Ireland, H., Pennington, R.T. and Preston, J. (2000). Molecular systematics of the Swartzieae.

In:
P.S. Herendeen and A. Bruneau (editors). Advances in Legume Systematics 9, pp 217–231. Royal
Botanic Gardens, Kew.

MOLECULAR SYSTEMATICS OF THE SWARTZIEAE

HELEN IRELAND 1,2,3, R. TOBY PENNINGTON 2, JILL PRESTON 2

1
Royal Botanic Gardens Kew, Richmond, Surrey, TW9 3AB, UK
2
Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh, EH3 5LR, UK
3
University of Reading, Whiteknights, Reading, RG6 6AS, UK

Abstract
Relationships remain poorly understood in a number of areas within the
Leguminosae, but particularly in the basal woody groups, such as the tribes Swartzieae
and Sophoreae, which are considered to be transitional between the Papilionoideae
and Caesalpinioideae. Sequences were generated from the chloroplast trnL intron-
spacer region for all genera within the Swartzieae plus placeholder representative
taxa from the tribes Sophoreae, Dipterygeae, and Dalbergieae, with three genera of
Caesalpinioideae as outgroups. The cladistic analysis shows Swartzieae and Sophoreae
to be polyphyletic. The coherence of each of the informal Swartzieae groups is
discussed in relation to this analysis. A monophyletic ‘swartzioid’ clade comprising
Swartzia, Bobgunnia, Bocoa, Ateleia, and Cyathostegia emerges as a poorly supported
sister group to the remainder of the Papilionoideae. It is suggested that this swartzioid
clade could constitute a reduced Swartzieae and that the remaining Swartzieae
genera be moved to other tribes.

Introduction

Relationships between genera and tribes within the Papilionoideae are poorly
understood, particularly amongst the putatively most basal tribes, including the
Swartzieae. Although now generally considered to be papilionoid, the Swartzieae
displays features in common with both subfamilies Papilionoideae and
Caesalpinioideae and has frequently been shifted between them. Recent research has
shown the Swartzieae and its neighbouring tribe Sophoreae to be non-monophyletic
(Ferguson and Schrire, 1994; Herendeen, 1995; Doyle et al., 1996; Gasson, 1996;
Doyle et al., 1997). It is important that relationships amongst these basal tribes be
understood to provide a basis for exploring the divergence of the remaining taxa of
Papilionoideae. This paper focuses on the systematics of the Swartzieae using DNA
sequence data from the trnL region of the chloroplast genome to contribute data
towards delimiting the tribe and elucidating its systematic position.
The trnL region comprises an intron and a spacer region and is approximately
1000 bases long in most legumes. It was chosen for this study because previous studies
show that it displays the appropriate level of sequence divergence for phylogenetic
studies above the species level (Richardson et al., in press). Its suitability for studying
relationships amongst basal papilionoid legume genera was confirmed in a pilot study
(Ireland, 1996).

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Advances in Legume Systematics 9

Objectives

The main objectives of the present study were to test if the Swartzieae as set out in
Polhill (1994) is monophyletic, or if the recent suggestions that it is polyphyletic
(Ferguson and Schrire, 1994; Herendeen, 1995; Doyle et al., 1996, 1997; Gasson,
1996) are correct, and to test the coherence of Polhill’s (1994) informal groupings
within the tribe. In addition, we wish to shed light on the problem of the systematic
position of the Swartzieae, and assess whether it should remain in a basal position
within the Papilionoideae, be transferred to the Caesalpinioideae, or be recognised
as a fourth subfamily.
This paper is closely linked to the paper by Pennington et al. (2000b) in which
sequences of the trnL intron-only were used in a much more comprehensive study of
the generic relationships amongst all the putatively basal tribes of the Papilionoideae,
including Aeschynomeneae, Dalbergieae, Dipterygeae, Sophoreae, and Swartzieae.
In our study, focussing on the Swartzieae, sequences from both the intron and the
spacer were generated. One aim was to discover if the spacer region would be
phylogenetically informative for Swartzieae genera, and in combination with the
intron, would provide more resolution than the intron alone for studying generic
relationships amongst the Swartzieae.

Background

The Swartzieae was first described by De Candolle (1825) as a ‘subordo’ of the

Leguminosae, containing Swartzia Schreb. and Baphia Afzel ex Lodd. (Table 1). He
considered it very distinct and gave it equal status to the Papilionoideae,
Mimosoideae, and Caesalpinioideae (which he termed subordos ‘Papilionaceae’,
‘Mimosae’ and ‘Caesalpineae’).
Table 1 summarises the taxonomic history of the Swartzieae in chronological order
since De Candolle (1825) to the most recent treatment by Polhill (1994). It illustrates
how the systematic position and rank of the Swartzieae have frequently been changed.
Bentham (1865), Hutchinson (1964), Cowan (1981), and Polhill (1994) ranked it at
tribal level in the Papilionoideae, whilst Taubert (1891) moved it to the
Caesalpinioideae, and De Candolle (1825), Bartling (1830), Endlicher (1840), and
Corner (1951) considered it a suborder, order, or subfamily respectively, with equal
rank to the Papilionoideae and Caesalpinioideae.
Polhill (1994) was aware of the intermediate position of the Swartzieae between
the Papilionoideae and Caesalpinioideae, but provisionally retained it in the
Papilionoideae as ‘an assemblage of convenience’. He recognised some variation
within the tribe and divided it into four informal groups (Table 1). The Swartzia
group was defined by a single petal and many stamens. It is similar to the Aldina
group, which differs in having five to six petals, or in the case of Mildbraediodendron
Harms and Cordyla Lour. no petals at all. The Lecointea group, which Polhill (1994)
considered to be closest to the Sophoreae, has 10 stamens, five sepals and the leaves
are often toothed, except in Harleyodendron R.S. Cowan. The Ateleia group is
distinguished by a single petal, a campanulate calyx, and a characteristic type of
endothecial thickening. Polhill (1994) noted that the defining characters of the
tribe – a closed calyx in bud splitting in various ways at anthesis, frequently
numerous stamens, and single or lacking petal – are not strongly correlated. For
example, some Swartzieae genera, including Ateleia (Sessé and Moçiño ex DC.)
Benth., Cyathostegia (Benth.) Schery, and Lecointea Ducke have a campanulate calyx
which does not split at anthesis; Lecointea, Harleyodendron, Exostyles Schott ex
Sprengel, and Amburana Schwacke and Taub. have only 10 stamens; and seven out
of the 15 genera, including Aldina Endl., Baphiopsis Benth. ex Bak., Lecointea,
Harleyodendron, Exostyles, Zollernia Nees, and Holocalyx Micheli, have three to six

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 Molecular systematics of the Swartzieae

petals. Clearly the features defining the tribe are inconsistent, but despite this
Polhill (1994) suggested that the Swartzieae might still prove to have some
coherence, and be expanded to include some of the more basal Sophoreae genera.
Polhill’s (1994) classification of the Swartzieae is the most recent to date, and this
was used as a basis for exploring the systematics of the tribe.

Materials and Methods

DNA was extracted and a full intron-spacer sequence was generated for 14 out of
the 15 Swartzieae genera (sensu Polhill, 1994) plus the more recently described
Bobgunnia Kirkbr. and Wiersema, which fits best into the Swartzieae (Kirkbride and
Wiersema, 1997). These sequences were combined with sequences from a total of
19 genera from the tribes Sophoreae, Dipterygeae, and Dalbergieae, in addition to
three Caesalpinioideae genera as outgroups. The Sophoreae, Dipterygeae, and
Dalbergieae genera were selected to represent the major clades in the cladogram of
Pennington et al. (2000b). The outgroup genera were selected as representative
non-papilionoids because the sequences are easily alignable with those of the
ingroup genera.
For methods of DNA extraction and sequencing and voucher details refer to
Pennington et al. (2000b). In our analysis, extra accessions were sequenced for eight
out of the 16 Swartzieae genera to confirm their position in the cladogram, and to
represent hypothesised groupings within some genera such as Bocoa Aubl. (Cowan,
1974; Herendeen, 1995; Gasson, 1996), Swartzia (Cowan, 1968) and Ateleia (pers. obs.).
Voucher details for the additional accessions of Swartzieae genera sequenced here but
not included in the analysis of Pennington et al. (2000b) are listed in Table 2.
Sequences were aligned in Sequence Navigator using the Clustal algorithm with
final alignment by eye. Cladistic analysis was performed using PAUP*4.0b2.
Heuristic searches used random addition sequence with 1000 replicates and tree-
bisection-reconnection (TBR) swapping. All characters were equally weighted and
unordered. Bias introduced by manual alignment was evaluated using sensitivity
analyses (Whiting et al., 1997; Beyra and Lavin, 1999). Firstly, indels of the same
size and position in different taxa were coded, so that they were treated as
individual characters rather than strings of missing data. A second sensitivity
analysis involved the inclusion and exclusion of alignment variable regions.
Thirdly, areas with high quantities of missing data were included and excluded
from the analysis. These occurred at the beginnings and ends of sequences, and in
the middle of the full sequence where the intron and spacer joined. Finally, four
taxa, Sweetia Spreng., Vatairea Aubl., Vataireopsis Ducke, and Luetzelburgia Harms,
which share a large deletion of 378 bases at the beginning of the spacer region,
were excluded from the analysis to investigate the effects of optimisation of
missing values in this region.

Results

Our study showed that sequence alignment of both the intron and spacer region
of trnL was straightforward. The results of this study indicate that the spacer region,
as well as the intron of trnL is phylogenetically informative. The amount of variation
displayed by the intron and the spacer was more or less equal; 113 out of 557 (20.3%)
of the characters for the intron were informative, and 102 out of 509 (20%) for the
spacer. In combination with the intron, the spacer is a useful tool for studying
relationships amongst basal papilionoid genera. The matrix and full details of all
analyses are available from the first author.

219
220
TABLE 1. Taxonomic history of the Swartzieae.

GENERA included RANK and POSITION DEFINING FEATURES

De Candolle (1825) Swartzia, Baphia ‘subordo’ Swartzieae Hypogynous stamens, very irregular or missing
(equal rank to ‘subordos’ corolla, and a bladder shaped calyx without a
Papilionaceae, suture, splitting into irregular lobes at anthesis
Mimosae and Caesalpineae)

Bartling (1830) Swartzia, Baphia, Zollernia ‘ordo’ Swartzieae (equal rank to Calyx finally splitting into valves and corolla
Advances in Legume Systematics 9

‘ordos’ Papilionaceae, irregularly hypogynous

Mimoseae and Caesalpineae)

Endlicher (1840) Swartzia, Baphia, Zollernia, ‘ordo’ Swartzieae (equal rank to Calyx splitting into valves, and frequently
Aldina, Cordyla, Detarium ‘ordos’ Papilionaceae and Mimosae) numerous stamens

Bentham (1865) Swartzia, Zollernia, Exostyles, tribe in the ‘Papilionaceae’ 1) In those genera of the Swartzieae which
Aldina, Cordyla (next to Caesalpinioideae) have five petals, the upper petal is most often
positioned outside the other petals
2) The radicle, where observed, is always inflexed

Taubert (1891) Tounatea [=Swartzia], Zollernia, tribe Tounateeae in the

Exostyles, Aldina, Cordyla, Baphiopsis, Caesalpinioideae
Holocalyx

Corner (1951) subfamily Swartzioideae (equal rank The seeds of Swartzia are intermediate between
to Papilionoideae, Mimosoideae and the papilionoid and the mimosoid–caesalpinioid
Caesalpinioideae) construction
 TABLE 1. continued

Hutchinson (1964) Swartzia, Zollernia, Aldina, Cordyla, tribe in the Papilionoideae Same as Bentham (1865)
Baphiopsis, Holocalyx, Lecointea,
Mildbraediodendron, Cashalia [=Dussia]

Cowan (1981) Swartzia, Zollernia, Exostyles, Aldina, tribe in the Papilionoideae An entire calyx
Cordyla, Baphiopsis, Lecointea,
Mildbraediodendron, Candolleodendron,
Harleyodendron, Bocoa

Polhill (1994) Swartzia group: Swartzia, Bocoa, tribe in the Papilionoideae Closed calyx in bud splitting in various ways at
Candolleodendron anthesis, frequently numerous stamens, and
Aldina group: Aldina, Baphiopsis, single or lacking petal
Cordyla, Mildbraediodendron
Lecointea group: Lecointea,
Harleyodendron, Exostyles, Zollernia,
Holocalyx,
Ateleia group: Ateleia, Cyathostegia,
Amburana

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Molecular systematics of the Swartzieae
 TABLE 2. Voucher details for extra accessions not included in Pennington et al. (2000b)

222
Taxon Locality Voucher

Amburana cearensis (Allemão) A.C. Sm. Brazil: Bahia. Bridgewater 1011 (E)
Ateleia albolutescens Mohlenbr. Mexico: Chiapas, Cintalapa. Linares 4330 (K)
Ateleia arsenii Standl. Mexico: Michoacan, Morelia. Linares 4484 (K)
Cyathostegia mathewsii (Benth.) Schery Ecuador: Loja. Klitgaard 377 (K)
Bocoa alterna (Benth.) R.S. Cowan Peru: Loreto, Panguana. Morawetz 12-71085 (NY)
Advances in Legume Systematics 9

Bocoa decipiens R.S. Cowan
Bocoa racemulosa (Huber) R.S. Cowan
Bocoa viridiflora (Ducke) R.S. Cowan
Harleyodendron unifoliatum R.S. Cowan
Lecointea marcano-bertii Barneby
Mildbraediodendron excelsum Harms
Swartzia arborescens (Aubl.) Pittier
Swartzia simplex (Sw.) Sprengel
Swartzia sp. nov.
Swartzia sp.
Brazil: Maranhão, Sant Luzia.
Brazil: Amazonia, Figueredo.
Brazil: Amazonia, Manaus.
Brazil: Bahia, Itacaré.
Venezuela: Barinas, Pedraza.
Cameroon.
Surinam: Bassin du Litany.
Colombia: Antioquia, Rio Claro.
Brazil: Maranhão, Loreto.
Ecuador: Napo, Jatun Sacha.
Lobo et al. 334 (F)
Ferreira 6990 (K)
Nascimiento et al. 645 (MO)
Harley 18333 (K)
Dorr et al. 4914 (K)
Kew living collections accession 1997–6092
Granville et al. 11947 (K)
R.T. Pennington 686 (E)
Ratter 7433 (K)
R.T. Pennington 650 (E)
 Molecular systematics of the Swartzieae

The analysis presented here excluded the areas with high quantities of missing
data and included gap characters. Cladistic analysis of 1095 characters (including 29
gap characters) of which 244 were informative generated 3898 equally most
parsimonious trees, with a length of 736 steps, a consistency index (CI) of 0.73 and a
retention index (RI) of 0.79. Figure 1 shows the strict consensus tree. Table 3
summarises the effects of sensitivity analyses on the tree statistics, and tree topology.
Swartzieae are clearly polyphyletic. Swartzieae genera emerge in four main clades and
many are more closely related to Sophoreae and Dalbergieae than they are to other
Swartzieae. In all sensitivity analyses these four clades remain monophyletic, but the
relationship between them changes (Table 3).
The first clade (hereafter referred to as the ‘swartzioid’ clade, of Pennington et al.,
2000b) consists of Swartzia, Bobgunnia, Ateleia, Cyathostegia and Bocoa. Within it, species
of Bocoa occur in two clades. Bocoa viridiflora (Ducke) R.S. Cowan emerges with
Swartzia (with 100% bootstrap). Bocoa alterna (Benth.) R.S. Cowan, B. decipiens R.S.
Cowan, B. mollis (Benth.) R.S. Cowan and B. racemulosa (Huber) R.S. Cowan group
with Ateleia and Cyathostegia (100% bootstrap), and a gap of 35 bases between
positions 361 and 395 in the data matrix unites these taxa. Examination of the
individual most parsimonious trees revealed that Bobgunnia emerges either as sister to
Swartzia, or sister to the swartzioid clade. In some sensitivity analyses, Cladrastis Raf.
and Styphnolobium Schott emerge in this swartzioid clade. The swartzioid clade is sister
to the remainder of the Papilionoideae, though this relationship is weakly supported
and breaks down in sensitivity analyses (Table 3).
Aldina, Cordyla, Mildbraediodendron, and Amburana form a group within the second
major clade (the ‘aldinoid’ clade), which also contains the Sophoreae genera
Myrospermum Jacq. and Dussia Krug and Urb. ex Taub. (86% bootstrap). In this
analysis Castanospermum A. Cunn. ex Hook., Xanthocercis Baill., and Angylocalyx Taub.
of the Sophoreae (sensu Polhill, 1994) and Pterodon Vogel and Dipteryx Schreb. of the
Dipterygeae also emerge in the aldinoid clade. Their inclusion in this clade is weak
with no bootstrap support. In the analysis of Pennington et al. (2000b) these taxa do
not group with the aldinoid clade but emerge independently.
The remainder of the Papilionoideae emerge in a more derived monophyletic
group with a bootstrap value of 59%, which is a higher level of support than this clade
received in the intron-only analysis of Pennington et al. (2000b). In some sensitivity
analyses this clade collapses (Table 3). This group is largely consistent with the
presence of a 50 kilobase inversion on the chloroplast genome, which is present in
the bulk of the Papilinoideae but absent in some members of the Swartzieae and
Sophoreae (Doyle et al., 1996). The occurrence of this inversion is indicated on the
cladogram. Aldina, which was found to possess the inversion, groups in a clade of taxa
which were found not to possess the inversion.
Polhill’s (1994) Lecointea group is divided in this analysis. Zollernia, Holocalyx, and
Lecointea emerge together with Uribea Dugand and Romero from the Sophoreae
within a third major clade (hereafter refered to as the ‘lecointeoid’ clade).
Relationships at the base of this clade are unresolved, and its bootstrap value is low
(56%). The remaining genera of the Lecointea group, Harleyodendron and Exostyles,
form a group within the fourth major clade (the ‘vataireoid’ clade of Pennington et
al., 2000b), which also contains Sweetia, Vatairea, Luetzelburgia, and Vataireopsis, with a
bootstrap of 99%. Baphiopsis emerges with Baphia from the Sophoreae and these two
taxa are weakly supported as sister to the vataireoid clade (55% bootstrap). The
branch length for the clade containing Baphiopsis and Baphia is long (40 bases).
The results of this analysis are largely consistent with the intron-only analysis of
Pennington et al. (2000b), with the same major swartzioid, vataireoid, lecointeoid,
and aldinoid clades emerge. In our analysis there is slightly more resolution and
support values are often higher.

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Advances in Legume Systematics 9

FIG. 1. Strict consensus tree of analysis with areas of missing data excluded and gaps coded, with
bootstrap values indicated above the branches. Names in upper case letters denote
Swartzieae taxa (sensu Polhill, 1994). The presence (+) or absence (-) of the 50 kilobase
inversion is indicated next to the taxon name.

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 Molecular systematics of the Swartzieae

Discussion

The results of this analysis confirm that the Swartzieae is polyphyletic, which is
consistent with much of the recent literature. Ferguson and Schrire (1994) were
among the first to suggest this in a study of pollen morphology of the Swartzieae. In
their cladistic analysis Swartzieae genera emerged in two separate clades; Swartzia,
Candolleodendron, Bocoa viridiflora (Polhill’s (1994) Swartzia group), and Aldina,
grouping in one clade with the Caesalpinioideae outgroups and the remainder of the
Swartzieae emerging in a different clade. These results were largely congruent with
those of Herendeen’s (1995) morphological phylogenetic analysis, in which Polhill’s
(1994) Swartzia group and Aldina group were united in one clade with some
Sophoreae genera, whilst the Lecointea group and the Ateleia group emerged in a
separate clade with other Sophoreae genera. In contrast, our results unite the
Swartzia group with the Ateleia group in the swartzioid clade, except for Amburana,
which emerges with some of the Aldina group in the aldinoid clade, whilst the Aldina
group and the Lecointea group emerge in separate clades.
One of the most striking results is the grouping of Swartzia, Bobgunnia, Bocoa,
Ateleia, and Cyathostegia in a clade that is sister to the remaining Papilionoideae. If
classification is to depend on monophyly then this has exciting implications for the
classification of the Swartzieae because it raises the possibility of redefining it to
include only these five genera. The remaining genera of Swartzieae might be placed
in an expanded Sophoreae, as suggested by Herendeen (1995). However, both this
analysis, and more particularly that of Pennington et al. (2000b), show these
Swartzieae genera to be members of disparate clades, such as the vataireoid and
aldinoid clades, containing other genera of various tribes including Dipterygeae and
Dalbergieae. It thus seems more likely that these Swartzieae would be moved to other
tribes. Some of these tribes await circumscription if well supported groups such as the
vataireoid clade are to be given tribal status.
The swartzioid clade is consistently monophyletic in all analyses. The association
of these five genera has never before been hypothesised. For a long time Ateleia and
Cyathostegia were generally included in the Sophoreae, whilst Swartzia and Bocoa were
included in the Swartzieae (Polhill and Raven, 1981), until Polhill (1994)
transferred the former genera to the Swartzieae. The unusual occurrence of a
meristem ring in the flower, which is visible at the early stages of development, unites
Ateleia (Tucker, 1990), Cyathostegia (Tucker, 2000), and Swartzia (Tucker, 2000).
Mildbraediodendron, which does not emerge in the swartzioid clade, also has this
feature (Tucker, 2000), and thus it is not unique to the swartzioid clade. The group
is further supported in Doyle et al.’s (1997) analysis of rbcL sequence data in which
Ateleia and Swartzia group together, and Aldina and Holocalyx emerged in a separate
clade. The association of Ateleia, Cyathostegia, and Swartzia is also corroborated by the
presence of root nodules, which are absent in other basal papilionoids such as most
members of the aldinoid and vataireoid clades (Sprent, 2000). Bobgunnia, described
by Kirkbride and Wiersema (1997), comprises two species originally described in
Swartzia (S. fistuloides Harms and S. madagascariensis Desv.) and its separation from
Swartzia is not universally accepted. Although unresolved from the remaining
Swartzia species in the strict consensus tree, its separation from Swartzia is supported
here because it emerges as sister to Swartzia in some of the most parsimonious trees
and in sensitivity analyses, and in the remaining most parsimonious trees it is sister
to the swartzioid clade..
There is strong support for the grouping of Ateleia and Cyathostegia with Bocoa
mollis, B. alterna, B. decipiens, and B. racemulosa (100% bootstrap). Whilst the
similarities between Ateleia and Cyathostegia have long been recognised (Rudd, 1968;
Austin et al., 1987; Ferguson and Skvarla, 1988), Bocoa has rarely been associated with
these genera, except when Bentham (1870) first described Swartzia matthewsii Benth.
(= Cyathostegia matthewsii (Benth.) Schery) and mentioned that the alternate leaflets

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 TABLE 3. Effects of sensitivity analyses on tree statistics and topology.

226
Data included/excluded CI RI Number Tree Effects on tree topology,
of trees length compared to topology in Fig. 1

Raw data (all data included)
0.7485 0.7917 12012 660 Swartzioid clade still sister to the
Papilionoideae, but Cladrastis and
Styphnolobium also emerge in this clade.
The clade possessing the 50 kilobase
inversion collapses.
Advances in Legume Systematics 9

Alignment variable 0.7555 0.8011 287 589 The swartzioid clade and the aldinoid clade
areas excluded emerge as more derived than the clade
marked by the presence of the 50 kilobase
inversion. Cladrastis and Styphnolobium emerge
in the swartzioid clade.

Areas of missing data
included (characters no.
765-775; 874-9001;
1008-1088)
0.7333 0.7381 9450 930 Swartzioid, aldinoid, lecointeoid and
vataireoid clades remain monophyletic
but relationships between them are
unresolved. The clade possessing the
50 kilobase inversion collapses.

Sweetia, Luetzelburgia, 0.7486 0.7998 3897 692 No change in tree topology.

Vatairea and Vataireopsis,
excluded
 Molecular systematics of the Swartzieae

and uniform anthers were very similar to those of Swartzia alterna Benth. (= Bocoa
alterna). A more detailed species level analysis using the Internal Transcribed Spacer
region (ITS) of the nuclear genome is currently being undertaken by the first author
to resolve more clearly the relationships within this clade.
The division of Bocoa in our analysis agrees with previous suggestions that the genus
is not a natural group, and that the species might belong to more than one genus. The
separation of B. viridiflora from B. alterna, B. decipiens, B. mollis, and B. racemulosa is
consistent with Herendeen’s (1995) division of the genus into those species with
alternate leaflets, including B. alterna, B. mollis, and B. decipiens, and those with opposite
leaflets, including B. viridiflora. The emergence of B. viridiflora nested within Swartzia in
this analysis is supported by pollen morphology (Ferguson and Schrire, 1994), and
wood anatomy (Gasson, 1996). In the light of this evidence the generic position of B.
viridiflora must be reassessed; its inclusion in Swartzia might be more appropriate.
No sequence was obtained for Candolleodendron, but we suspect that it will emerge
in the swartzioid clade, because its general aspect is reminiscent of Swartzia and Bocoa
(Cowan, 1966), and its flower structure is very similar to that of Swartzia (Pennington
et al., 2000a).
The association of Cordyla, Mildbraediodendron, and Aldina, which represent three
out of the four genera in Polhill’s (1994) Aldina group, with Amburana in the aldinoid
clade is confirmed in Pennington et al. (2000b), and has not been suggested before
in the literature. The floral morphology of Amburana is unusual (Pennington et al.,
2000a); although it has the superficial appearance of a papilionoid flower, it has a
single petal, which has often lead authors to group it with Ateleia and Cyathostegia
(Polhill, 1994; Herendeen, 1995). It has a long hypanthium, to which the ovary is
fused. It might represent an intermediate morphology between a typical papilionoid
flower and the unusual floral forms in Aldina, Cordyla and Mildbraediodendron. Cordyla
and Mildbraediodendron are unusual amongst legumes in that they lack petals and this
feature is also apparent in some species of Bocoa and Swartzia. Cordyla and
Mildbraediodendron lack nodules, however, which differentiates them from Swartzia
and other members of the swartzioid clade, all of which nodulate, except for Bocoa
(Sprent, 2000). The presence of a hypanthium in Aldina, Cordyla, Mildbraediodendron,
and Amburana further separates these genera from the swartzioid clade (Pennington
et al., 2000a). Cowan (1981) noted that Cordyla and Mildbraediodendron ‘appear to
have little in common with Swartzia except an entire calyx, which is possibly the result
of convergence’.
One feature that the swartzioid clade and the aldinoid clade (except Aldina) have in
common is the absence of the 50 kilobase inversion on the chloroplast genome (Doyle
et al., 1996). This inversion is present in most Papilionoideae, but absent in the
Caesalpinioideae and Mimosoideae (Doyle et al., 1996). Swartzieae and Sophoreae are
heterogeneous for the inversion, suggesting that these tribes are not monophyletic if
the mutation arose only once. Our results are largely consistent with Doyle et al.’s
(1996) suggestion that the inversion was a unique event. Aldina, however, which was
recorded as possessing the inversion, emerges in a clade of genera that lack it. In the
light of this result, the position of Aldina must be re-examined, and more species should
be screened for the 50 kilobase inversion to confirm its presence in the genus.
The separation of Harleyodendron and Exostyles from Holocalyx, Zollernia, and
Lecointea (the genera which made up Polhill’s (1994) Lecointea group) is supported in
the intron-only analysis (Pennington et al., 2000b), and has not previously been
hypothesised in the literature. The emergence of Holocalyx with these genera is
notable because its systematic position has been unclear in the past. Taubert (1891)
first included it in the Swartzieae, but Cowan (1981) later referred it to the
Sophoreae, and Polhill (1994) finally returned it to the Swartzieae.
The association of Baphiopsis with Baphia in our cladogram is supported by
Herendeen’s (1995) morphological analysis, and studies of pollen morphology
(Ferguson and Skvarla, 1988). Polhill (1994) included it in the Aldina group because

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of its six petals and numerous stamens, but it is otherwise very similar
morphologically to Baphia in the Sophoreae. The emergence of Baphiopsis and Baphia
as sister to the vataireoid clade is probably erroneous, illustrated by the low bootstrap
of 55%, and is probably due to an absence of more derived placeholders in this
analysis. In the Pennington et al. (2000b) analysis Baphiopsis and Baphia emerge in a
separate clade with Bowringia, Leucomphalos, Airyantha, and Dalhousiea, which are all in
Polhill’s (1994) Baphia group of the Sophoreae, and this ‘baphioid’ group is in a
clade containing placeholders for various more derived papilionoids, such as
Millettieae, Desmodieae, and Robinieae.
The systematic position of the Swartzieae has been uncertain, as illustrated in
Table 1. Much of the literature in the late 1970s and 1980s, which followed the
International Legume Conference in Kew in 1978, supported the placement of the
Swartzieae in the Papilionoideae. Baretta-Kuipers (1981) compared the wood
anatomy of the Swartzieae with that of the Caesalpinioideae and woody
Papilionoideae, and found that the advanced ray features and the storeying of all
elements in all genera of the Swartzieae surveyed matched the Papilionoideae. Of the
species surveyed by Behnke and Pop (1981) in their study of sieve element plastids
and ‘Crystaline’ P-proteins in the phloem of legumes, one member of the Swartzieae
was included, Swartzia crocea Benth., and it was found to be more similar to the
Papilionoideae than the Caesalpinioideae. Corby (1981) included Swartzia in the
Papilionoideae because it regularly forms nodules, a feature that is common in the
Papilionoideae, but infrequent in the Caesalpinioideae. Ingham (1981) discovered
the production of isoflavonoid phytoalexins in Swartzia madagascariensis Desv. (=
Bobgunnia madagascariensis (Desv.) Kirkbr. and Wiersema), S. leiocalycina Benth., S. ulei
Harms, Aldina heterophylla Benth., Cordyla africana Lour, and Mildbraediodendron excelsa
Harms, which are not found in the Caesalpinioideae, but appear to be a feature of
some papilionoid legumes, supporting the tribe’s inclusion in the Papilionoideae.
Based on these studies, Cowan (1981) placed the Swartzieae in a relatively less
advanced position in the Papilionoideae. Some of the more recent studies do not
support this basal placement. For example in Herendeen’s (1995) analysis, neither
his most parsimonious trees nor any of the trees produced from experimenting with
the data resulted in the Swartzieae emerging as basal in the Papilionoideae, and he
concluded that ‘the concept of the Swartzieae as the basal tribe of Papilionoideae …
should be abandoned’ and that the Swartzieae should be subsumed within an
expanded Sophoreae. Gasson (1996), who found that there is no clear delimitation
between the Swartzieae and the Sophoreae based on 12 wood anatomical characters,
supported this view.
In contrast to the view that Swartzieae are papilionoid, Ferguson and Skvarla
(1991) suggested that their analysis of Swartzieae pollen demonstrated that the pollen
characters of Swartzia are specialised and that the Swartzieae might represent a
‘specialised offshoot arising near the Amherstieae and Detarieae in the
Caesalpinioideae.’ Ferguson and Schrire (1994) found that the pollen of
Candolleodendron, Bocoa viridiflora, and perhaps Aldina also appears to be closer to the
Amherstieae and Detarieae in the Caesalpinioideae than to the Sophoreae in the
Papilionoideae. The placement of the Swartzieae in the Caesalpinioideae is further
supported by floral morphological studies. Missing floral organs are common in the
Caesalpinioideae, leading workers to consider various Swartzieae to be close to the
Caesalpinioideae because they too lack organs. Most examples of missing floral
organs can be found in the Caesalpinioideae. Total absence of four out of the five
petals, even at the earliest stages of development of the bud, has been reported in
Ateleia herbert-smithii Pittier (Tucker, 1989, 1990). Several other genera, including
Cyathostegia, Candolleodendron, and some Bocoa species also have only one petal, and
Mildbraediodendron, Cordyla and some species of Swartzia and Bocoa lack petals
altogether. This suggests a close affinity to the Caesalpinioideae.

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 Molecular systematics of the Swartzieae

In our analysis most Swartzieae are nested within clades containing genera of other
papilionoid tribes, and this clearly places these Swartzieae taxa in the Papilionoideae.
Unlike these clades, the swartzioid clade contains only Swartzieae genera and because
of its sister relationship to the rest of the Papilionoideae in some analyses the
subfamilial placement of these taxa is less clear. If the sister relationship of the
swartzioid clade is corroborated in further studies, our analysis might support
recognition of a fourth subfamily, as originally advocated by De Candolle (1825),
Bartling (1830), Endlicher (1840) and Corner (1951). In sensitivity analyses this sister
relationship breaks down, and the occasional inclusion of Cladrastis and Styphnolobium
in the swartzioid clade illustrates the poor support for this clade. Such a taxonomic
decision is therefore premature, and the swartzioid clade should be provisionally
retained in the Papilionoideae until further evidence is gathered to confirm its
relationship and placement.

Conclusions

The Swartzieae, as traditionally circumscribed, is polyphyletic. This analysis

corroborates the coherence of genera within some of Polhill’s (1994) informal
groups of the Swartzieae, but some genera, including Amburana and Baphiopsis, are
widely separated from the informal group to which they were assigned. The
emergence of Swartzia, Bobgunnia, Bocoa, Ateleia, and Cyathostegia in the swartzioid
clade at the base of the Papilionoideae raises interesting questions about redefining
the Swartzieae to include just this clade, or indeed recognising it as a fourth subfamily
of legumes. Support for this placement of the swartzioid clade is low, however, and
such taxonomic decisions require further evidence. The remaining genera of the
tribe should be retained in the Papilionoideae, but will probably need to be removed
from the Swartzieae and included in other tribes.

Acknowledgements

We thank Dr Brian Schrire for comments and suggestions on drafts of this paper,
Dr Gwil Lewis for his general guidance, the staff in the Jodrell laboratory at the Royal
Botanic Gardens Kew, Glasgow University Taxonomy Centre and the Systematics
Association for awarding an NERC grant to help fund the costs of the molecular
work, The Royal Botanic Garden Edinburgh Trustees Molecular Phylogenetics
Project for financial support, British Airways for donating a free flight to Mexico for
fieldwork, Paul Smith for collecting Bobgunnia, the New York Botanical Garden,
Field Museum, Chicago, and Missouri Botanical Garden for the loan of plant
material for DNA extraction.

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