 2010). The
best-fitting nucleotide substitution model GTR + I + Γwith base fre-
quency, substitution rates, and among-site variation variables was esti-
mated from the data via the Akaike information criterion (AIC) (Akaike,
1974) as implemented in ModelTest 3.7 (Posada and Crandall, 1998).
Two separate runs of a Metropolis-coupled Markov Chain Monte
Carlo (MCMC) permutation of parameters were each initiated with a
random tree and eight simultaneous chains set at default temperatures
(Huelsenbecketal.,2001). Markov chains were run for 28 190 000 gen-
erations and sampled every 10 000th generation such that 2220
nonautocorrelated Bayesian trees were sampled broadly from likeli-
hood stationarity for each of the two runs after a burn-in of 6 000 000
generations. The program Tracer v1.3 (Rambaut and Drummond,
2004) was used to assess the convergence of the MCMC run and the ad-
equacy of the burn-in length. Trees sampled from post burn-in genera-
tions were summarized in a majorityrule consensus tree that included
posterior probabilities as branch support estimates. The Bayesian
majority-rule consensus was then visualized and partially edited using
FigTree v1.4.0 (Rambaut, 2012).
Clade nomenclature and classification
We followed the criteria of Wojciechowski et al. (2004) for recog-
nizing major papilionoid clades, which are consistent with formal
node-based definitions under a system of phylogenetic nomenclature
(de Queiroz and Gauthier, 1994). These involved the definition of
strongly supported monophyletic groups that are congruent with
other studies based on different molecular markers. We give sugges-
tions for future renaming of clades with available previously published
names of papilionoid tribes. Formal taxonomic changes will be the focus
of a more complete treatment for the whole family authored by the
Legume Phylogeny Working Group (LPWG). We advocate that along-
side a future new Linnean classification the informally named clades,
especially more inclusive ones such as the Genistoids s.l., Dalbergioids
s.l., Millettioids or Robinioids should be maintained in a new phyloge-
netic classification of legumes (Wojciechowski, 2013). Without group-
ing the tribes under such consistently supported clades the legume
classification will be just a collection of tribes without implicit informa-
tion of phylogenetic relationships between them. Such inclusive infor-
mal clades are not only taxonomically informative, but also bring a
phylogenetic dimension for the practical purpose of classification. We
recommend that phylogenetically unresolved genera should not be for-
mally classified in a Linnean rank-based classification as distinct mono-
typic tribes at this stage when our phylogenetic estimates are based
fundamentally on a few chloroplast loci. They should be recognized as
incertae sedis until better resolved phylogenies, based upon multiple
loci, including nuclear regions, are available (LPWG, 2013).
3. Results
The matK Bayesianmajority-rule consensus tree washighly resolved
and well supported with respect to the relationships for the major
clades of the papilionoid legumes (Fig. 1; Appendix S1, see Supplemen-
tal data with the online version of this article). The monophyly of
the Leguminosae is corroborated (Fig. 2). The Papilionoideae and
Mimosoideae, excluding Dinizia Ducke, were each strongly supported
as monophyletic and nested within a paraphyletic Caesalpinioideae
(Fig. 2). Within the Papilionoideae, deep-branching relationships
had increased support for many clades, and taxonomic realignments
of some genera and of numerous tribes are necessary. The earliest di-
chotomy subtends two clades, one of which we term the ADA clade
and it includes three lineages: the Angylocalyceae, Dipterygeae, and
Amburaneae clades (Fig. 2). The ADA clade is sister to a weakly support-
ed clade comprising the newly circumscribed tribe Swartzieae and a
clade that includes the Cladrastis clade and the rest of the papilionoid le-
gumes in the strongly-supported 50-kb inversion clade (Figs. 2–3).
Nine strongly supported constituent clades within the 50-kb inversion
clade were resolved as a polytomy: the genera Amphimas Pierre ex
Dalla Torre & Harms, Aldina Endl., and Dermatophyllum Scheele, the
newly circumscribed Exostyleae, the Vataireoid, Andira, and Genistoid
s.l. clades, the Dalbergioid s.l. clade comprising tribes Amorpheae and
the newly circumscribed Dalbergieae, and a large clade containing the
newly circumscribed monophyletic Baphieae and the remaining
papilionoids from within the NPAAA clade, namely the Hypocalypteae,
Mirbelioids, Indigoferae, Millettioids, and the predominantly temperate
Hologalegina clade (Figs. 3–5;AppendixS1).
The non-monophyly of several genera was also confirmed:
Aeschynomene L., Baphia Afzel. ex Lodd., Cladrastis Raf., Clathrotropis
Harms, Myrocarpus Allemão, Psorothamnus Rydb., Sophora L., and
Thermopsis R.Br. The large Genistoid s.l. clade is strongly supported
and fully resolved, and includes the monophyletic Brongniartieae,
Crotalarieae, Genisteae, Podalyrieae with the inclusion of the morpholog-
ically unusual genus Cadia Forssk., and the resurrected tribes Leptolobieae
and Ormosieae, which is strongly supported as sister to all Genistoids
(Fig. 4). Camoensia Welw. ex Benth. & Hook.f., which has morphologically
anomalous flowers, is the first-branching genus of the Core Genistoids
and placed in its own monotypic tribe Camoensieae. Sophoreae is now
dramatically reorganized to encompass only a small clade within the
Core Genistoids (Fig. 4). A putative new genus to be segregated from
Clathrotropis is not resolved with respect to any of the aforementioned
main Genistoid subclades (Fig. 4). The genus Acosmium Schott is
60 D. Cardoso et al. / South African Journal of Botany 89 (2013) 58–75

excluded from the Genistoids s.l. and strongly confirmed within the
newly circumscribed Dalbergieae (Fig. 5).
4. Discussion
The present matK phylogenetic analysis (Fig. 2) corroborates the
monophyly of the subfamilies Mimosoideae and Papilionoideae
nested within a paraphyletic Caesalpinioideae (Doyle et al., 1997,
2000; Luckow et al., 2003; Bruneau et al., 2008; Kajita et al., 2001;
Pennington et al., 2001; Wojciechowski et al., 2004; Lavin et al.,
2005; Cardoso et al., 2012a; LPWG, 2013). Relationships among
the early-branching papilionoid lineages that fall outside of the
non-protein–amino-acid-accumulating (NPAAA) clade (Fig. 1) were
recently well resolved in phylogenetic analyses of matK and trnL intron
sequences (Cardoso et al., 2012a). That study revealed the identity,
generic composition and realignments, and inter-relationships of several
new clades, which were largely unresolved in previous analyses
(e.g., Doyle et al., 1997; Kajita et al., 2001; Pennington et al., 2001;
Wojciechowski et al., 2004; McMahon and Sanderson, 2006). The
present study confirms the same deep-node relationships revealed by
the parsimony and Bayesian phylogenetic analyses of Cardoso et al.
(2012a) (Figs. 1–5), as well as the subclades within the large NPAAA
clade as revealed by the first most comprehensive family-level phylog-
eny of Wojciechowski et al. (2004) (Appendix S1), demonstrating the
value of the matK gene in resolving legume relationships. Dense sam-
pling of taxa for matK provided resolution of the early-branching
papilionoids even when preliminary studies suggested that resolution
would be difficult to obtain.
When the latest tribal legume classification was published (Lewis
et al., 2005), adequate genus-level sampling was not yet available to em-
bark upon formal changes to the taxonomic scheme of Polhill (1994).The
accumulation of new molecular data in recent years, especially with re-
spect to the use of the matK gene (e.g., Bruneau et al., 2008; Egan and
Crandall, 2008; Stefanovićet al., 2009; Delgado-Salinas et al., 2011;
Cardoso et al., 2012a, 2012b, 2013a; Sirichamorn et al., 2012)hasprovid-
ed the impetus to move Papilionoideae systematics forward toward a
Angylocalyceae
Dipterygeae
Amburaneae
Swartzieae
Cladrastis
clade
Exostyleae
Vataireoid
clade
Andira
clade
Podalyrieae
Ormosieae
Crotalarieae
Brongniartieae
Genisteae
Leptolobieae
Sophoreae
Camoensieae
Amorpheae
Baphieae
Dalbergieae
NPAAA
50-kb
paps
genistoids s.l.
ADA
dalbergioids s.l.
matK
Fig. 1. Summary of the matK Bayesian majority-rule consensus tree of legumes showing the main early-branching papilionoid clades that are the focus of this study. The focus is set
on the clades outside the large and diverse non-protein–amino-acid-accumulating (NPAAA) clade. Branches in bold are those supported by a posterior probability of 0.99–1.0.
61D. Cardoso et al. / South African Journal of Botany 89 (2013) 58–75

more stable higher-level classification of the entire family that reflects
phylogeny. We provide below an overview of the relationships and
generic composition of the early-branching clades, most of which
are readily distinguished by non-molecular synapomorphies, and
which might be recognized at tribal level in a new phylogenetically
based Linnean classification. In terms of species diversity, from
the currently recognized 196 early-branching genera (Table 1), it
is noteworthy that more than 70% are species-poor (48 genera are
0.1 changes
Castanospermum australe JX295891
Suriana maritima AY386950
Quillaja saponaria AY386843
Umtiza clade
Diptychandra aurantiaca EU361935
Cordyla africana JX295923
Prioria clade
Dimorphandra conjugata EU361934
Myrocarpus frondosus AY386925
Stylobasium spathulatum EU604032
Angylocalyx talbotii JQ669611
Myrocarpus emarginatus JX295863
Amherstieae clade
Myroxylon balsamum JX295935
Myroxylon peruiferum JX295911
Taralea cordata JX295872
Cordyla africana JF270724
Arapatiella psilophylla EU361859
Mora gonggrijpii EU362005
Myrocarpus emarginatus JQ669614
Dipteryx oleifera JX295933
Angylocalyx sp. AY553715
Duparquetia orchidacea EU361937
Dipteryx polyphylla JX295870
Taralea oppositifolia JX295900
Dipteryx rosea JF491268
Cercideae clade
Brandzeia filicifolia EU361870
Myrospermum frutescens JQ587796
Alexa bauhiniiflora JX295931
Myrospermum sousanum AY386959
Dipteryx punctata JX295869
Pterodon pubescens AF272095
Goniorrhachis marginata EU361959
Alexa grandiflora JF491262
Detarieae s.s. clade
Cassia clade
Myrospermum frutescens JQ587794
Dussia lehmannii JX295924
Dipteryx magnifica JX295871
Caesalpinia clade
Moldenhawera brasiliensis EU362004
Xanthocercis zambesiaca JF270996
Taralea rigida JX295934
Myroxylon balsamum FJ151488
Amburana acreana JX295866
Monopteryx inpae JX295875
Erythrophleum suaveolens EU361949
Guilfoylia monostylis EU604031
Dipteryx alata AY553717
Daniellia klainei EU361927
Dialiinae clade
Pterodon emarginatus JX295874
Myrocarpus fastigiatus JX295966
Monopteryx inpae JX295876
Amburana cearensis JX846614
Amburana cearensis AY553712
Vauquelinia californica AY386949
Peltophorum clade
Barnebydendron riedelii EU361868
Myroxylon balsamum JX295937
Myroxylon balsamum JX295912
Alexa grandiflora JX295968
Pterodon abruptus JX295873
Dussia lanata JX295925
Myroxylon balsamum JX295936
Myrospermum sousanum JX295938
Dipteryx odorata JX295898
Dinizia excelsa JX295860
Monnina phytolaccifolia EU596519
Alexa wachenheimii JQ626338
Alexa canaracunensis JQ669613
Myrospermum frutescens AF142679
Dussia macroprophyllata AY386903
Polygala californica AY386842
Myrospermum sousanum JX295922
72
85
78
76
97
85
97
68
95
54
93
82
85
95
73
Mimosoideae
Length
= 0.45
Swartzieae
Cladrastis clade
50-kb inversion clade
Papilionoideae
Angylocalyceae
Dipterygeae
Amburaneae
ADA clade
Castanospermum
Pterodon
Amburana
Leguminosae
Caesalpinioideae
Myrocarpus
Monopteryx
matK
Fig. 2. Majority-rule consensus tree derived from the matK Bayesian analysis of the legumes with emphasis on the early-branching papilionoid clades. This portion of the tree high-
lights the relationships and generic composition of the first-branching ADA lineage. Representative outgroups from within mimosoids and caesalpinioids were comprehensively
sampled. Most taxon names of mimosoids and caesalpinioids as well as of the non-protein–amino-acid-accumulating (NPAAA) papilionoids are omitted to focus on clades of
interest. Numbers on branches are Bayesian posterior probabilities. Posterior probabilities are not given for the resolved branches weakly supported by 0.50–0.79. Branches in
bold are those supported by a posterior probability of 0.99 or 1.0. GenBank accession numbers are provided after taxon names. Photos: Domingos Cardoso[Amburana cearensis
(Allemão) A.C.Sm., Castanospermum australe A.Cunn. & C.Fraser ex Hook., and Myrocarpus fastigiatus Allemão], Mauricio Mercadante (Pterodon pubescens Benth.), and Scott Mori
(Monopteryx inpae W.A.Rodrigues).
62 D. Cardoso et al. / South African Journal of Botany 89 (2013) 58–75

monospecific and 92 have 2–10 species) and mostly non-papilionate-
flowered, whereas only 10 genera can be considered species rich
(>100 species). All together these genera contribute towards making
the early radiation of papilionoid legumes one of the most striking
examples of unparalleled evolution of flower diversity among the
flowering plants (Figs. 2–5).
Aldina
Zollernia ilicifolia JX152654
Vatairea macrocarpa JX152609
Ateleia guaraya JX295883
Vatairea sp. nov. AF270859
Zollernia aff. glabra JX295916
Luetzelburgia praecox JX152646
Candolleodendron brachystachyum JX295929
Sweetia fruticosa JX152620
Luetzelburgia sotoi JX152652
Styphnolobium burseroides JQ619938
Vatairea lundellii JX152605
Ateleia pterocarpa GU220023
Vatairea fusca JX152599
Swartzia arborescens JX295964
Bobgunnia fistuloides EU361885
Luetzelburgia bahiensis JX152634
Swartzia cubensis JQ587869
Vatairea paraensis JX152611
Ateleia popenoei GU220022
Cladrastis delavayi AY386861
Exostyles aff. venusta JX152591
Lecointea peruviana EU361990
Sweetia fruticosa JX152621
Pickeringia montana var. montana AY386863
Candolleodendron brachystachyum JX295890
Sweetia fruticosa AY386911
Ateleia glazioveana GU220020
Zollernia glabra JX295915
Ateleia mcvaughii GU220021
Holocalyx balansae JX152593
Styphnolobium japonicum AY386962
Swartzia pickelii JX295905
Styphnolobium conzattii JQ619939
Lecointea hatschbachii JX152594
Swartzia flaemingii AY386941
Vatairea heteroptera JX152603
Swartzia pinheiroana JX295914
Bocoa prouacensis FJ037904
Uribea tamarindoides AY553719
Styphnolobium affine JQ619972
Ateleia herbert-smithii AY386953
Luetzelburgia andrade-limae JX152627
Harleyodendron unifoliolatum JX152592
Pickeringia montana var. tomentosa JQ669636
Sweetia fruticosa JX152619
Vatairea guianensis JX152600
Swartzia apetala JX295908
Trischidium molle JX295868
Luetzelburgia purpurea JX152648
Styphnolobium monteviridis JQ619940
Luetzelburgia harleyi JX152642
Bocoa prouacensis JQ626415
Cyathostegia matthewsii HM347483
Trischidium alternum JX295928
Luetzelburgia amazonica JX152622
Luetzelburgia guianensis JX152639
Swartzia canescens JQ626472
Amphimas pterocarpoides JX295894
Zollernia glaziovii JX295952
Zollernia magnifica JX152595
Luetzelburgia neurocarpa JX152645
Swartzia jorori AY386942
Cladrastis lutea AF142694
Luetzelburgia trialata JX152617
Trischidium decipiens JX295867
Luetzelburgia guaissara JX152636
Swartzia polita JX295913
Zollernia modesta JX295917
Exostyles venusta JX152590
Luetzelburgia andina JX152624
Holocalyx balansae AY553714
Zollernia latifolia JX295918
Swartzia simplex AF142678
Luetzelburgia auriculata JX152630
Vataireopsis araroba JX152613
Swartzia cardiosperma EU362053
Cyathostegia matthewsii HM347486
Vatairea erythrocarpa JX152597
Cyathostegia matthewsii HM347482
Ateleia arsenii GU220019
Vataireopsis surinamensis JX152618
Lecointea peruviana JX295927
Cladrastis platycarpa AY386935
Bobgunnia madagascariensis AY386940
Vatairea sericea JX152612
Vataireopsis speciosa JX152615
Exostyles godoyensis JX152589
72
91
96
98
88
85
91
89
94
96
Aldina heterophylla JX295956
Aldina insignis JN168674
Aldina latifolia JX295861
84
Hymenolobium heringerianum JX295910
Hymenolobium petraeum JX295909
Andira legalis JX295893
Andira humilis JX295960
Hymenolobium janeirense JX295904
Andira inermis JF501102
Hymenolobium heterocarpum JX295902
Andira ormosioides JX295962
Andira sp. JX295896
Andira marauensis JX295899
Hymenolobium alagoanum JX295906
Hymenolobium mesoamericanum AY386934
Hymenolobium grazielanum JX295907
Andira galeottiana AF142681
Hymenolobium heterocarpum JX295901
Andira carvalhoi JX295958
Hymenolobium sericeum JX275933
92
Angylocalyceae
Dipterygeae
Amburaneae
0.1 changes
Papilionoideae
50-kb inversion clade
Swartzieae
Cladrastis clade
Exostyleae
Vataireoid clade
Andira clade
Zollernia
Harleyodendron
Cladrastis
Hymenolobium
Andira
Swartzia Trischidium
Vatairea
Luetzelburgia
Ateleia
clade
Swartzia
clade
Fig. 3. Continuation of the matK Bayesian majority-rule consensus tree of the early-branching papilionoids. This portion shows the first-branching Swartzieae and Cladrastis clades,
as well as some isolated, unresolved genera, the Exostyleae, Vataireoid, and Andira clades from the large 50-kb inversion clade. See Fig. 2 for details. Photos: Cecília de Azevedo
(Andira fraxinifolia Benth.), Domingos Cardoso [Aldina latifolia Benth., Harleyodendron unifoliolatum R.S.Cowan, Luetzelburgia sotoi D.B.O.S.Cardoso, L.P.Queiroz & H.C.Lima, Swartzia
macrostachya Benth., Trischidium molle (Benth.) H.E.Ireland, and Vatairea guianensis Aubl.] Alan Cressler [Cladrastis kentukea (Dum.Cours.) Rudd], Vinícius Dittrich (Hymenolobium
alagoanum Ducke), and Gustavo Shimizu (Zollernia ilicifolia Vogel).
63D. Cardoso et al. / South African Journal of Botany 89 (2013) 58–75

Earliest-branching papilionoid clades
We have identified 26 morphologically disparate and mostly
species-poor woody genera, traditionally classified into the tribes
Swartzieae, Sophoreae, and Dipterygeae, as comprising the first-
branching papilionoids. They fall into three strongly supported line-
ages, a large ADA clade of morphologically eclectic genera, which is
weakly supported as sister to all remaining papilionoids, the newly
Podalyrieae
Ormosieae
Crotalarieae
Brongniartieae
Genisteae
Leptolobieae
Ormosia
Poecilanthe falcata GQ246155
Ormosia smithii JX295954
Crotalaria incana GQ246141
Templetonia retusa GQ246158
Ormosia macrocalyx GQ982056
Poecilanthe subcordata GQ246156
Spirotropis longifolia JX295948
Diplotropis purpurea JX124418
Lupinus texensis JQ619989
Argyrolobium velutinum JQ412199
Amphiodon effusus JX295892
Lupinus cosentinii AY386943
Templetonia hookeri GQ246157
Calpurnia aurea AY386951
Ormosia sp. nov. JX295945
Sophora microphylla JQ619976
Sophora davidii AY386958
Piptanthus nepalensis AY386924
Staminodianthus racemosus JX124420
Harpalyce formosa GQ246154
Diplotropis brasiliensis AY386939
Ormosia henryi HM049514
Ormosia krugii HM446725
Clathrotropis nitida JX295951
Cyclolobium brasiliense GQ246152
Thermopsis lanceolata JQ669595
Baptisia australis AY386900
Ammopiptanthus mongolicus JQ820169
Crotalaria pumila AY386867
Dicraeopetalum stipulare GQ246142
Camoensia brevicalyx JX295946
Ormosia costulata JX295887
Diplotropis triloba JX124398
Leptolobium dasycarpum JX124408
Anarthrophyllum desideratum AY386923
Tabaroa caatingicola GQ246162
Spirotropis longifolia JX295950
Laburnum anagyroides HE967423
Diplotropis incexis JX124401
Cytisus scoparius AY386902
Leptolobium bijugum JX124404
Brongniartia peninsularis GQ246148
Leptolobium elegans JX124410
Lupinus sparsiflorus JQ619990
Genista monspessulana AY386862
Bolusanthus speciosus AF142685
Diplotropis martiusii AY386938
Ormosia excelsa JX295884
Crotalaria saltiana JQ619981
Lupinus argenteus AY386956
Ormosia sp. nov. JX295877
Ormosia arborea JX295939
Sophora stenophylla JQ669580
Staminodianthus duckei JX124405
Spirotropis longifolia JX295949
Thermopsis rhombifolia AY386866
Ammodendron argenteum AY386957
Cyclolobium nutans AF142686
Plagiocarpus axillaris GQ246160
Crotalaria juncea JQ619982
Bowdichia virgiloides AY386937
Camoensia scandens JX295919
Ormosia stipularis JX295882
Lupinus odoratus EU025914
Ormosia paraensis JX295888
Ulex europaeus JQ669586
Ormosia semicastrata HQ415280
Bowdichia nitida JX124395
Ammopiptanthus nanus JQ820170
Diplotropis ferruginea JX124397
Sophora macrocarpa JQ619975
Sophora nuttalliana AY386865
Leptolobium panamense AF142684
Ormosia formosana AF142682
Tabaroa caatingicola GQ246161
Ormosia colombiana AY386960
Ormosia coutinhoi JX295880
Ormosia coccinea GQ982055
Euchlora hirsuta JQ041113
Hovea purpurea AY386889
Bolusia amboensis JQ040984
Ormosia timboensis JX295878
Guianodendron praeclarum JX124403
Aspalathus pinguis JQ412203
Panurea longifolia JX295947
Ormosia fastigiata JX295941
Rafnia angulata JQ412281
Ormosia nitida JX295881
Dichilus lebeckioides GQ246143
Staminodianthus rosae JX124396
Poecilanthe parviflora AF142687
Ormosia bahiensis JX295886
Maackia amurensis AY386944
Harpalyce brasiliana GQ246153
Ormosia fordiana HQ415278
Clathrotropis macrocarpa JX295930
Leptolobium brachystachyum JX124407
Spartium junceum AY386901
Leptolobium parvifolium JX124411
Guianodendron praeclarum JX124402
Ormosia glaberrima HQ415279
Ormosia limae JX295879
Harpalyce arborescens AF142689
Lebeckia sericea GQ246144
Ormosia aff. fastigiata JX295885
Lamprolobium fruiticosum GQ246159
Leptolobium tenuifolium JX124413
Ormosia aff. bahiensis JX295944
Thermopsis alpina JQ669594
Cadia purpurea JX295932
Brongniartia alamosana AF142688
Leptolobium nitens JX124409
96
69
96
95
87
91
98
91
98
81
96
69
95
87
50-kb inversion clade
0.1 changes
Sophoreae
Camoensieae
Sophora
Camoensia
Cadia
Crotalaria
Genistoids s.l.
Core Genistoids
New genus
Dermatophyllum secundiflorum AF142693
Dermatophyllum arizonicum AY386864
Dermatophyllum
Lupinus
Spirotropis
Bowdichia
Tabaroa
Harpalyce
Leptolobium
Fig. 4. Continuation of the matK Bayesian majority-rule consensus tree of the early-branching papilionoids. This portion shows the large Genistoid s.l. clade and its putative related, yet
unresolved genus Dermatophyllum.SeeFig. 2 for details. Photos: Domingos Cardoso [Bowdichia virgilioides Kunth, Camoensia scandens (Welw.) J.B.Gillett, Crotalaria maypurensis Kunth,
Harpalyce lanata L.P.Queiroz, Leptolobium dasycarpum Vogel, Lupinus sericeus Pursh, Ormosia sp. nov., and Sophora tomentosa L.], Émile Fonty [Spirotropis longifolia (DC.) Baill.], Mark Olson
(Cadia purpurea Forssk.), Luciano P. de Queiroz (Tabaroa caatingicola L.P.Queiroz, G.P.Lewis & M.F.Wojc.), and Martin Wojciechowski [Dermatophyllum secundiflorum (Ortega) Gandhi & Reveal].
64 D. Cardoso et al. / South African Journal of Botany 89 (2013) 58–75

recircumscribed Swartzieae, and the Cladrastis clade (Figs. 1–3;Table 1).
All earliest-branching genera that have been screened for the 50-kb in-
version in the plastid DNA genome lack this feature (Doyle et al.,
1996). Our analysis is consistent with previous results (Wojciechowski
et al., 2004; McMahon and Sanderson, 2006; Cardoso et al., 2012a;
LPWG, 2013) in that the Cladrastis clade is strongly resolved as sister
Amorpheae
Baphieae
50-kb inversion clade
0.1 changes
Dalbergieae
Poiretia angustifolia AF270864
Baphiopsis parviflora JX295895
Riedeliella graciliflora AH009910
Amorpha fruticosa AY391785
Dalea lanata AY391790
Zornia sp. AF203584
Baphia madagascariensis AY553718
Errazurizia megacarpa AY391804
Dalea cliffortiana AY391787
Dalea scandens AY391800
Dalea hospes AY391789
Dalea brachystachya EU025886
Psorothamnus arborescens AY391814
Fissicalyx fendleri AF272063
Geoffroea spinosa AF270879
Cascaronia astragalina AF272072
Cyclocarpa stellaris AF272067
Kotschya ochreata AF272065
Discolobium psoraleifolium AF270874
Maraniona lavinii AY247263
Amorpha apiculata AY391784
Ormocarpum keniense AF203602
Nissolia hirsuta AF270868
Weberbauerella brongniartioides AF272075
Fiebrigiella gracilis AF203590
Psorothamnus emoryi AY391815
Acosmium lentiscifolium JX124417
Dalbergia congestiflora AF142696
Dalea lumholtzii AY391791
Cranocarpus martii AF270875
Adesmia lanata AF270863
Brya ebenus AF270876
Diphysa floribunda AF203575
Stylosanthes capitata AF203595
Bryaspis lupulina AF272068
Parryella filifolia AY391812
Grazielodendron riodocense AF270862
Centrolobium robustum EU401414
Eysenhardtia polystachya EU025905
Marina parryi AY386859
Acosmium diffusissimum JX124415
Machaerium capote AF142692
Paramachaerium schomburgkii AF272062
Dalea neomexicana AY391795
Platypodium elegans AF270877
Eysenhardtia orthocarpa AY386909
Amicia glandulosa AF203583
Baphia leptobotrys EU361865
Airyantha schweinfurthii JX295897
Steinbachiella leptoclada JQ710653
Aeschynomene purpusii AF270870
Errazurizia benthamii AY391803
Baphiastrum brachycarpum JX295864
Dalea purpurea AY391798
Arachis pintoi AF203596
Tipuana tipu AF270882
Ramorinoa girolae AF270881
Bowringia mildbraedii JX295865
Smithia ciliata AF272066
Baphia nitida EU361867
Pictetia marginata AF203578
Zygocarpum yemenense AF203573
Chapmannia gracilis AF203592
Chaetocalyx scandens AF270865
Psorothamnus polydenius AY391819
Inocarpus fagifer AF270878
Acosmium cardenasii JX124425
Dalea pulchra AY386860
Dalea pogonathera AY391796
Soemmeringia semperflorens AF272088
Dalea mollissima AY391794
Apoplanesia paniculata AF270860
Baphia massaiensis AF142683
Eysenhardtia texana AY391807
Platymiscium stipulare AF270872
Etaballia guianensis AF272074
Psorothamnus fremontii AY391817
Ormocarpopsis itremoensis AF203567
Humularia corbisieri AF272069
Psorothamnus scoparius AY391821
Psorothamnus spinosus AY391822
Pterocarpus indicus AF142691
Marina scopa AY391811
Aeschynomene indica AF272084
93
96
98
98
95
94
83
97
NPAAA clade
IR-Lacking clade
Robinioids
Mirbelioids
Dalbergia
Platymiscium
Amorpha
Inocarpus
Millettioids
Baphia
Dalbergioids s.l.
Adesmia
clade
Dalbergia
clade
Pterocarpus
clade
Amorpha
clade
Dalea
clade
Hologalegina
Fig. 5. Continuation of the matK Bayesianmajority-rule consensus tree of the early-branchingpapilionoids. This portion shows relationships and generic composition of the Amorpheae,
Dalbergieae, Baphieae,and the remaining papilionoids within the large non-protein–amino-acid-accumulating(NPAAA) clade. See Fig. 2 for details. Photos:Domingos Cardoso [Dalbergia
ecastaphyllum (L.) Taub.and Platymiscium floribundum Vogel], Thomas Palmer (Amorpha fruticosa L.), Gerald Carr (Inocarpus edulisJ.R.Forst. & G.Forst.), and Mark Hydeand Bart Wursten
(Baphia massaiensis Taub., available at www.zimbabweflora.co.zw).
65D. Cardoso et al. / South African Journal of Botany 89 (2013) 58–75

Table 1
The early-branching clades of papilionoid legumes and constituent genera as recog-
nized in the present study. Estimated numbers of species diversity (from Lewis et al.,
2005 and augmented from our review of recent literature) are provided. Genera
marked by an asterisk (*) were not sampled in any matK phylogeny, but for which
there is information from other molecular markers (e.g., ITS, rbcL or trnL intron). Gen-
era marked by two asterisks (**) were never sampled in a molecular phylogeny, but for
which the morphology and chemistry may tentatively suggest their phylogenetic posi-
tion. The plus sign (
+
) highlights the non-monophyletic genera as suggested by prelim-
inary molecular evidences discussed in the text.
Clade/Genus No. spp.
ADA clade Angylocalyceae 21
Alexa 9
Angylocalyx 7
Castanospermum 1
Uleanthus** 1
Xanthocercis 3
Dipterygeae 25
Dipteryx 12
Monopteryx 3
Pterodon 3
Taralea 7
Amburaneae 29
Amburana 2
Cordyla 7
Dussia 9
Mildbraediodendron* 1
Myrocarpus+5
Myrospermum 2
Myroxylon 3
Swartzieae 213
Ateleia 20
Bobgunnia 2
Bocoa 3
Candolleodendron 1
Cyathostegia 1
Fairchildia* 1
Swartzia 180
Trischidium 5
Cladrastis clade 17
Cladrastis+7
Styphnolobium 9
Pickeringia 1
Exostyleae 21
Exostyles 4
Harleyodendron 1
Holocalyx 1
Lecointea 4
Uribea 1
Zollernia 10
Vataireoid clade 27
Luetzelburgia 13
Sweetia 1
Vatairea 9
Vataireopsis 4
Andira clade 46
Andira 29
Hymenolobium 17
Genistoids s.l. Ormosieae 139
Clathrotropis 2
Haplormosia** 1
Ormosia 130
Panurea 2
Petaladenium** 1
Spirotropis 3
Brongniartieae 153
Amphiodon 2
Brongniartia 63
Cristonia* 1
Cyclolobium 1
Harpalyce 25
Hovea 37
Lamprolobium 2
Plagiocarpus 1
Poecilanthe 7
Tabaroa 1
Templetonia 10
Thinicola* 1
New genusa2
Leptolobieae 29
Bowdichia 2
Diplotropis 10
Guianodendron 1
Leptolobium 13
Staminodianthus
b
3
Camoensieae 2
Camoensia 2
Core Genistoids
Sophoreae 122
Ammodendron 5
Ammopiptanthus 2
Ammothamnus** 2
Anagyris* 2
Baptisia 17
Bolusanthus 1
Dicrae opetalum 3
Euchresta* 4
Maackia 8
Piptanthus 2
Platycelyphium* 1
Salweenia* 2
Sophora
+
50
Thermopsis
+
23
Podalyrieae 130
Amphithalea* 42
Cadia 7
Calpurnia 7
Cyclopia* 23
Liparia
+
*20
Podalyria* 17
Stirtonanthus* 3
Virgilia* 2
Xiphoteca* 9
Crotalarieae 1221
Aspalathus 280
Bolusia 5
Calobota* 16
Crotalaria 700
Euchlora 1
Ezoloba* 1
Lebeckia* 14
Leobordea* 51
Listia* 7
Lotononis* 91
Pearsonia* 13
Rafnia 19
Robynsiophyton* 1
Rothia* 2
Wiborgia* 10
Wiborgiella* 10
Genisteae 618
Adenocarpus* 15
Anarthrophyllum 15
Argyrocytisus* 1
Argyrolobium
+
80
Calicotome* 3
Cytisophyllum* 1
Cytisus 65
Dichilus 5
Echinospartum* 5
Erinacea* 1
Genista
+
90
Gonocytisus* 3
Hesperolaburnum* 1
Laburnum 2
Lembotropis* 2
Lupinus 275
Melolobium* 15
Petteria* 1
Podocytisus* 1
Polhillia* 8
Retama* 4
Sellocharis* 1
Clade/Genus No. spp.
Genistoids s.l.
Table 1 (continued)
66 D. Cardoso et al. / South African Journal of Botany 89 (2013) 58–75

to a well-supported 50-kb inversion clade (Figs. 1–3). This clade is
marked by a structural rearrangement within the large single copy re-
gion of the plastid genome (Doyle et al., 1996)andincludesthebulk
of Papilionoideae (LPWG, 2013).
The Angylocalyceae clade
The Angylocalyceae includes ca. 21 species and five genera (Fig. 2;
Table 1), but the putatively related monospecific Amazonian genus
Uleanthus remains to be studied further. Although we were not able
to generate DNA sequences of Uleanthus,floral and pod morphologies
suggest it might well belong here (Yakovlev, 1972; Povydysh et al.,
2011). This clade is strongly marked by an ornithophilous floral
syndrome in which the calyx and hypanthium are enlarged, the petals
thickened and often red or orange, the standard often distinctly large,
the lower petals undifferentiated or sometimes highly reduced, and the
stamens and gynoecium exserted. The mostly white flowers of Alexa,
however, have also been reported to be pollinated by phyllostomatid
bats (Ramirez, 1995). The Angylocalyceae is bi ogeographically inter-
esting for studies of long-distance dispersal as its constituent gen-
era are widely disjunct: Angylocalyx Taub. and Xanthocercis Baill.
occur in Africa and Madagascar, the monospecificCastanospermum
A.Cunn. ex Hook. is endemic to Australia, and Alexa and Uleanthus
are distributed only in the northern South American rain forests
(Pennington et al., 2005).
The Dipterygeae clade
This is an exclusively Neotropical clade of ca. 25 woody species
in four genera (Fig. 2;Table 1), of which Dipteryx Schreb., Pterodon
Vogel, and Taralea Aubl. have consistently appeared in the same clade
(Pennington et al., 2001; Wojciechowski et al., 2004). The morphologi-
cally disparate Monopteryx Spruce ex Benth. waspreviously classified in
Sophoreae (Polhill, 1981a), but the matK and trnL intron phylogenies of
Cardoso et al. (2012a) resolved the genus as sister to the rest of the
Dipterygeae. The non-papilionate flowers of Monopteryx, in which the
wing petals are much reduced and the keel petals are connate and
open out exposing the free stamens, greatly contrasts with the truly
papilionate flowers with fused stamens of the other Dipterygeae
genera (Fig. 2). Despite the contrasting petal morphology, a synapo-
morphy of the Dipterygeae that encompasses Monopteryx is an unusual
two-lipped calyx in which the two upper lobes are much enlarged and
the three lower lobes are reduced to small teeth (Polhill, 1981a, 1981b).
The two upper enlarged lobes of Dipteryx,Pterodon,andTaralea are petal-
oid and completely free to their base so that they resemble additional lat-
eral wing petals. In Monopteryx theupperlobesareconnateandassumea
standard-like position. The monophyly and inter-relationships of the
Dipterygeae genera are also strongly supported by floral and fruit traits
(Cardoso et al., 2012a).
Stauracanthus* 3
Ulex 20
Unresolved Genistoids
Dermatophyllum 4
Neoharmsia** 2
Pericopsis* 4
Sakoanala** 2
New genus
c
5
Dalbergioids s.l. Amorpheae 247
Amorpha 15
Apoplanesia 1
Dalea 165
Errazurizia 3
Eysenhardtia 15
Marina 38
Parryella 1
Psorothamnus
+
9
Dalbergieae 1367
Adesmia clade
Adesmia 240
Amicia 6
Chaetocalyx 13
Nissolia 13
Poiretia 11
Zornia 75
Dalbergia clade
Aeschynomene
+
250
Bryaspis 2
Cyclocarpa 1
Dalbergia 250
Diphysa 14
Geissaspis* 2
Humularia 35
Kotschya 31
Machaerium 130
Ormocarpopsis 8
Ormocarpum 18
Pictetia 8
Smithia 20
Soemmeringia 1
Steinbachiella 1
Weberbauerella 2
Zygocarpum 6
Pterocarpus clade
Acosmium 3
Arachis 69
Brya 4
Cascaronia 1
Centrolobium 7
Chapmannia 7
Cranocarpus 3
Discolobium 8
Etaballia 1
Fiebrigiella 1
Fissicalyx 1
Geoffroea 2
Grazielodendron 1
Inocarpus 3
Maraniona 1
Paramachaerium 5
Platymiscium 19
Platypodium 2
Pterocarpus+40
Ramorinoa 1
Riedeliella 3
Stylosanthes 48
Tipuana 1
Baphieae 57
Airyantha 2
Baphia
+
47
Spartium 1
Clade/Genus No. spp.
Genistoids s.l.
Bowringia 4
Dalhousiea* 3
Leucomphalos** 1
Unresolved genera
Aldina 22
Amphimas 4
Baphiastrum 1
1
No. spp.
Baphiopsis
Clade/Genus
a
New genus to accommodate two Amazonian mostly unifoliolate species from
Poecilanthe s.l. (J.E. Meireles, unpubl.).
b
Segregated genus from within Diplotropis s.l. to accommodate D. sect. Racemosae
(Cardoso et al., 2012a; 2013b).
c
New genus to accommodate Clathrotropis macrocarpa and related species with large
elastically dehiscent pods mostly with thickened and dilated upper sutures (Cardoso
et al., 2012a; D. Cardoso, unpubl.).
Table 1 (continued)Table 1 (continued)
67D. Cardoso et al. / South African Journal of Botany 89 (2013) 58–75

The Amburaneae clade
This is a mostly Neotropical clade comprising ca. 29 species and
seven morphologically eclectic genera in terms of floral morphology
(Fig. 2;Table 1). Dussia Krug & Urb. ex Taub. and Myrospermum Jacq.
have strongly differentiated papilionate flowers, while Myroxylon L.f.
has a well-differentiated standard, but the remaining petals are undif-
ferentiated and much reduced. Myrocarpus Allemão has radially
symmetrical, mimosoid-like flowers, whereas Amburana Schwacke &
Taub. has only one petal and a long hypanthium (Fig. 2). The African
genera Cordyla Lour. and Mildbraediodendron have a swartzioid-like
floral morphology in which the flowers have an entire calyx, no petals,
and numerous exserted stamens. The Amburaneae has been unresolved
or only poorly supported in phylogenetic analyses of individual molec-
ular data (e.g., Doyle et al., 1997; Pennington et al., 2001; Cardoso et al.,
2012a), but itsmonophyly was better supported in the recentcombined
analysis of matK and trnL intron sequences (Cardoso et al., 2012a). We
have added a few more taxa in the present matK analysis to challenge
the monophyly of Amburaneae, which was maintained, yet with poor
support (Fig. 2). We suggest recognizing Amburaneae as a new mono-
phyletic tribe of the Papilionoideae because the poor support is only
from a weak phylogenetic signal, not a strongly conflicting one. Branch
lengths are short for most internodes that separate the three main
ADA lineages (Fig. 2). Despite the lack of a clear non-molecular syn-
apomorphyfortheAmburaneaeandthehighleveloffloral diversity,
resin chemistry marks the monophyly of this clade. This includes the
production of balsams (Myrocarpus,Myrospermum,Myroxylon), cou-
marins (Amburana), abundant red resin from cut bark and twigs
(Dussia), and the glandular punctate leaves of several genera (Cordyla,
Mildbraediodendron,Myrocarpus,Myrospermum,Myroxylon). Some of
these features, however, are shared with genera of its sister Dipterygeae
clade (Pennington et al., 2001; Cardoso et al., 2012a).
The Swartzieae clade
The realignment of Swartzieae with the consistently resolved
Swartzioid clade (Ireland et al., 2000; Pennington et al., 2001;
Wojciechowski et al., 2004; Lavin et al., 2005; Torke and Schaal, 2008;
Cardoso et al., 2012a; LPWG, 2013) is necessary because the current
tribe (Cowan, 1981;seealsoIreland, 2005)ispolyphyletic.The
Swartzieae as here circumscribed comprises ca. 213 species and eight
genera, most of which are monospecific or weakly diversified (Fig. 3;
Table 1). Swartzia Schreb. is exceptional in this clade in being the most di-
verse and species-rich papilionoid genus of Neotropical rain forests
(Torke and Schaal, 2008). The non-papilionate swartzioid flowers are
largely characterized by a tendency to lack petals combined witha profu-
sion and elaboration of free stamens (Fig. 3). The relationships and mono-
phyly of each of the constituent genera of this clade were better resolved
in the comprehensive combined phylogeny of Torke and Schaal (2008).
The present matK analysis included most Swartzieae genera, except for
the re-established monospecificFairchildia (Torke and Schaal, 2008),
and recovered two well-supported subclades with contrasting internal
resolution and ecological structuring. The Swartzia clade comprises most-
ly Neotropical genera and the African Bobgunnia J.H.Kirkbr. & Wiersema,
all with a strong ecological predilection to lowland rain forests (Ireland,
2005; Schrire et al., 2005; Torke and Schaal, 2008). This subclade was
however resolved as a polytomy (Fig. 3). The Ateleia clade was strongly
resolved and ecologically concentrated in Neotropical seasonally dry
woodlands (Schrire et al., 2005; Ireland, 2007; Ireland et al., 2010;
Pennington et al., 2010). The highly resolved Ateleioid phylogeny repre-
sents a common pattern in legumes with predilection to the succulent
biome (e.g., Pennington et al., 2009, 2010; de Queiroz and Lavin,
2011; Särkinen et al., 2012),which contrasts to the low resolution with-
in the Swartzia clade and which is taken as evidence of rapid and recent
diversification of the constituent genera expected for rain forest
legumes (e.g., Richardson et al., 2001; Pennington et al., 2009).
The Cladrastis clade
The monophyly and inter-relationships of the Cladrastis clade have
been consistently resolved in all molecular phylogenies (Figs. 1, 3;
Wojciechowski et al., 2004; McMahon and Sanderson, 2006; LPWG,
2013; Cardoso et al., 2012a; Wojciechowski, 2013). The clade com-
prises 17 species in the papilionate-flowered genera Cladrastis Raf.
and Styphnolobium Schott, which are disjunctly distributed in East
Asia and North America, and the monospecific Californian chaparral
endemic Pickeringia Nutt. ex Torr. & A.Gray (Wojciechowski et al.,
2004; Wojciechowski, 2013). Both Pickeringia and Styphnolobium are
individually strongly supported as monophyletic and nested within a
paraphyletic Cladrastis (Fig. 3;Wojciechowski, 2013). The disjunct
distribution of members of the clade in warm temperate to tropical
regions of the Northern Hemisphere is a pattern common to many
other legume genera, including the caesalpinioids Gleditsia L. and
Gymnocladus Lam., as well as the species-rich papilionoids Astragalus
L. and Oxytropis DC. (Schrire et al., 2005).
The Exostyleae clade
The Exostyleae corresponds to the Lecointeoid clade, first identi-
fied by morphological cladistic analysis (Herendeen, 1995) and later
confirmed by molecular data (Fig. 3;Mansano et al., 2004; Cardoso
et al., 2012a; LPWG, 2013). It is an exclusively Neotropical clade
of ca. 21 woody species and six genera mostly from tropical rain
forests. The non-papilionate Exostyleae flowers vary from truly radial-
ly symmetrical in most genera (Lecointea Ducke, Exostyles Schott,
Harleyodendron R.S.Cowan, and Holocalyx Micheli) to bilaterally
symmetrical in Zollernia Wied-Neuw. & Nees and Uribea Dugand &
Romero. Likely synapomorphic morphological features for the Exostyleae
are the serrate and sometimes spinescent leaflet or leaf margins, basifixed
anthers, and drupaceous fruits (Herendeen, 1995; Mansano et al., 2004).
The clade also shows a tendency towards unifoliolate or simple leaves
(Mansano et al., 2004).Additionally,thesetaxasharesomeuniquetraits
in wood anatomy (Gasson, 1996; Gasson and Webley, 1999)andfloral
ontogeny (Mansano et al., 2002). The ecological predilection and lack
of resolution within the Exostyleae (Fig. 3) mirrors the phylogenetic
pattern described for the predominantly rain forest-inhabiting
Swartzia clade. Other sources of molecular data may help to resolve
generic relationships within Exostyleae, although it is clear that the
trnL intron also does not provide sufficient resolution (Mansano
et al., 2002). A resolved phylogeny for the Exostyleae would be help-
ful to investigate the evolution of floral symmetry within this inter-
esting early-branching clade.
The Vataireoid clade
The Vataireoids comprise ca. 27 woody species from the Neotropi-
cal genera Luetzelburgia Harms, Vatairea Aubl., Vataireopsis Ducke, and
the monospecificSweetia Spreng. (Fig. 3). The monophyly and internal
relationships of the Vataireoid clade were strongly supported in
a comprehensive seven-gene phylogeny (Cardoso et al., 2013a). An in-
teresting result stemming from that study included the evidence of in-
dependent evolution of the undifferentiated, non-papilionate flowers
of Sweetia and Luetzelburgia, both traditionally classified in Sophoreae
(Polhill, 1981a). The Vataireoid clade is synapomorphically diagnos-
able by, among other characters, the highly congested leaves at the
distal ends of fascicled branches and the samara-like fruit with
a long distal wing arising from a basal seed-chamber (Cardoso et al.,
2013a). The unusual small lateral wing attached to each side of the
seed-chamber in most Vataireoids is closely similar only to the
single-seeded pods of the South African Cape genus Wiborgia of
Crotalarieae (Boatwright et al., 2008b). The sister-group relationship
of the Vataireoids in the context of the Papilionoideae phylogeny re-
mains unclear (Figs.1,3;Cardoso et al., 2012a). Lavin et al. (2005)
68 D. Cardoso et al. / South African Journal of Botany 89 (2013) 58–75

found representatives of the Exostyleae as a weakly supported sister to
the Vataireoids. These two early-branching clades have many species un-
usually marked by leaves or leaflets with non-entire margins (Cardoso
et al., 2013a). The congested leaves at the distal branch ends characterize
not only the Vataireoids but also several species of Hymenolobium Benth.
and Andira Lam. of the Andira clade. Despite the many similarities of the
Vataireoids with other early-branching clades, all phylogenetic studies,
not just the present one, did not resolve the sister relationship of the
Vataireoid clade among the other main eight lineages of the 50-kb inver-
sion clade.
The Andira clade
This clade includes ca. 46 species of predominantly Neotropical
rain forest trees in the genera Andira and Hymenolobium (Fig. 3). The
close relationship of these genera is suggested by their similar floral,
vegetative, and root nodule morphologies, which include the mostly
fascicled leaves and densely flowered paniculate inflorescences at dis-
tal branch ends, and the truly papilionate flowers involving petal dif-
ferentiation and stamen connation (Pennington, 1995, 2003). The
monophyly of both genera has been strongly supported by phyloge-
netic analyses of restriction sites and nrDNA ITS and plastid sequence
data (Pennington, 1995; Simon et al., 2009; Cardoso et al., 2012a)and
is further supported by the drupaceous fruits of Andira that greatly con-
trasts with the laterally compressed samaras of Hymenolobium.The
Andira clade has remained unresolved within the 50-kb inversion
clade in all broad-level phylogenies of Papilionoideae (e.g., Doyle
et al., 1997; Pennington et al., 2001; Wojciechowski et al., 2004;
Cardoso et al., 2012a; LPWG, 2013). Wojciechowski et al. (2004)
found only a very weakly supported sister relationship of the Andira
clade and Dalbergioids s.l. Indeed, mostly because of their indehiscent
fruits Andira and Hymenolobium were long classified in the Dalbergieae
(Polhill, 1981c, 1994; de Lima, 1990).
The Genistoid s.l. clade
The Genistoids s.l. are the most species-rich early-branching clade
with over 2400 species (Table 1;Fig. 4). This clade was defined by
Wojciechowski et al. (2004) and expanded by Cardoso et al. (2012a) to
include a strongly supported Ormosia clade, which is here proposed to
accommodate the resurrected tribe Ormosieae. The Genistoid s.l. clade
includes the many papilionate-flowered genera from within the pre-
dominantly Southern Hemisphere tribes Brongniartieae, Crotalarieae,
Genisteae, Podalyrieae, the recircumscribed Sophoreae, and the resurrected
Camoensieae and Leptolobieae, in addition to Ormosieae. Genera also
exhibiting radial floral symmetry and undifferentiated petals or free sta-
mens, hitherto considered typical of the traditional circumscription of
Sophoreae (Polhill, 1981a), are found dispersed across the clade. The
Genistoid legumes are largely known to accumulate quinolizidine alkaloids
(e.g., Hatfield et al., 1980; Waterman and Faulkner, 1982; Kinghorn et al.,
1988; Ricker et al., 1994, 1999; Greinwald et al., 1995, 1996; Veitch et al.,
1997; Van Wyk, 2003; Wink and Mohamed, 2003; Kite et al., 2013), al-
though there exist examples of pyrrolizidine alkaloid-bearing genera [e.g.,
Crotalaria L., Laburnum Fabr., Lotononis (DC.) Eckl. & Zeyh., Pericopsis;Van
Wyk, 2003; Wink and Mohamed, 2003] or taxa exhibiting a total absence
of alkaloids (e.g., Cyclopia Vent.; Boatwright et al., 2008a). Relationships
within the Genistoids s.l. are generally well resolved, except for the
placement of Dermatophyllum,Neoharmsia,Pericopsis,Sakoanala,and
an undescribed new genus, as well as the relationships between
Brongniartieae, Leptolobieae, and Core Genistoids (Fig. 4).
The early-branching-genistoid Ormosieae clade
The Ormosieae is sister to the rest of theGenistoids s.l. and includes
six genera and ca. 138 species, of which the genus Ormosia Jacks. alone
accounts for ca. 130 species (Fig. 4;Table 1). The Ormosieae has mainly
diversified in Neotropical rain forests of the Amazon basin, but the larg-
est genus Ormosia also shows diversity in southeast Asia and northern
Australia (Rudd, 1965; Pennington et al., 2005). The few Asian species
of Ormosia (Ormosia formosana Kaneh., Ormosia fordiana Oliv., Ormosia
glaberrima Y.C.Wu, Ormosia henryi Prain, and Ormosia semicastrata
Hance) newly included in this study suggest the monophyly of the
genus (Fig. 4). A robust generic circumscription within Ormosieae
requires additional sampling of the morphological diversity of Ormosia
(Rudd, 1965) and of the potentially related monospecificgenera
Haplormosia and Petaladenium. The African Haplormosia,unusually
marked by simples leaves, and the enigmatic Petaladenium from Brazilian
Amazonia have strong morphological ties to Ormosieae but they have
never been sampled in any molecular phylogenies (Table 1;Pennington
et al., 2005; Cardoso et al., 2012a). In addition to producing quinolizidine
alkaloids (Kinghorn et al., 1988), Haplormosia is very similar to Ormosia
with respect to floral and pod morphology and shares the simple leaves
with Panurea Spruce ex Benth. & Hook.f. Petaladenium is distinctive
among Papilionoideae in having fimbriate-glandular wing petals, but its
overall vegetative and inflorescence morphology suggests some affinity
to Ormosia, whereas the linear-oblong dehiscent pods are similar to
Panurea and Spirotropis. Perhaps the clearest synapomorphy of Ormosieae
as circumscribed here (to also include Petaladenium and Haplormosia)is
the mostly dehiscent pods with woody valves.
The genistoid Brongniartieae clade
The Brongniartieae includes ca. 153 species and 13 genera (Table 1),
among which the Neotropical Harpalyce D.Don is perhaps the most un-
usual because of the peltate glands and resupinate flowers with strong-
ly bilabiate calyx and mostly helically contorted keel (Fig. 4). Three
genera have been added after the latest circumscription of the tribe by
Ross and Crisp (2005): the monospecificTabaroa L.P.Queiroz, G.P.Lewis
& M.F.Wojc. from the Brazilian Caatinga dry woodlands (de Queiroz
et al., 2010), Amphiodon from the non-flooded Amazonian forest
(Cardoso et al., 2012a; J.E. Meireles, unpubl.), and a new Amazonian
genus with mostly unifoliolate leaves yet to be segregated from
Poecilanthe s.l. (J.E. Meireles, unpubl.). Brongniartieae has been tradi-
tionally diagnosed by the dimorphic anthers that are alternately
basifixed and dorsifixed. However, dimorphic anthers are also found
variously among African Crotalarieae, Podalyrieae, and Genisteae of
the Core Genistoids (Polhill, 1976). Phylogenetic analyses of matK se-
quences have consistently resolved all Australian genera (Hovea R.Br.,
Lamprolobium Benth., Plagiocarpus Benth., Templetonia R.Br.) nested
within a paraphyletic group of American genera (Fig. 4;seealsode
Queiroz et al., 2010), in contrast with the results derived from ITS
sequences, which did not resolve a clade of Australian genera
(Thompson et al., 2001). A putative morphological synapomorphy for
the Australian Brongniartieae clade is the simple or unifoliolate leaves,
but this feature has also evolved independently in the Neotropical
Cyclolobium Benth., Poecilanthe s.s., and the new segregate genus
from Poecilanthe s.l. (J.E. Meireles, unpubl.; H.C. de Lima, pers. comm.).
Generic relationships within Brongniartieae have also been strongly
supported by individual analysis of matK data (Fig. 4;de Queiroz et al.,
2010), except for Templetonia and the remaining Australian genera.
Thompson et al. (2001) however found a strongly supported sister
relationship between Templetonia and Hovea. The Australian genera
Cristonia J.H.Ross with unusual features such as simple leaves that
are distinctly bilobed apically and two upper calyx lobes that are
united into a truncate limb, and Thinicola J.H.Ross with dense silvery
indumentum, foliaceous stipules, and ornithophilous flowers, were
not sampled in the present matK phylogeny, but they have been
resolved close to Lamprolobium in the ITS phylogeny (Thompson et al.,
2001). Most Brongniartieae genera are not only clearly distinguished
based on molecular data, but also on exclusive morphological features
(Ross and Crisp, 2005; de Queiroz et al., 2010).
69D. Cardoso et al. / South African Journal of Botany 89 (2013) 58–75

The genistoid Leptolobieae clade
The resurrection of tribe Leptolobieae (Fig. 4;Table 1) should cor-
respond to the recently recognized Bowdichia clade, which includes
the papilionate-flowered Bowdichia Kunth, Diplotropis Benth., and
Staminodianthus D.B.O.S.Cardoso, H.C.Lima & L.P.Queiroz gen. nov. ined.,
and the nearly-radial-flowered Leptolobium Vogel and Guianodendron
Sch.Rodr. & A.M.G.Azevedo (Cardoso et al., 2012b, 2012c, 2013b). The
Leptolobieae includes ca. 29 species of trees mostly from tropical rain for-
ests and savannas of South America and only one species endemic to
Central America. Notable morphological synapomorphies of this clade
are the flowers with subequal and symmetric lower petals (wings and
keel), lateral petals (wings) without sculpturing, staminal filaments
free to the base, and compressed samaroid fruits with a narrow marginal
wing (Cardoso et al., 2012c). Within Leptolobieae, the non-homology of
traits involved in floral symmetry (Cardoso et al., 2012c)providesanex-
ample of the recurrent convergent floral evolution among the
early-branching papilionoids (Pennington et al., 2000; McMahon, 2005;
Cardoso et al., 2012b).
The genistoid Camoensieae clade
The Camoensieae includes only two species from the African genus
Camoensia. This is perhaps the strangest genus of Papilionoideae
because of its large flowers with a long hypanthium and free, weakly-
differentiated, crimped petals that expose the stamens (Fig. 4). The
distinctiveness of Camoensia also led Polhill (1981a) to classify the
genus separately in its own group in Sophoreae. The phylogenetic
position of Camoensia was only recently clarified in the matK phy-
logeny of Cardoso et al. (2012a). That study resolved the genus as
sister to a strongly supported clade comprising the Core Genistoid
lineages originally circumscribed by Crisp et al. (2000),aresult
also recovered in the present analysis, though only moderately
supported (Fig. 4).
The genistoid Sophoreae clade
The monophyletic Sophoreae as circumscribed here is greatly
narrowed to encompass ca. 122 species and 14 genera from a strong-
ly supported clade within the Core Genistoids (Fig. 4;Table 1). The
pantropical Sophora tomentosa L. with sea-drifted seeds is the most
widespread species, but members of Sophoreae are distributed vari-
ously in Mediterranean and temperate regions of North America, the
Mediterranean Basin, Africa, tropical regions of Australasia and the
Pacific, and western South America. Our new circumscription of
Sophoreae still includes the florally disparate Dicraeopetalum Harms
marked by radially-symmetrical flowers and embraces the currently
recognized tribes Thermopsideae and the monotypic Euchresteae
(Lock, 2005; Ohashi, 2005). Free stamens, the hallmark morphology of
Sophoreae, also characterize the Thermopsideae. If Thermopsideae and
Euchresteae have to be maintained, new tribes would have to be created
for some taxonomically small clades of genera traditionally classified in
Sophoreae (Fig. 4) and even the non-monophyletic Thermopsideae
would have to be recircumscribed (Wang et al., 2006). We suggest a
more inclusive concept of Sophoreae, which is indeed an opinion shared
by others (e.g., Lock, 2005; Ohashi, 2005; Wang et al., 2006; LPWG, 2013).
The identification of morphological synapomorphies for a newly
circumscribed Sophoreae is yet to be further investigated.
We might have resolved the long standing taxonomic puzzle sur-
rounding the tribe Sophoreae, but the genus Sophora still reflects the
problems of the tribe and is not monophyletic. Even with the dismember-
ing of Sophora by the segregation of Styphnolobium and Dermatophyllum,
which fall in two disparate clades outside the Genistoids (Figs.3,4;
Cardoso et al., 2012a), the monophyly of Sophora still remains unclear
with respect to the genera Ammodendron Fisch. ex DC., Euchresta Benn.,
Maackia Rupr., and Salweenia (Fig. 5;Kajita et al., 2001). The genera
Euchresta and Salweenia were never evaluated in a matK phylogeny, but
phylogenetic analyses of other plastid genes have consistently placed
them close to Sophora (Kajita et al., 2001; Yue et al., 2011). The mysteri-
ous African Sophora inhambanensis Klotzsch, once thought to be closely
related to the Podalyrieae, was strongly resolved within Sophora by re-
cent phylogenetic analysis of ITS sequences (Boatwright and Van Wyk,
2011). The East Asian and North American disjunct Thermopsis is also
not monophyletic. Phylogenetic analysis of both matK and ITS sequences
suggests a geographical division between the Old World and New World
Thermopsis,buttheEastAsianThermopsis species are still poorly resolved
with respect to the genera Piptanthus Sweet and Anagyris L. (Fig. 4;Wang
et al., 2006).
The genistoid Podalyrieae clade
The monophyly and generic composition of the Podalyrieae were
defined in the comprehensive analysis of nrDNA ITS and rbcL
sequences of Boatwright et al. (2008a). This clade comprises ca. 130
species and nine genera (Table 1), within which the florally anoma-
lous genus Cadia has evolved, as also confirmed by analyses of matK
sequences (Fig. 4;Cardoso et al., 2012a). Despite Cadia being the
only genus with radially symmetrical flowers within a clade otherwise
largely marked by papilionate flowers, it indeed shares several charac-
ters with members of the Podalyrieae, including the imparipinnately
compound leaves, axillary racemose inflorescences, carboxylic acid es-
ters of quinolizidine alkaloids, and the isoflavone 3-hydroxydaidzein
as a major seed flavonoid (Van Wyk, 2003; Boatwright et al., 2008a).
Most Podalyrieae genera can be recognized by the combination of an
intrusive calyx base, weakly dimorphic anthers, and arillate seeds (Van
Wyk and Schutte, 1995). Together with the majority of Crotalarieae gen-
era (e.g., Aspalathus and Rafnia), the Podalyrieae is among the oldest radi-
ations of the Cape floral clades largely endemic to the mountain fynbos of
South Africa (Edwards and Hawkins, 2007).
The genistoid Crotalarieae clade
The Crotalarieae is mostly endemic to Africa and by far the largest
subclade within the Genistoids s.l., with ca. 1221 species and 16 gen-
era. Over 80% of the species diversity of Crotalarieae comes from only
two genera, Crotalaria and Aspalathus (Table 1). All Crotalarieae genera
bear the typical papilionate flowers, but Bolusia has more elaborate re-
supinate flowers with the keel helically coiled through several turns
(Polhill, 1976; Le Roux and Van Wyk, 2012). The re-circumscription of
the Crotalarieae and the transfer of Argyrolobium,Dichilus,Melolobium
Eckl. & Zeyh., and Polhillia C.H.Stirt. to the tribe Genisteae (Van Wyk
and Schutte, 1995) agree with the complete generic phylogeny of
the tribe Crotalarieae (Boatwright et al., 2008b), which has led to ongo-
ing taxonomic revision and delimitation of all Crotalarieae genera
(Boatwright et al., 2008c; Boatwright and Van Wyk, 2009, 2011;
Boatwright et al., 2009, 2010, 2011; Van Wyk et al., 2010; Le Roux
et al., in press). The present matK phylogeny agrees with the more com-
prehensive analysis of ITS and rbcL sequences of Boatwright et al.
(2008b) in revealing well-supported generic relationships in two
main subclades (Fig. 4). Among the close relatives from within the
Core Genistoids, the Crotalarieae has been strongly resolved as sister
to the Genisteae (Fig. 4). Indeed, both tribes are the only Genistoids
accumulating pyrrolizidine alkaloids, although the Genisteae is primar-
ily known to accumulate quinolizidine alkaloids of the α-pyridone
type (Van Wyk, 2003; Wink and Mohamed, 2003). Despite a lack of
defining morphological synapomorphies, the Crotalarieae is easily
distinguished from the Genisteae by the absence of bilabiate calyces
with a bifidupperlipandatrifid lower lip, which is a potential syn-
apomorphy for the Genisteae (Van Wyk, 2005; Boatwright et al.,
2008b).
70 D. Cardoso et al. / South African Journal of Botany 89 (2013) 58–75

The genistoid Genisteae clade
The Genisteae includes ca. 618 papilionate-flowered species in 25
genera (Table 1;Polhill and Van Wyk, 2005) that are largely confined
to the temperate biome (Schrire et al., 2005). The genus Lupinus L., one
of the most spectacular plant radiations (Hughes and Eastwood, 2006),
is also the most diverse within the clade. All molecular phylogenies
that have comprehensively sampled within the Genisteae have
strongly resolved its monophyly (Käss and Wink, 1997; Kajita
et al., 2001). The small African genus Dichilus that was transferred
from the Crotalarieae (Polhill, 1976; Bisby, 1981) to the Genisteae
by Van Wyk and Schutte (1995) is for the first time sampled in a
matK phylogeny. Our results confirm the analysis of rbcL sequences
that place the genus as closely related to the Genisteae (Fig. 5;
Kajita et al., 2001). Morphological features that traditionally distin-
guished the tribe (e.g., the lack of an aril, or the presence of an aril
but on the short side of the seed, and stamen filaments fused in a
closed tube with markedly dimorphic anthers; Polhill, 1976; Bisby,
1981) might be synapomorphies, to whic hcan be added the bilabiate
calyx and presence of α-pyridone alkaloids (Polhill and Van Wyk,
2005). Noteworthy, the rare isoflavone 5-O-methylgenistein that
has been reported in the leaves of most Genisteae genera is very like-
ly a synapomorphy of the whole clade (Van Wyk, 2003). Previous
molecular phylogenies indicate several generic recircumscriptions
yet are poorly resolved (Kajita et al., 2001; Wink and Mohamed,
2003; Pardo et al., 2004). The matK gene provided excellent resolu-
tion for the few accessions included in the present study (Fig. 5). Per-
haps, the inclusion of the many genera for which matK data are still
lacking (Table 1), as well as the broad morphological diversity of
putatively non-monophyletic genera (Wink and Mohamed, 2003;
Pardo et al., 2004), can help to resolve relationships within
Genisteae.
Unplaced genistoid genera
Five genera with strongly bilaterally-symmetrical papilionate
flowers still remain unresolved within the Genistoid s.l. clade with
respect to the previously described lineages (Table 1). The genus
Dermatophyllum comprises only four species from warm temperate
woodlands, chaparral, and deserts of southern United States to central
Mexico (Fig. 4;Pennington et al., 2005). Its phylogenetic position has
not yet been resolved within the 50-kb inversion clade (Fig. 4;Cardoso
et al., 2012a), but because it also accumulates a range of quinolizidine al-
kaloids (Kite and Pennington, 2003) and has some morphological simi-
larity to Sophora L. (Polhill, 1981a), we follow the suggestion of LPWG
(2013) who indicated that this genus might be a sister to the Genistoid
s.l. clade.
Cardoso et al. (2012a) suggested the segregation of five Neotropical
species of the Clathrotropis macrocarpa group into a separate genus,
which is distinguished by leaflets with prominent venation and larger
elastically dehiscent pods that are sometimes thickened and dilated
along the upper sutures. This new genus is also known to bear
quinolizidine alkaloids (Ricker et al., 1994; Sagen et al., 2002) and its re-
lationship is still elusive with respect to the Brongniartieae, Leptolobieae,
and Core Genistoids (Fig. 4).
The small African genus Pericopsis, which also accumulates
quinolizidine alkaloids (Kinghorn et al., 1988), is strongly supported
within the Genistoids s.l., but unresolved with respect to the C.
macrocarpa group, Brongniartieae, Leptolobieae, and Core Genistoids
based on our preliminary analysis of trnL intron sequences (R.T.
Pennington and D. Cardoso, unpubl.), a result also consistent with
phylogenetic analysis of rbcL sequences (Doyle et al., 1997). The alter-
nate leaflets, colleter-like glands in the axils of bract and bracteoles, and
the characteristic compressed samaroid fruits with marginal narrow
wings of Pericopsis suggest an affinity to the Leptolobieae genera
(Cardoso et al., 2012c).
The small Malagasy genera Sakoanala and Neoharmsia were never
sampled in molecular phylogenies, but their overall morphology
indicates more similarity with Genistoid genera than any other major
early-branching papilionoid lineage (Pennington et al., 2005;P.
Herendeen, pers. comm.). Additionally, quinolizidine alkaloids have
been reported for Sakoanala (Van Wyk et al., 1993).
The Amorpheae clade
This is a predominantly North American temperate clade of eight
genera and ca. 247 species, most of which belong to the species-rich
genus Dalea L. (Table 1). The Amorpheae is remarkably distinguished
by the evolution of radial symmetry or the simplification of the
papilionate flowers in most genera (Fig. 5;McMahon and Hufford,
2004; McMahon, 2005). The Amorpheae has been resolved as mono-
phyletic in all previous molecular phylogenies (McMahon and
Hufford, 2004; Wojciechowski et al., 2004; Cardoso et al., 2012a).
These studies also show Amorpheae as sister to the Dalbergioid le-
gumes (Lavin et al., 2001), herein Dalbergieae, in a well-supported
more inclusive clade that has been collectively referred to as the
Dalbergioid s.l. clade (Fig. 5). The Amorpheae has been diagnosed
morphologically by synapomorphies that include the punctate glands
throughout the plant body, indehiscent, single-seeded fruits, and ter-
minal inflorescences (Barneby, 1977; McMahon and Hufford, 2004)
but these features are found variously among the Dalbergieae genera
(Lavin et al., 2001). Indeed, the indehiscent pods probably constitute
a good synapomorphy for the larger Dalbergioid s.l. clade. Two main
subclades and generic relationships within Amorpheae were strongly
resolved in the comprehensively-sampled phylogeny of McMahon
and Hufford (2004) (see Fig. 5), who first suggested a more narrowly
circumscribed Psorothamnus Rydb. to include only the species with
sessile or nearly sessile flowers, non-exserted pods, and non-spiny in-
florescences. The genus Psorodendron Rydb. should be reestablished
to accommodate the species with stout woody branches, spiny inflo-
rescences and/or exserted pods that hitherto formed part of the
non-monophyletic Psorothamnus (McMahon and Hufford, 2004).
The Dalbergieae clade
This is a mostly pantropical clade of 46 genera and ca. 1367 spe-
cies, of which more than 60% belong to only the four species-rich gen-
era Adesmia DC., Aeschynomene L., Dalbergia L.f., and Machaerium Pers.
(Fig. 5;Table 1). The Dalbergieae corresponds to the Dalbergioid
legumes largely defined by Lavin et al. (2001) with phylogenetic analyses
of molecular and morphological data. The distinctive aeschynomenoid
root nodule of the Dalbergieae (Lavin et al., 2001) makes this one of the
very few large clades of Papilionoideae that are defined by a morpholog-
ical synapomorphy (LPWG, 2013). Three main Dalbergioid lineages of
morphologically eclectic genera, the Adesmia,Dalbergia,andPterocarpus
clades have been consistently resolved (Fig. 5;Lavin et al., 2001;
Cardoso et al., 2012a, 2012b). The Dalbergieae is also marked by indepen-
dent evolution of non-papilionate flowersinthesmallgeneraAcosmium,
Etaballia Benth., Inocarpus J.R.Forst. & G.Forst., Riedeliella Harms, and some
Pictetia DC. species (Fig. 5;Lavin et al., 2001; Cardoso et al., 2012b).
In the last ten years after the publication of Lavin et al. (2001),
we have seen three unexpected additions to the Dalbergieae: the
monospecific genus Maraniona C.E.Hughes, G.P.Lewis, Daza & Reynel,
a completely new discovery arising from fieldwork (Hughes et al.,
2004); the radially-symmetrical-flowered Acosmium, which was
thought to belong to the Genistoids (Cardoso et al., 2012b); and
more recently, Steinbachiella Harms. Lewis et al. (2012) clarified the
taxonomic identity of this orphaned monospecific taxon by showing
it to be a clearly defined genus, phylogenetically close to Machaerium
(Fig. 5). Other recent advances within Dalbergieae include an attempt
to elucidate inter-relationships between Aeschynomene s.l., Dalbergia,
and Machaerium (Ribeiro et al., 2007), and the phylogenies of
71D. Cardoso et al. / South African Journal of Botany 89 (2013) 58–75

individual genera, such as Platymiscium (Saslis-Lagoudakis et al.,
2008), Centrolobium Mart. ex Benth. (Pirie et al., 2009), Arachis L.
(Bechara et al., 2010), and Pterocarpus Jacq. (Saslis-Lagoudakis et al.,
2011). Studies are already underway or about to be published
that provide new results concerning the phylogeny and bioge-
ography of Adesmia (Iganci et al., 2013), Amicia (T. Särkinen &
C. Hughes, unpubl.), Dalbergia (Vatanparast et al., 2013), Machaerium
(F. Filardi et al., unpubl.), and Zornia (A.P. Fortuna-Perez et al., unpubl.).
Additionally, a new assessment of relationships among the Malagasy
endemic Ormocarpopsis R.Vig. and allies suggests a broader circum-
scription of Ormocarpopsis to encompass the monospecificPeltiera Du
Puy & Labat (Thulin et al., 2013). Substantial progress also needs to be
made with respect to the poorly resolved relationships among the
mostly monospecific or species-poor genera of the Pterocarpus clade
(Fig. 5;Lavin et al., 2001; Saslis-Lagoudakis et al., 2008; Cardoso et al.,
2012b). A better sampling would be important for the large genus
Aeschynomene s.l., which clearly comprises two disparate clades that
are also morphologically, ecologically, and biogeographically distinct
(Fig. 5;Lavin et al., 2001; Ribeiro et al., 2007; M. Lavin, unpubl.).
Aeschynomene sect. Aeschynomene is paraphyletic with respect to the
genera Kotschya Endl., Smithia Aiton, Humularia P.A.Duvign., Bryaspis
P.A.Duvign., Geissaspis Wight & Arn., Cyclocarpa Afzel. ex Urb., and
Soemmeringia Mart., and its constituent species have medifixed stipules
and are primarily distributed in wet forests and savannas, where they
have broad geographic ranges. The monophyletic Aeschynomene sect.
Ochopodium Vogel is closer to Machaerium and its members have
basifixed stipules and are primarily inhabiting seasonally dry forests,
with individual species narrowly distributed (M. Lavin, unpubl.).
Further taxonomic changes to the delimitation of Aeschynomene will
inevitably require a comprehensive phylogenetic analysis and sampling
which will also have to include much of the diversity of the large genus
Machaerium, as well as the recently reestablished Steinbachiella.
The Baphieae clade
The Baphioid legumes, first defined in the trnL intron phylogeny
of Pennington et al. (2001) and confirmed in the matK phylogeny of
Cardoso et al. (2012a) could be clearly distinguished as a separate
papilionoid tribe that is sister to the species-rich NPAAA clade
(Fig. 5; Appendix S1). The Baphieae comprises ca. 57 species largely
from Africa and southern Asia and includes the genera Airyantha
Brummitt, Baphia Afzel. ex Lodd., Baphiastrum Harms, Bowringia
Champ. ex Benth., Dalhousiea,andLeucomphalos traditionally clas-
sified in Sophoreae (Polhill, 1981a), plus Baphiopsis Benth. ex
Baker of Swartzieae (Polhill, 1994). In addition to the free stamens
and poorly differentiated lower petals, or flowers sometimes
appearing radially symmetrical, Baphieae is characterized by
having simple or unifoliolate leaves, anthers more or less basifixed,
and the calyx splitting to the base either down one side only and
therefore appearing spathaceous, or down both sides and thus be-
coming bilabiate (Brummitt, 1968; Polhill, 1981a). Taxonomic and
phylogenetic progress is yet to be made with respect to the
non-monophyletic large genus Baphia, and to evaluate the relation-
ship and generic status of Bowringia and the monospecific
Baphiastrum and Leucomphalos.
Unresolved early-branching genera
Tribal designations for two unresolved early-branching genera remain
uncertain and depend on whether monotypic tribes should be recognized
or not. The phylogenetically isolated and radially-symmetrical-flowered
genus Amphimas from lowland rain and seasonally dry tropical forests
of west and central Africa is one of the nine unresolved lineages of the
large 50-kb inversion clade (Fig. 3;Cardoso et al., 2012a). In addition to
its non-papilionate flowers with free stamens and unusually feature of
having only three petals that are each deeply two-lobed, Amphimas
is known to produce balsam (Polhill, 1981a; Pennington et al., 2005).
The South American Aldina is also phylogenetically isolated within
50-kb inversion clade (Fig. 3;Cardoso et al., 2012a). Traditionally, this
genus was included in the tribe Swartzieae (Cowan, 1981) because of
its non-papilionate, radially symmetrical flowers with entire calyces
and numerous stamens (Fig. 5). Aldina includes ca. 22 species primar-
ily in the rain forest biome, including habitats such as tropical mon-
tane and lowland Amazonian forests and white sand savannas
(Stergios and Cowan, 1999; Ireland, 2005).
The NPAAA clade
The non-protein–amino-acid-accumulating (NPAAA) clade (Fig. 5;
Appendix S1) is not the focus of the present study, although we also
have comprehensively sampled genera within this clade. The NPAAA
clade is species-rich and comprises about 9464 species and 305 genera,
representing almost 70%of the species and more than 60% of the genera
in the Papilionoideae, and almost 50% of the species and genus diversity
of the whole legume family (Lewis et al., 2005). All NPAAA lineages
are predominantly marked by the evolution of highly specialized
papilionate flowers (Lewis et al., 2005). Detailed taxonomic, biogeo-
graphical, and phylogenetic accounts of many NPAAA papilionoids are
addressed elsewhere (Hu et al., 2000; Wojciechowski et al., 2000,
2004; Allan et al., 2003; Crisp and Cook, 2003; Lavin et al., 2003;
Steele and Wojciechowski., 2003; Lewis et al., 2005; Schrire et al.,
2009; Stefanovićet al., 2009; Sirichamorn et al., 2012) and recently
reviewed by the LPWG (2013). The present matK phylogeny resolved
many well-supported major clades within the NPAAA papilionoids
(Appendix S1), such as the Mirbelioids, Indigofereae, Millettioids,
Robinioids, and the inverted-repeat-lacking clade (IR-Lacking clade),
which are also consistent with those resolved by Wojciechowski et al.
(2004) and McMahon and Sanderson (2006), the latter of which
involved an analysis of more than two thousand sequences in a
supermatrix framework. However, it is clear that greater phylogenetic
resolution is yet to be achieved among the early-branching genera of
the Millettioids and IR-Lacking clade, and within the Phaseoloid
subclades (Appendix S1; Wojciechowski et al., 2004; Stefanovićet al.,
2009).
Challenges in reconstructing the Papilionoideae phylogeny
The challenge of reconstructing the deep-branching history of the
papilionoid legumes has been addressed numerous times in the last de-
cades (Doyle et al., 1997; Käss and Wink, 1995, 1996, 1997; Doyle et al.,
1997, 2000; Kajita et al., 2001; Pennington et al., 2001; Wojciechowski
et al., 2004; McMahon and Sanderson, 2006; Cardoso et al., 2012a). Al-
though we have revealed many strongly supported and well-resolved
clades within Papilionoideae, relationships among the first-diverging
clades and the main lineages within the 50-kb inversion clade still remain
unresolved (Fig. 1). Because our analyses are based upon a single gene,
this is not surprising, and the addition of more loci is necessary. Fur-
thermore, much is yet to be accomplished on integrating data on the
incredible morphological and chemical diversity of legumes into our
phylogenetic estimates, and to sample the many genera for which molec-
ular data are still lacking (LPWG, 2013). Many promising opportunities
are now possible by the increasing development of cost-effective
high-throughput next generation sequencing (e.g., Harrison and Kidner,
2011; Egan et al., 2012; LPWG, 2013). Although next-gen technologies
may eventually help, given the excellent phylogenetic resolution
obtained with the matK gene, we make a plea that future efforts on
Papilionoideae phylogenetics should focus more on those genera for
which the matK sequences are still lacking. We do not have matK
sequences for 52 of the 196 early-branching papilionoid genera
(Table 1). At least for most of them we have fairly reliable information
from other DNA markers, but unfortunately no molecular data are
72 D. Cardoso et al. / South African Journal of Botany 89 (2013) 58–75

available for some key genera, such as Haplormosia,Neoharmsia,
Petaladenium,Sakoanala,andUleanthus (Table 1). More thorough sam-
pling is also needed to resolve the taxonomy of non-monophyletic
genera, such as Aeschynomene,Baphia,Clathrotropis,Myrocarpus,and
Sophora (Table 1). We must also devote our attention to morphologically
heterogeneous species-rich genera, such as Crotalaria,Dalea,Machaerium,
and Ormosia.
The recent formation of the Legume Phylogeny Working Group
holds out hopes of integrating legume expertise worldwide to take
advantage of sharing data and new approaches in phylogenetics
(LPWG, 2013). Under such a collaborative effort, a complete generic
phylogeny and revised clade-based classification of the whole legume
family should be feasible in the near future (LPWG, 2013). Certainly,
by having a more complete and resolved Papilionoideae phylogeny,
we will be able to further explore the evolution of other features,
particularly those that vary in the early-branching clades. An excel-
lent example of this is the recurrent convergent evolution of non-
papilionate floral morphologies (Figs. 2–5;Pennington et al., 2000;
McMahon, 2005; Boatwright et al., 2008a; Cardoso et al., 2012a,
2012b, 2013a). An exciting research direction would be to explore
the interplay between floral morphology and species diversification
that have ultimately resulted in the predominance of species-rich
papilionoid clades.
Supplementary data to this article can be found online at http://
dx.doi.org/10.1016/j.sajb.2013.05.001.
Acknowledgments
We would like to extend our thanks to Cecília de Azevedo, Gerald
Carr, Alan Cressler, Vinícius Dittrich, Émile Fonty, Mark Hyde, Mauricio
Mercadante, Scott Mori, Thomas Palmer, Gustavo Shimizu, and Bart
Wursten for kindly providing their beautiful photographs to illustrate
some of the figures. This paper arose from the first author's plenary lec-
ture at Sixth International Legume Conference held at the University of
Johannesburg, South Africa. It is also part of the first author's PhD thesis
developed at Programa de Pós-Graduação em Botânica (PPGBot-UEFS)
and supported by SWE grant from CNPq (process 201621/2010-0)
at Montana State University, Bozeman, USA. Financial support for
field work and DNA sequencing were partially sponsored by Sistema
Nacional de Pesquisa em Biodiversidade (SISBIOTA, processes CNPq
563084/2010-3 and FAPESB PES0053/2011).
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50-kb inversion clade
0.1 changes
Mirbelioids
Muellera campestris DC2320
Piscidia piscipula AF142710
Nesphostylis holosericea AY582979
Tibetia yunnanensis JQ669583
Wisteria frutescens AF142731
Strophostyles helvola AY509949
Kummerowia stipulacea EU717417
Ornithopus compressus AF142727
Decorsea schlechteri AY582975
Lathyrus sativus AF522086
Lespedeza cuneata EU717416
Genistidium dumosum AF543858
Lessertia herbacea AY920453
Apios americana AY386926
Melilotus albus AF142738
Bionia bella Torres12
Gompholobium minus AY386891
Millettia grandis AF142724
Callerya reticulata JQ619954
Glycyrrhiza lepidota AY386883
Colutea arborescens AY386874
Mysanthus uleanus AY509941
Shuteria vestita EU717423
Pseudarthria hookeri JF270902
Oxyrhynchus volubilis AY509935
Sutherlandia frutescens AY386913
Spathionema kilimandscharicum JN008193
Brachypterum robustum AF142716
Wajira danissana AY583008
Dioclea lasiophylla DC2324
Kunstleria ridleyi JX506598
Physostigma venenosum JN008195
Robinia pseudoacacia AF142728
Dalbergiella nyasae AF142706
Ononis natrix AF522114
Aganope thyrsiflora JX506602
Neorautanenia mitis JN008178
Cullen tenax EF550004
Pongamiopsis amygdalina AF142711
Dipogon lignosus AY582988
Barnebyella calycina JQ669593
Phaseolus vulgaris AY582987
Pachyrhizus erosus EU717401
Ancistrotropis peduncularis JN008272
Rhynchosia edulis JQ587827
Alistilus jumellei JN008191
Gastrolobium punctatum AY386885
Disynstemon paullenoides GU951670
Daviesia latifolia AY386887
Lackeya multiflora AL
Alhagi sparsifolia AY177669
Galega orientalis AF522083
Chesneya elegans JQ619958
Ptycholobium biflorum JQ669619
Canavalia parviflora HQ707539
Ramirezella strobilophora AY509936
Calophaca pskemica JQ669603
Leptospron adenanthum AY582983
Cajanus cajan EU717414
Condylostylis candida JN008260
Collaea stenophylla LPQ12460
Microcharis karinensis AY650279
Neodunnia richardiana AF142726
Cymbosema roseum DC2868
Cleobulia multiflora Jesus13
Hypocalyptus coluteoides AY386886
Phyllodium pulchellum HM049524
Astragalus canadensis AY386875
Millettia thonningii AF142723
Alysicarpus vaginalis JQ587510
Rupertia physodes AY386868
Sphinctospermum constrictum AF547191
Mundulea sericea AF142713
Vigna unguiculata AY589510
Halimodendron halodendron JQ619947
Apurimacia dolichocarpa FJ968527
Lens culinaris AF522089
Vatovaea pseudolablab AY583017
Dorycnium pentaphyllum JQ619968
Carmichaelia williamsii AY386873
Mucuna pruriens AB627857
Sphenostylis angustifolia AY582978
Leptoderris brachyptera JX506611
Amphicarpaea bracteata AY582971
Pediomelum pentaphyllum EF549992
Bituminaria bituminosa JF501107
Otoptera burchellii JN008176
Ebenus cretica JQ619960
Cyamopsis senegalensis AF142698
Desmodium barbatum EU717420
Erythrina cristagalli AY386869
Cologania pallida JQ619980
Centrosema sagittatum JQ587552
Vicia faba AY386899
Kennedia nigricans EU717424
Deguelia dasycalyx LPQ14503
Hedysarum boreale AY386892
Sesbania tomentosa JX295926
Oxytropis lambertii AY386915
Pisum sativum AY386961
Rhodopsis planisiliqua AAC1765
Philenoptera eriocalyx AF142720
Paraderris elliptica AF142714
Parochetus communis AF522115
Tadehagi triquetrum JN407128
Campylotropis macrocarpa AY386870
Cochliasanthus caracalla JN008274
Pseudovigna argentea JN008179
Ostryocarpus riparius JX506599
Hardenbergia violacea EU717425
Isotropis foliosa AY386890
Taverniera glauca JQ669601
Trifolium repens AF522131
Eriosema diffusum JQ587629
Sphaerophysa salsula JQ669581
Onobrychis montana AY386879
Dolichopsis paraguariensis AY509942
Xeroderris stuhlmannii AF142708
Hybosema ehrenbergii AF547195
Lennea modesta AF543851
Bossiaea cordigera AY386888
Swainsona pterostylis AF142735
Abrus precatorius AF142705
Poitea glyciphylla AY650278
Anthyllis vulneraria AF543845
Indigofera suffruticosa AF142697
Austrosteenisia blackii AF142707
Clianthus puniceus AY386914
Phylloxylon spinosa AY650280
Calopogonium sp. JQ669608
Galactia martii LPQ7583
Camptosema spectabile LPQ7088
Olneya tesota AF543857
Neonotonia wightii EU717402
Clitoria ternatea EU717427
Camptosema ellipticum LPQ14073
Teramnus uncinatus EU717400
Hippocrepis unisiliquosa JQ619986
Coronilla coronata JQ619970
Poissonia hypoleuca AF547193
Gueldenstaedtia stenophylla JQ669620
Smirnowia turkestana JQ669579
Helicotropis linearis JN008258
Hebestigma cubense AF543850
Coursetia glandulosa AF543852
Peteria thompsonae AF47190
Ophrestia radicosa EU717430
Lablab purpureus AY582989
Orbexilum lupinellum EF549995
Dioclea grandiflora JX295862
Lotus purshianus AF142729
Fordia splendidissima AF142718
Dolichos trilobus AY582976
Sigmoidotropis speciosa DQ443466
Caragana arborescens AF142737
Lonchocarpus lanceolatus AF142717
Derris laxiflora AF142715
Tephrosia heckmanniana AF142712
Trigonella cretica AF522146
Butea monosperma JN008175
Aotus ericoides AY386884
Craspedolobium schochii JF953573
Psophocarpus lancifolius JN008177
Pueraria montana AY582972
Otholobium bracteolatum EF550005
Eremosparton flaccidum JQ619964
Psoralea cinerea AF142699
Uraria crinita JN407138
Hammatolobium kremerianum JQ619984
Cratylia mollis LPQ8024
Ladeania juncea EF549986
Securigera varia AF543846
Gliricidia brenningii AF547199
Macroptilium longipedunculatum AY509939
Macrotyloma stenophyllum JN008187
Cicer canariense AF522079
Platycyamus regnellii AF142709
Medicago sativa AY386881
Glycine max AF142700
Hoita orbicularis EF549962
Bionia coriacea LPQ13611
Galactia striata AF142704
97
85
95
88
80
88
88
83
92
96
80
98
91
91
98
91
91
95
98
84
97
94
97
80
92
89
89
97
95
Baphieae
NPAAA clade
Hypocalypteae
Indigofereae
Abreae
Millettieae
Diocleae
Barbierieae
Desmodieae
Psoraleeae
Cajaninae clade
Erythrininae clade
Kennediinae clade
Phaseolinae
clade
Sesbanieae
Robinieae
Loteae
IR-Lacking clade
Hedysareae
Astragaleae
Fabeae
Millettioids
Appendix S1. Continuation from Fig. 5 of the matK Bayesian majority-rule consensus tree of the legumes. This portion shows the relationships among the large non-protein-amino-acid-accumulating (NPAAA)
papilionoid clade. Numbers on branches are Bayesian posterior probabilities. Posterior probabilities are not given for the resolved branches weakly supported by 0.50–0.79. Branches in bold are those supported by
a posterior probability of 0.99 or 1.0. GenBank accession numbers are provided after taxon names. The informally named main NPAAA papilionoid lineages (Mirbelioids, Millettioids, and Hologalegina including
the Robinioids and the inverted-repeat-lacking clade) are according to Wojciechowski et al. (2004). Strongly supported clades that might be recognized at the tribal rank are named. The resurrection of tribe Diocleae
was newly suggested by Queiroz et al. (unpubl.). The tribal classification largely follows a reconciliation of the present phylogeny and the proposals of the Legume Phylogeny Working Group (LPWG) presented at
the symposium “Draft Classification of Leguminosae” during the Sixth International Legume Conference held at Johannesburg, South Africa.
Hologalegina
Robinioids