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Botanical Journal of the Linnean Society, 2013, 173, 387–406. With 2 figures
Phylogenetic relationships and new tribal delimitations
in subfamily Ixoroideae (Rubiaceae)
KENT KAINULAINEN1,2*, SYLVAIN G. RAZAFIMANDIMBISON1,2 and
BIRGITTA BREMER1,2
1
Bergius Foundation, The Royal Swedish Academy of Sciences, SE-106 91 Stockholm, Sweden
Department of Ecology, Environment and Plant Sciences, Stockholm University, SE-106 91
Stockholm, Sweden
2
Received 4 April 2012; revised 2 October 2012; accepted for publication 31 January 2013
Subfamily Ixoroideae is one of three major lineages in Rubiaceae, with approximately 4000 species. Previous
molecular phylogenetic studies have indicated that many genera and tribes previously placed in other subfamilies
are better considered as part of Ixoroideae. However, the internal resolution and clade support have generally been
low, and several genera found to be nested in the subfamily do not appear to be associated with any described tribe.
In order to resolve the phylogeny and assess the tribal delimitations in the expanded Ixoroideae, phylogenetic
reconstructions were performed using Bayesian and parsimony analyses of six plastid DNA regions and a broad
sampling of genera from all tribes of the subfamily. In the inferred phylogenetic hypotheses, the tribal relationships
were mostly well supported, with Ixoroideae consisting of the Coffeeae and the Vanguerieae alliances as sister
groups and a grade comprising Condamineeae, Henriquezieae, Posoquerieae, Retiniphylleae, Sipaneeae and the
genus Steenisia. A revised tribal classification, including the description of five new tribes, Airospermeae,
Augusteae, Scyphiphoreae, Steenisieae and Trailliaedoxeae, is provided. © 2013 The Linnean Society of London,
Botanical Journal of the Linnean Society, 2013, 173, 387–406.
ADDITIONAL KEYWORDS: Airospermeae – Augusteae – molecular phylogenetics – Scyphiphoreae –
Steenisieae – systematics – Trailliaedoxeae.
INTRODUCTION
With >13 000 species (Davis et al., 2009), Rubiaceae is
one of the largest and most diverse families of
angiosperms. Well-known representatives include
Coffea L., Ixora L. and Gardenia J.Ellis, all part of
Ixoroideae, a subfamily comprising about 4000 species
of pantropical and subtropical distributions. Ixoroideae, as recognized by Bremekamp (1952, 1966),
included taxa characterized by secondary pollen presentation (‘ixoroid pollination mechanism’), a feature
that Bremekamp considered to be of high taxonomic
value because of its requirement for a combination of characters for functionality. Included were
tribes Acranthereae, Chiococceae, Coptosapelteae,
Cremasporeae, Gardenieae, Ixoreae and Vanguerieae.
Verdcourt (1958), however, considered pollen presentation to be of less importance, and preferred to
*Corresponding author. E-mail: kent@bergianska.se
include Ixoroideae in a wide Cinchonoideae (see also
Robbrecht & Manen, 2006). In a comprehensive classification of the family, Robbrecht (1988) restricted
Ixoroideae to include genera with contorted corolla
lobe aestivation and fleshy fruits. In his system,
Ixoroideae comprised tribes Cremasporeae, Gardenieae and Ixoreae sensu Bremekamp (the correct
name of which would have been Coffeeae; Darwin,
1976), i.e. Aulacocalyceae, Coffeeae, Gardenieae,
Octotropideae and Pavetteae. For an overview of the
changes in the classification of Ixoroideae, the reader
is referred to Andreasen & Bremer (2000).
Results of molecular phylogenetic studies have since
then indicated many unknown relationships and also,
consequently, possible improvements in the classification of Rubiaceae. This includes the expansion of
Ixoroideae, as many additional tribes or segregates of
tribes and a number of taxa of uncertain taxonomic
placement have been shown to be associated with the
subfamily. Ixora, the type of the subfamily, was shown
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 387–406
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K. KAINULAINEN ET AL.
to form a clade with Vanguerieae (Bremer et al., 1999),
confirming the position of Vanguerieae in Ixoroideae,
as suggested by Bremekamp (1952, 1966), and supporting the exclusion of Ixora from Pavetteae.
Andreasen & Bremer (2000) resurrected Ixoreae and
provided new circumscription for several other tribes
in the subfamily. Many additional taxa have been
found to be associated with Ixoroideae sensu Robbrecht
(1988), including Bertiera Aubl. (Bremer, Andreasen &
Olsson, 1995), Mussaendeae and Sabiceeae, (Bremer &
Thulin, 1998), Alberteae and Scyphiphora C.F.Gaertn.
(Bremer et al., 1999), Condamineeae and many genera
formerly placed in Cinchoneae or Rondeletieae (e.g.
Bremer et al., 1999; Rova et al., 2002; Delprete &
Cortés-B., 2004; Kainulainen et al., 2010). Crossopteryx Fenzl, part of Ixoroideae sensu Bremekamp
(included in Coptosapelteae), but considered part of
Cinchoneae by Robbrecht (1988), has also been found
to be nested in Ixoroideae (Razafimandimbison &
Bremer, 2001), as have Mussendopsis (Razafimandimbison & Bremer, 2001), Hekistocarpa Hook.f. (Dessein
et al., 2001), Gleasonia Standl., Retiniphyllum Humb.
& Bonpl. and Sipaneeae (Rova et al., 2002; Delprete &
Cortés-B., 2004), Boholia Merr. and Steenisia Bakh.f.
(Bremer & Eriksson, 2009), Airosperma K.Schum. &
Lauterb. (Kainulainen et al., 2009), Greeniopsis Merr.
(Alejandro et al., 2010), Glionnetia Tirveng., Jackiopsis Ridsdale and Trailliaedoxa W.W.Sm. & Forrest
(Razafimandimbison et al., 2011). Although the
expanded Ixoroideae is well supported by molecular
data, internal resolution and clade support, especially
among the early divergent clades, have generally been
low.
Ixoroideae, as widely delimited according to recent
molecular phylogenetic studies, includes all tribes of
Robbrecht’s (1988) narrow circumscription of the subfamily, whereas tribes Acranthereae, Chiococceae and
Coptosapelteae are not part of Ixoroideae as suggested by Bremekamp (1966). Chiococceae has been
shown to be part of Cinchonoideae (Bremer et al.,
1995), and Acranthera Arn. ex Meisn. and Coptosapelta Korth. appear to represent a separate, early
divergent clade in the family (Rydin et al., 2009). The
expanded Ixoroideae is morphologically diverse and
can no longer be easily characterized morphologically.
Molecular phylogenetic studies have also shown that
some tribes of the subfamily are not monophyletic (i.e.
Gardenieae including Aulacocalyceae, and Pavetteae;
Andreasen & Bremer, 2000; Persson, 2000; Bremer &
Eriksson, 2009) and that several genera found to be
nested in Ixoroideae do not appear to be associated
with any described tribe, i.e. Airosperma, Aleisanthia
Ridl., Aleisanthiopsis Tange, Augusta Pohl, Boholia,
Glionnetia, Greenea Wight & Arn., Scyphiphora,
Steenisia, Trailliaedoxa and Wendlandia Bartl. ex
DC. (Rova et al., 2002; Bremer & Eriksson, 2009;
Kainulainen et al., 2009; Razafimandimbison et al.,
2011). Subsequent tribal recognition of the lineages
represented by these genera has so far only been
performed for Aleisanthia and Aleisanthiopsis and
Greenea (Aleisanthieae and Greeneeae, respectively;
Mouly et al., 2009a).
In this study, we analyse data from six combined
plastid DNA regions (matK, ndhF, rbcL, the rps16
intron, trnS-G and trnT-F) using Bayesian and parsimony methods of phylogenetic reconstruction to
resolve the tribal relationships of the expanded
Ixoroideae and, in particular, the relationships of the
genera which, in previous studies, have not been
associated with any previously described tribes. Following the inferred phylogenetic hypothesis, we also
provide a revised tribal classification of the subfamily.
MATERIAL AND METHODS
TAXON SAMPLING
This study includes genera representing all tribes
associated with Ixoroideae in previous molecular phylogenetic studies. The ingroup included 110 species
from 87 genera. An effort was made to sample primarily material representing the types of genera. Gelsemium sempervirens (L.) J.St.-Hil. (Gelsemiaceae),
Logania vaginalis (Labill.) F.Muell. (Loganiaceae),
Luculia gratissima (Wall.) Sweet, Colletoecema dewevrei (De Wild.) E.M.A.Petit, Ophiorrhiza mungos L.
and six species of Cinchonoideae were utilized as
outgroup. Because the focus of the study is primarily
concerned with the phylogeny of the early divergent
lineages of the subfamily, sampling was limited in the
large and problematic Gardenieae and associated
tribes (Octotropideae and Pavetteae), the phylogeny
of which will be investigated further in an upcoming
study (A. Mouly et al., Université de Franche-Comté,
Besançon, unpubl. data). Sampling was increased for
Airosperma, Augusta and Wendlandia, all of which
have widely disjunct distributions and in previous
molecular phylogenetic studies have been resolved in
Ixoroideae, but not in association with any previously
recognized tribes (Rova et al., 2002; Kainulainen
et al., 2009). We were able to obtain sequences
of Airosperma taxa from New Guinea and Fiji, including A. trichotomum (Gillespie) A.C.Sm., originally
described as Abramsia trichotoma Gillespie. The
Augusta sample comprised specimens of the type
A. longifolia (Spreng.) Rehder from Brazil, A. austrocaledonica (Brongn.) J.H.Kirkbr. from New Caledonia
and A. rivalis (Benth.) J.H.Kirkbr. from Central
America, the last two species of which were previously recognized as Lindenia Benth. The Wendlandia
sample included W. arabica Deflers and W. ligustroides (Boiss. & Hohen.) Blakelock, the inclusion of
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 387–406
PHYLOGENY OF IXOROIDEAE
which in Wendlandia was considered to be doubtful in
the last comprehensive revision of the genus by
Cowan (1932). We were unsuccessful in obtaining
DNA sequences from any Steenisia spp. other than
S. pleurocarpa (Airy Shaw) Bakh.f. An overview of the
sampling and voucher specimens is given in the
Appendix, and a few species representing the different tribes of Ixoroideae are shown in Figure 1.
DNA
EXTRACTION, AMPLIFICATION AND SEQUENCING
Three protein coding genes (matK, ndhF and rbcL)
and three noncoding regions [the rps16 intron, the
trnS-G spacer including the trnG intron (trnSGCUtrnGUUC-trnGUUC) and the trnT-F region (trnTUGUtrnLUAA-trnLUAA-trnFGAA)] of the plastid DNA,
previously shown to be phylogenetically informative
in Rubiaceae (Andersson & Rova, 1999; Bremer et al.,
1999; Razafimandimbison & Bremer, 2002; Rova
et al., 2002; Andersson & Antonelli, 2005;
Kainulainen et al., 2009), were used in this study.
DNA was extracted from leaf material using a MiniBeadbeater 3110BX (BioSpec), following the protocol
of Doyle & Dickson (1987), and was subsequently
purified using the QIAquick® PCR purification kit
according to the manufacturer’s instructions
(Qiagen). PCR amplifications were performed using
standard PCR settings and the following primers:
matK1198F and matK2053R (Andersson & Antonelli,
2005) for matK; 2F, 1000R, 720F, 1700R, 1320F and
2280R (Rydin, Razafimandimbison & Bremer, 2008)
for ndhF; rbcL5’F, rbcL_Z895F, rbcL_Z895R and
rbcL3’R (Bremer et al., 2002) for rbcL; rsp16_2F
(Bremer et al., 2002) and rpsR2 (Oxelman, Lidén &
Berglund, 1997) for the rps16 intron; and cF, eF, dR,
fR (Taberlet et al., 1991), A1F, IR (Bremer et al.,
2002), 820R, 940F, 1250F, 1880F and 2670R (Rydin
et al., 2008) for trnT-F. The trnS-G region was amplified using the primers and protocols of Shaw et al.
(2005). Sequences were assembled using the Staden
package v1.5.3 (Staden, 1996). Sequences new to this
study (324) were deposited in GenBank (Appendix).
Additional sequences (361) were obtained from
GenBank (for references, see Appendix).
DATA
ANALYSES
The sequences were preliminarily aligned using
Clustal W (default settings; Thompson, Higgins &
Gibson, 1994), as implemented in BioEdit (Hall,
1999), and then adjusted manually. Sequence inversions were dealt with by separating the alternative
sequence versions in the alignment. Inversions in the
included sequences occurred in regions corresponding
to positions 5417–5430 (rps16), 9082–9113, 9164–
9169, 9330–9335 and 9714–9723 (trnS-G) of the
389
Coffea arabica L. plastid genome (GenBank accession
number, EF044213; Samson et al., 2007). An AT-rich
region in the trnS-G spacer, corresponding to positions 9184–9203 of the C. arabica plastid genome,
was excluded from the analyses because of difficulties
in finding an unambiguous alignment. The combined
dataset consisted of 10 165 characters, 10 003 of
which were included in the analyses. Methods of
phylogenetic reconstruction included maximum parsimony (MP) and Bayesian inference (BI; Yang &
Rannala, 1997), using the programs PAUP* v4.0b10
(Swofford, 2002) and MrBayes v3.1.2 (Huelsenbeck &
Ronquist, 2001; Ronquist & Huelsenbeck, 2003),
respectively. Gaps were treated as missing data. MP
analyses were performed using heuristic searches
with the tree bisection–reconnection (TBR) branch
swapping algorithm, Multrees on, 1000 random
sequence addition replicates and a maximum of 10
trees saved per replicate. Clade support was estimated using 1000 bootstrap replicates, with three
random addition replicates per replicate. For the BI
analyses, the protein coding and noncoding data were
analysed as separate partitions with unlinked model
parameter estimates (except topology). Substitution
models suggested as best fit to the data under the
corrected Akaike information criterion (AICc), as
implemented in MrAIC v1.4.4 (Nylander, 2004; a
script dependent on the program PHYML v3.0;
Guindon & Gascuel, 2003), were used for each partition (the GTR + G + I model for both datasets). The
analysis comprised two runs of four chains each and
was monitored for 107 generations, with every 1000th
generation being sampled. The chain heating parameter was 0.10. The initial 25% of the sampled trees
were considered as burn-in and excluded from the
consensus. The effective sample sizes (ESSs) of the
model parameters were checked using the program
Tracer v1.5 (Rambaut & Drummond, 2007), in order
to ensure an ESS > 200, as recommended by
Drummond et al. (2007) for the adequate representation of the posterior probability (PP).
RESULTS
The combined dataset contained 10 003 DNA characters, 2410 of which were potentially phylogenetically
informative in the MP analysis. Analyses of the coding
and noncoding datasets separately (data not shown)
showed no incongruences with bootstrap support (BS)
values ⱖ70% or PPs ⱖ 0.95, with the exception of the
position of Randia L., which formed a sister group to
Euclinia Salisb. (PP, 0.99; BS, 73%) in the coding
dataset, but was resolved as sister group to a clade
comprising Rosenbergiodendron Fagerl. and Tocoyena
Aubl. in the noncoding dataset (PP, 0.95; BS, 84%). The
inferred phylogenetic hypotheses of the MP and BI
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 387–406
390
K. KAINULAINEN ET AL.
A
B
E
F
G
H
G
I
J
J
K
L
C
M
D
N
Figure 1. Selected taxa of Ixoroideae: A, Posoqueria longiflora; B, Schizomussaenda henryi; C, Bremeria pervillei; D,
Sabicea diversifolia; E, Steenisia pleurocarpa; F, Scyphiphora hydrophylacea; G, Glionnetia sericea; H, Ixora borboniae; I,
Augusta rivalis; J, Wendlandia tinctoria; K, Bertiera rufa; L, Pavetta sp.; M, Mitriostigma axillare; N, Rosenbergiodendron
densiflorum (image credits: A–D, G, H, K–N, by Kent Kainulainen; E, F, J, © Christian Puff, Faculty Centre of Biodiversity,
University of Vienna; used with permission; I, by Indiana Coronado, Tropicos, botanical information system at the Missouri
Botanical Garden – http://www.tropicos.org, © MBG, licensed under a Creative Commons by-nc-nd 3.0 licence).
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 387–406
PHYLOGENY OF IXOROIDEAE
analyses were overall mostly congruent, well resolved
and strongly supported. Figure 2 shows the majority
rule consensus tree from the BI analyses of the combined data, including the PPs of the clades and the
clade BS values of the MP analysis.
The clades corresponding to the Coffeeae and Vanguerieae alliances, respectively (cf. Razafimandimbison et al., 2011), were resolved as sister groups
(‘the core Ixoroideae’; PP, 1.00; BS, 100%). The Coffeeae
alliance comprised the tribes Alberteae, Bertiereae,
Coffeeae, Gardenieae, Octotropideae and Pavetteae
and the genera Airosperma, Augusta, Boholia and
Wendlandia. Gardenieae did not appear to be monophyletic, because Burchellia R.Br. was resolved as
sister group to Octotropideae (PP, 1.00; BS, 64%), and
Mitriostigma Hochst. and Oxyanthus DC. formed a
sister group to Pavetteae, although with weak support
(PP, 0.80; BS, 54%). The Gardenieae–Pavetteae clade
was resolved as sister group to the Burchellia–
Octotropideae clade (PP, 1.00; BS, 65%), and a clade
comprising Bertiereae and Coffeeae (PP, 1.00; BS,
98%), in turn, formed a sister group to this clade (PP,
1.00; BS, 100%). Strongly supported successive sister
groups were Alberteae (PP, 1.00; BS, 85%), an
Augusta–Wendlandia clade (PP, 1.00; BS, 100%) and
an Airosperma–Boholia clade (PP, 1.00; BS 100%).
In the Vanguerieae alliance, Aleisanthieae formed a
sister group to Ixoreae (PP, 1.00; BS, 100%) and this
clade was, in turn, sister to Greeneeae (PP, 1.00; BS,
100%). Relationships between the Aleisanthieae–
Greeneeae–Ixoreae clade, Vanguerieae and Glionnetia were unresolved. Although strongly supported by
the BI analyses (PP, 1.00), the support for this trichotomy was low in the MP analysis (< 50%). Trailliaedoxa was resolved as sister to the clade formed by
this trichotomy. However, this clade also had low
support (PP, 0.83; BS, 54%). Successive sister groups
were Scyphiphora (PP, 1.00; BS, 87%), Jackiopsis (PP,
1.00; BS, 97%) and Crossopteryx (PP, 1.00; BS, 91%).
A grade of successive sister clades to core Ixoroideae
comprised, in turn, Retiniphylleae (PP, 1.00; BS,
100%), Steenisia (PP, 1.00; BS, 100%) and a clade
comprising the sister tribes Mussaendeae and Sabiceeae (PP, 0.98; BS, 54%). The Mussaendeae–
Sabiceeae clade was well supported (PP, 1.00; BS,
96%). A Condamineeae–Henriquezieae–Posoquerieae–
Sipaneeae clade was resolved as the earliest diverging
clade in relation to the rest of the subfamily. However,
the support for this clade was low (PP, 0.79; BS, 72%).
Subfamily Ixoroideae received strong support (PP,
1.00; BS, 100%).
DISCUSSION
In this study, we infer the tribal relationships
in Ixoroideae by the phylogenetic reconstruction of
391
six combined plastid regions. The phylogenetic
hypotheses indicate that Ixoroideae can be considered as comprising the Coffeeae alliance, the Vanguerieae alliance and a grade consisting of Retiniphylleae, Steenisia, Mussaendeae with Sabiceeae
and a Condamineeae–Henriquezieae–Posoquerieae–
Sipaneeae clade (Fig. 2). Henriquezieae, Posoquerieae
and Sipaneeae form a clade, as in the study by Rova
et al. (2002). This clade forms a weakly supported
sister group to Condamineeae, and the Condamineeae–Henriquezieae–Posoquerieae–Sipaneeae clade
is, in turn, sister group to the remainder of the
subfamily. This is congruent with the results of Rydin
et al. (2009). However, in the phylogenetic hypotheses
of Kainulainen et al. (2009), Condamineeae appeared
closer to core Ixoroideae. Further research is needed
in order to better understand the relationships of
these early divergent lineages. As in previous studies
(Rova et al., 2002; Bremer & Eriksson, 2009;
Kainulainen et al., 2010), the resolution in Condamineeae was low.
In the phylogenetic tree presented, Mussaendeae is
resolved as sister group to Sabiceeae with strong
support, in agreement with the results of Alejandro,
Razafimandimbison & Liede-Schumann (2005). As, in
their study, Heinsia DC. forms a sister group to the
remaining genera of the tribe, and Mussaenda L.
forms a clade with Pseudomussaenda Wernham.,
Schizomussaenda H.L.Li (Fig. 1B) from South-East
Asia is here further resolved as sister group to a clade
comprising the Malagasy–Mascarene genera Bremeria Razafim. & Alejandro (Fig. 1C) and Landiopsis
Capuron ex Bosser. In Sabiceeae, Virectaria Bremek.
is resolved as sister group to Tamridaea Thulin &
B.Bremer, as in previous studies by Bremer & Thulin
(1998) and Khan et al. (2008). These genera, together
with Hekistocarpa, have been suggested as constituting a clade recognized at tribal level (Virectarieae s.l.,
based on molecular data) by Dessein et al. (2001), and
the three genera also formed a well-supported clade
in the study by Bremer & Eriksson (2009). These
relationships are not supported in our study, in which
Hekistocarpa instead forms a poorly supported sister
group to Sabicea Aubl. However, previously, Hekistocarpa has also been resolved as sister group to the
remaining Sabiceeae (Khan et al., 2008; based on
nrDNA data). Phylogenetic relationships in this tribe
should be investigated further. The position of Retiniphyllum indicated in this study conforms with that
first found in the study by Rova et al. (2002).
Cortés-B., Delprete & Motley (2009) have subsequently demonstrated the monophyly of the monogeneric Retiniphylleae.
The South-East Asian genus Steenisia (Fig. 1E) was
segregated from Neurocalyx Hook. (subfamily Rubioideae) by Bakhuizen van den Brink (1952). In a
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0.61/-
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Vanguerieae-alliance
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Condamineeae
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1.00/100
Sabiceeae
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Mussaendeae
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Retiniphylleae
Trailliaedoxeae
0.80/54
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Augusteae
Bertiereae
Coffeeae
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Pavetteae
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Octotropideae
Gardenieae
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Vanguerieae
Airospermeae
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Sipaneeae
Aleisanthieae
Ixoreae
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Henriquezieae
Posoquerieae
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AUGUSTEAE
AIROSPERMEAE
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core Ixoroideae
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TRAILLIAEDOXEAE
SCYPHIPHOREAE
STEENISIEAE
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0.98/54
0.54/72
Gelsemium sempervirens
Logania vaginalis
Luculia gratissima
Colletoecema dewevrei
Ophiorrhiza mungos
Cinchona pubescens
Rondeletia odorata
Guettarda speciosa
Cubanola domingensis
Cephalanthus occidentalis
Nauclea orientalis
Henriquezia nitida - HEN
Molopanthera paniculata - POS
Posoqueria latifolia - POS
Posoqueria longiflora - POS
Chalepophyllum guyanense - SIP
Dendrosipanea spigelioides - SIP
Neobertiera gracilis - SIP
Sipanea aff. biflora - SIP
Sipanea hispida - SIP
Pinckneya bracteata - CON
Mastixiodendron flavidum - CON
Emmenopterys henryi - CON
Dioicodendron dioicum - CON
Condaminea corymbosa - CON
Pogonopus speciousus - CON
Ferdinandusa speciosa - CON
Simira cordifolia - CON
Hippotis triflora - CON
Rustia thibaudioides - CON
Calycophyllum candidissimum - CON
Chimarrhis hookeri - CON
Bathysa stipulata - CON
Virectaria multiflora - SAB
Tamridaea capsulifera - SAB
Hekistocarpa minutiflora - SAB
Sabicea diversifolia - SAB
Sabicea aspera - SAB
Sabicea africana - SAB
Heinsia crinita - MUS
Pseudomussaenda flava - MUS
Mussaenda erythrophylla - MUS
Mussaenda arcuata - MUS
Schizomussaenda henryi - MUS
Bremeria landia - MUS
Landiopsis capuronii - MUS
Steenisia pleurocarpa
Retiniphyllum pilosum - RET
Crossopteryx febrifuga - CRO
Jackiopsis ornata - JAC
Scyphiphora hydrophylacea
Trailliaedoxa gracilis
Glionnetia sericea
Greenea oblonga - GRE
Aleisanthia rupestris - ALE
Aleisanthiopsis distantiflora - ALE
Ixora novoguineensis - IXO
Ixora margaretae - IXO
Ixora coccinea - IXO
Ixora ferrea - IXO
Ixora borboniae - IXO
Ixora trilocularis - IXO
Canthium coromandelicum - VAN
Rytigynia senegalensis - VAN
Fadogia tetraquerta - VAN
Vangueria madagascariensis - VAN
Multidentia concrescens - VAN
Psydrax obovata - VAN
Afrocanthium lactescens - VAN
Keetia gueinzii - VAN
Cyclophyllum deplanchei - VAN
Peponidium horridum - VAN
Pyrostria hystrix - VAN
Boholia nematostylis
Airosperma sp.
Airosperma psychotrioides
Airosperma trichotomum
Airosperma vanuense
Augusta austrocaledonica
Augusta longifolia
Augusta rivalis
Wendlandia ligustroides
Wendlandia formosana
Wendlandia tinctoria
Wendlandia arabica
Wendlandia paniculata
Alberta magna - ALB
Bertiera guianensis - BER
Bertiera longithyrsa - BER
Bertiera aethiopica - BER
Empogona coriacea - COF
Coffea ebracteolata - COF
Coffea sessiliflora - COF
Coffea arabica - COF
Burchellia bubalina - GAR
Cremaspora triflora - OCT
Paragenipa lancifolia - OCT
Hypobathrum racemosum - OCT
Fernelia buxifolia - OCT
Feretia apodanthera - OCT
Oxyanthus speciosus - GAR
Mitriostigma axillaris - GAR
Pavetta abyssinica - PAV
Pavetta indica - PAV
Tennantia sennii - PAV
Coptosperma supra-axillare - PAV
Genipa americana - GAR
Gardenia hansemanni - GAR
Coddia rudis - GAR
Kailarsenia tentaculata - GAR
Rothmannia capensis - GAR
Aulacocalyx jasminiflora - GAR
Atractocarpus balansaeanus - GAR
Duperrea pavettifolia - GAR
Catunaregam spinosa - GAR
Aoranthe penduliflora - GAR
Hyperacanthus grevei - GAR
Euclinia longiflora - GAR
Randia aculeata - GAR
Tocoyena pittieri - GAR
Rosenbergiodendron densiflorum - GAR
Figure 2. The majority-rule consensus tree from the Bayesian inference analysis of the combined plastid data (ndhF,
matK, rbcL, rps16 intron, trnS-G and trnT-F). Posterior probabilities and bootstrap support values from the parsimony
analysis are indicated below the clades (a dash indicates bootstrap support of <50%). Phylogram of the tree with the
highest marginal likelihood in inset. New tribal names presented in this article are highlighted. ALB, Alberteae; ALE,
Aleisanthieae; BER, Bertiereae; COF, Coffeeae; CON, Condamineeae; CRO, Crossopterygeae; GAR, Gardenieae; GRE,
Greeneeae; HEN, Henriquezieae; IXO, Ixoreae; JAC, Jackieae; MUS, Mussaendeae; OCT, Octotropideae; PAV, Pavetteae;
POS, Posoquerieae; RET, Retiniphylleae; SAB, Sabiceeae; SIP, Sipaneeae; VAN, Vanguerieae.
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 387–406
PHYLOGENY OF IXOROIDEAE
revision of the genus, Bremer (1984) proposed that it
should be transferred from Argostemmateae to Rondeletieae (subfamily Cinchonoideae). However, in the
molecular phylogenetic study of Bremer & Eriksson
(2009), Steenisia was found nested in Ixoroideae. Steenisia can be readily characterized by a suffrutescent
unicaulous habit, rotate corolla and anthers with
apical appendages fused to form a hollow cone around
the style (in a manner reminiscent of the flowers of
Solanum L.), characters which are all unusual (the
latter unique) in Ixoroideae. A region of the style
covered with hairs that probably catch released pollen
is usually found level with the pollen sacs (Bremer,
1984; Puff et al., 1995). However, as this region does
not appear to extend above the surrounding staminal
tube, pollen is not presented in a secondary manner.
Instead, the mode of pollination is most likely by buzz
pollination (Puff et al., 1995). Steenisia is not associated with any previously described tribe in our analyses and, consequently, the recognition of the Steenisia
clade at the tribal level is proposed in the Taxonomic
synopsis section.
THE VANGUERIEAE
ALLIANCE
The Vanguerieae alliance comprises Aleisanthieae,
Crossopterygeae, Glionnetia, Greeneeae, Ixoreae,
Jackieae, Scyphiphora, Trailliaedoxa and Vanguerieae. The clades resolved in Vanguerieae in this
study are congruent with the results of Lantz &
Bremer (2004). However, the position of Psydrax
Gaertn. is here further resolved in a clade consisting
of Afrocanthium (Bridson) Lantz & B.Bremer, Keetia
E.Phillips and a clade comprising Cyclophyllum
Hook.f., Peponidium (Baill.) Arènes and Pyrostria
Comm. ex Juss., representing the ‘dioecious group’ of
Razafimandimbison et al. (2009). In agreement with
the results of Rova et al. (2002) and Mouly et al.
(2009a), Ixoreae forms a sister group to Aleisanthieae,
and these are, in turn, sister to Greeneeae. Aleisanthia and Greenea both have traditionally been considered part of Rondeletieae (Hooker, 1873), a tribe
characterized by contorted or imbricate corolla aestivation and capsular fruits. Molecular phylogenetic
studies have indicated that this is an unnatural
group, and Rondeletieae has since been much reduced
(see Rova et al., 2002; Manns & Bremer, 2010; Rova,
Delprete & Bremer, 2009).
Glionnetia (Fig. 1G), an endemic of the Seychelles,
has also been suggested as part of Rondeletieae by its
author (Tirvengadum, 1984). However, in a recent
study by Razafimandimbison et al. (2011), Glionnetia
was found nested in the Vanguerieae alliance,
although with an unresolved position relative to Vanguerieae and the Aleisanthieae–Greeneeae–Ixoreae
clade (Rondeletieae s.s. can consequently be consid-
393
ered as restricted to the New World; cf. Manns &
Bremer, 2010). Despite the inclusion of more sequence
data in this study, the phylogenetic position of Glionnetia is still unresolved.
As in the study by Razafimandimbison et al. (2011),
successive sister groups to the Aleisanthieae–
Glionnetia–Greeneeae–Ixoreae clade are Trailliaedoxa, Scyphiphora, Jackieae and Crossopterygeae.
The little-studied Trailliaedoxa has hitherto remained without taxonomic placement in Rubiaceae. It
occurs in the highlands of southern China, although it
has rarely been collected. Trailliaedoxa is an erect
shrublet with minute schizocarpic fruits with solitary
pendulous ovules. The corolla aestivation is leftcontort. Whether or not secondary pollen presentation
occurs is not known. Our results support the recognition of a monogeneric tribe, Trailliaedoxeae (see
Taxonomic synopsis section).
The mangrove plant Scyphiphora (Fig. 1F) occurs
in coastal areas of tropical Asia and the western
Pacific (Puff & Rohrhofer, 1993). Scyphiphora has a
complex taxonomic history (see Puff & Rohrhofer,
1993; Mouly et al., 2009a), as the highly modified
fruits, in particular, which are adapted for sea dispersal, have caused difficulties in assessing its systematic placement. The fruits are indehiscent and
corky, with one ascending and one descending ovule
per locule (Puff & Rohrhofer, 1993). However, the
flowers have secondary pollen presentation and leftcontort corolla aestivation, characteristics shared by
most of the core Ixoroideae. Andreasen & Bremer
(2000) tentatively included the genus in Ixoreae.
However, in the studies by Bremer et al. (1999),
Bremer & Eriksson (2009) and Cortés-B. et al. (2009),
Scyphiphora was resolved as sister to the Ixoreae–
Vanguerieae clade, a position congruent with this
study, in which Scyphiphora is resolved as sister to
the
Aleisanthieae–Glionnetia–Greeneeae–Ixoreae–
Trailliaedoxa–Vanguerieae clade. Consequently, we
propose the recognition of tribe Scyphiphoreae (see
Taxonomic synopsis section).
THE COFFEEAE
ALLIANCE
The Coffeeae alliance comprises Airosperma, Augusta,
Boholia, Wendlandia and tribes Alberteae, Coffeeae,
Gardenieae, Octotropideae and Pavetteae. As in previous molecular studies (Andreasen & Bremer, 1996;
Bremer & Eriksson, 2009), Gardenieae is not monophyletic. Mitriostigma (Fig. 1M) and Oxyanthus form
a poorly supported sister group to Pavetteae, and
Burchellia forms a sister group to Octotropideae.
Further research is needed to better understand
the phylogenetic relationships in the Gardenieae–
Octotropideae–Pavetteae complex. Successive sister
groups to this complex are the Bertiereae–Coffeeae
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 387–406
394
K. KAINULAINEN ET AL.
clade, Alberteae, the Augusta–Wendlandia clade and
the Airosperma–Boholia clade. The included representatives of Bertiera form a monophyletic group
sister to Coffeeae, a relationship also inferred in other
studies (e.g. Bremer et al., 1995; Persson, 2000; Davis
et al., 2007; see the latter for a discussion on the
delimitation and morphological differentiation of
these tribes, which some authors have treated as one,
i.e. Andreasen & Bremer, 2000; Robbrecht & Manen,
2006).
Augusta and Wendlandia have traditionally
(Hooker, 1873) been considered as part of Rondeletieae. However, in the molecular phylogenetic study of
Rova et al. (2002), they were resolved as a clade in
Ixoroideae. Both genera have widely disjunct distributions. In Augusta, A. longifolia occurs in northeastern and central Brazil (Delprete, 1997), A. rivalis
(Fig. 1I) in Central America, A. austrocaledonica in
New Caledonia and A. vitiensis (Seem.) J.H.Kirkbr. in
Fiji. The last three species have previously been recognized as Lindenia, a name that was reduced to
synonymy by Kirkbride (1997). This is supported by
our results, because A. rivalis and A. austrocaledonica are paraphyletic with respect to A. longifolia
(Fig. 2). Wendlandia (Fig. 1J) has a wide distribution
in East Asia and Australasia (centre of diversity in
China), with one species, W. ligustroides, in southeastern Turkey–northern Iraq and one species,
W. arabica, in Ethiopia, Somalia and Yemen (see Puff,
1990). Cowan (1932), who provided the last comprehensive revision of the genus, considered the last two
species as exceptional, and their inclusion in Wendlandia as doubtful. However, Wendlandia appears to
be monophyletic in our phylogenetic analyses, in
which W. ligustroides forms a sister group to the
remaining included species, whereas W. arabica is
nested in the East Asian clade. Secondary pollen
presentation appears to be absent in Wendlandia (D.
Zhang, South China Botanical Garden, Guangzhou,
Guangdong, China, pers. comm.). The status of this
character in Augusta is not known. Both genera have
left-contorted corolla aestivation. In the Coffeeae alliance, the Augusta–Wendlandia clade is distinguished
by capsular fruits. This clade is not associated with
any previously described tribe; consequently, we
propose that it should be recognized at tribal level
(see Taxonomic synopsis section).
Airosperma and Boholia were placed in Alberteae
by their respective authors (Schumann & Lauterbach,
1900; Merrill, 1926) based on the presence of solitary
pendulous ovules and contorted corolla aestivation.
Boholia occurs in the Philippines, but has also been
collected on the island of Flores in Indonesia
(Schmutz 2691; P; image seen). Airosperma has a
disjunct distribution, occurring in New Guinea and
the Fiji islands (in the phylogenetic hypothesis, the
included species from the respective areas form sister
groups). One of the Fijian species, A. trichotomum,
was originally described by Gillespie (1932) as
Abramsia trichotoma. Smith (1945: 108) considered
the generic concepts as ‘essentially identical’ and subsumed Abramsia. This synonymization is supported
by the molecular data, because A. trichotomum is
nested in Airosperma, forming a sister group to
A. vanuense S.P.Darwin (Fig. 2). Secondary pollen
presentation is not present in Airosperma (Darwin,
1979) and at least some of the New Guinean species
of the genus appear to be functionally dioecious
(Darwin, 1980). The status of this character in
Boholia is not known. Although having been
described as right-contorted or imbricate, the corolla
aestivation is left-contorted in both genera (K. Kainulainen, pers. observ.). The fruits are fleshy and
contain pyrenes, and were interpreted by Robbrecht
(1988) as adapted for dispersal by sea currents.
However, animal dispersal also seems a possibility
considering the vivid colour of the fruits (blue–purple,
white or yellow; Darwin, 1980). In this study, as in
that of Kainulainen et al. (2009), they form a clade
separate from Alberteae; consequently, we propose
that this clade should be recognized at the tribal level
(see Taxonomic synopsis section).
TAXONOMIC SYNOPSIS
Following the results of the molecular phylogenetic
analyses, we present here a revised tribal classification of Ixoroideae, although we do not address the
tribal delimitation in the problematic Gardenieae
complex, i.e. Gardenieae, Octotropideae (including
Cremasporeae) and Pavetteae, which will be discussed further by A. Mouly et al. (Université de
Franche-Comté, Besançon; unpubl. data). Including
these three tribes, Ixoroideae comprises 24 tribes, five
of which are newly and formally described below.
Although the molecular support for Ixoroideae is
strong, morphologically the members are diverse and
not easily characterized; no potential morphological
synapomorphies for the subfamily are known at this
point. In particular, Condamineeae and Henriquezieae contain morphologically aberrant genera
(Rogers, 1984; Kainulainen et al., 2010), some of
which, at times, have been classified outside
Rubiaceae [e.g. Dialypetalanthus Kuhlm. in Dialypetalanthaceae (Rizzini & Occhioni, 1949) and Henriquezia Spruce ex Benth. and Platycarpum Humb. &
Bonpl. in Henriqueziaceae (Bremekamp, 1957)].
SUBFAMILY IXOROIDEAE RAF.
Trees, shrubs, monocaulous treelets, subshrubs or
rarely herbs. Raphides absent. Stipules entire, bifid
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PHYLOGENY OF IXOROIDEAE
or rarely fimbricate; interpetiolar or rarely intrapetiolar. Flowers usually actinomorphic, protandrous,
often with secondary pollen presentation; rarely zygomorphic, heterostylous, dioecious, monoecious or protogynous. Calyces mostly persistent, in several taxa
with one or several lobes expanded and showy.
Corolla aestivation contorted to left, rarely to right,
imbricate, valvate or rarely open. Fruits fleshy and
indehiscent, dry and indehiscent or capsular, with
numerous, few or solitary ovules per locule.
Tribe Airospermeae Kainul. & B.Bremer, trib. nov.
Type: Airosperma K.Schum. & Lauterb., Fl.
Schutzgeb. Südsee: 565 (1900)
Suffrutices, frutices vel arbusculae unicaules. Flores
5-meri in paniculis terminalibus. Calyx persistens.
Corolla brevi- vel longi-tubularis, lobis in aestivatione
sinistrorsum contortis. Ovarium biloculare, ovulo uno
pendulo in quoque loculo. Stylus inclusus vel (longi-)
exsertus. Fructus carnosi, pyrenis duabus, in maturitate azureopurpurei, albidi vel lutescentes.
Unicaulous subshrubs, shrubs or small trees.
Flowers 5-merous in terminal panicles. Calyx persistent. Corolla short- to long-tubular, with left-contorted
aestivation. Ovary bilocular, with one pendulous
ovule in each locule. Style included to (long-)exserted.
Fruits fleshy, with two pyrenes, becoming blue–
purple, whitish or yellowish in maturity.
Included genera: Airosperma with six species in Fiji
and New Guinea, and the monotypic Boholia from the
Philippines and the island of Flores, Indonesia.
Tribe Alberteae Hook.f.
For descriptions, see Puff et al. (1984), Robbrecht
(1988) and Kainulainen et al. (2009).
Distribution: South-east Africa and Madagascar.
395
Inclusion based on Alejandro et al. (2010): Greeniopsis, occurring in South-East Asia.
Tribe Augusteae Kainul. & B.Bremer, trib. nov.
Type: Augusta Pohl, Pl. Bras. Icon. Descr. 2: 1
(1828)
Frutices vel arbusculae. Inflorescentiae cymae terminales compositae aut raro corymbi. Flores 5-meri.
Calyx persistens. Corolla tubulari-infundibuliformis,
lobis in aestivatione sinistrorsum contortis. Ovarium
biloculare, ovulis numerosis horizontaliter insertis.
Stylus exsertus. Fructus capsulares, dehiscentia septicida (Augusta) aut loculicida (Wendlandia). Semina
minuta, complanata, testa reticulata.
Shrubs to small trees. Inflorescences terminal compound cymes or rarely corymbs. Flowers 5-merous.
Calyx persistent. Corolla tubular-funnel-shaped, with
left-contorted
aestivation.
Ovary
bilocular,
with numerous ovules horizontally inserted. Style
exserted. Fruits capsular, with septicidal (Augusta) or
loculicidal (Wendlandia) dehiscence. Seeds minute,
compressed, with reticulate testa.
Included genera: Augusta, with four species occurring
in Mexico, north-eastern and central Brazil, the Fiji
islands and New Caledonia, and Wendlandia (c. 80
spp.), occurring in north-eastern Africa, west Asia,
South-East Asia and northern Australia.
Tribe Bertiereae Bridson
For a description, see Bridson & Verdcourt (2003).
Bertiereae as currently defined is monogeneric.
Distribution: Tropical South America to southern
Mexico, tropical Africa, Madagascar and Mascarenes.
Included genus: Bertiera.
Included genera (here investigated): Alberta.
Included based on Kainulainen et al. (2009): Nematostylis Hook.f and Razafimandimbisonia Kainul. &
B.Bremer.
Tribe Coffeeae DC.
For a description, see Davis et al. (2007). Recent taxonomic changes have been made by Tosh et al. (2009;
resurrection of Empogona Hook.f.) and Davis et al.
(2011; inclusion of Psilanthus Hook.f. in Coffea).
Tribe Aleisanthieae Mouly, J.Florence & B.Bremer
For descriptions, see Mouly et al. (2009a) and
Alejandro et al. (2010).
Distribution: Tropical Africa, Madagascar, Comores,
Mascarenes, Seychelles and tropical Asia to Australia.
Distribution: South-East Asia.
Included genera (here investigated): Aleisanthia and
Aleisanthiopsis.
Included genera (here investigated): Coffea and
Empogona.
Inclusion based on Davis et al. (2007): Argocoffeopsis Lebrun, Belonophora Hook.f., Calycosiphonia
Pierre ex Robbr., Diplospora DC., Discospermum
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K. KAINULAINEN ET AL.
Dalzell, Nostolachma T.Durand, Sericanthe Robbr.,
Tricalysia A.Rich. ex DC. and Xantonnea Pierre ex
Pit.
Tribe Condamineeae Hook.f.
For a description, see Kainulainen et al. (2010).
Distribution: Neotropics, south-eastern USA (Pinckneya Michx.), South-East Asia (Emmenopterys Oliv.)
and the Malesia-Pacific region (Dolicholobium
A.Gray, Mastixiodendron Melch. and Mussaendopsis
Baill.).
Included genera (here investigated): Bathysa C.Presl,
Calycophyllum DC., Chimarrhis Jacq., Condaminea
DC., Dioicodendron Steyerm., Emmenopterys, Ferdinandusa Pohl, Hippotis Ruiz & Pav., Mastixiodendron, Pinckneya, Pogonopus Klotzsch, Rustia
Klotzsch and Simira Aubl.
Inclusion based on Kainulainen et al. (2010): Alseis
Schott, Bothriospora Hook.f., Capirona Spruce, Dialypetalanthus, Dolichodelphys K.Schum. & K.Krause,
Dolicholobium, Elaeagia Wedd., Holtonia Standl.,
Macbrideina Standl., Macrocnemum P.Browne,
Mussaendopsis, Parachimarrhis Ducke, Pentagonia
Benth., Picardaea Urb., Schizocalyx Wedd., Semaphyllanthe L.Andersson, Sommera Schltdl., Tammsia
H.Karst., Warszewiczia Klotzsch and Wittmackanthus
Kuntze.
Tribe Crossopterygeae F.White ex Bridson
For a description, see Bridson & Verdcourt (2003).
Crossopterygeae as currently defined is monogeneric.
Inclusion based on Rogers (1984) and Delprete &
Cortés-B. (2004): Gleasonia Standl. and Platycarpum.
Tribe Ixoreae A.Gray.
For descriptions, see Mouly et al. (2009a, b). Ixoreae
as currently defined is monogeneric.
Distribution: Neotropics, tropical Africa, Madagascar,
Comores, Mascarenes, Seychelles, tropical Asia to the
Pacific.
Included genus: Ixora.
Tribe Jackieae Korthals
For descriptions, see Ridsdale (1979) and
Razafimandimbison et al. (2011). Jackieae as currently defined is monogeneric.
Distribution: South-East Asia.
Included genus: Jackiopsis.
Tribe Mussaendeae Hook.f.
For descriptions, see Alejandro et al. (2005).
Distribution: Tropical Africa, Madagascar,
carenes, South-East Asia to the Pacific.
Mas-
Included genera (here investigated): Bremeria,
Heinsia, Landiopsis, Mussaenda, Pseudomussaenda
and Schizomussaenda.
Inclusion based on Tange (1994): Neomussaenda
Tange.
Distribution: Tropical Africa.
Tribe Posoquerieae Delprete
For a description, see Delprete (2009).
Included genus: Crossopteryx.
Distribution: Neotropics.
Tribe Greeneeae Mouly, J.Florence & B.Bremer
For a description, see Mouly et al. (2009a).
Included genera: Molopanthera Turcz. and Posoqueria
Aubl.
Distribution: South-East Asia.
Tribe Retiniphylleae Hook.f.
For a description, see Robbrecht (1988). Retiniphylleae as currently defined is monogeneric.
Included genera (here investigated): Greenea.
Inclusion based on Mouly et al. (2009a): Spathichlamys R.Parker.
Tribe Henriquezieae Hook.f.
For a description, see Rogers (1984).
Distribution: Tropical South America.
Included genus: Retiniphyllum.
Tribe Sabiceeae Bremek.
For a description, see Khan et al. (2008).
Distribution: Tropical South America.
Included genera (here investigated): Henriquezia.
Distribution: Neotropics, Tropical Africa, Madagascar,
São Tomé, Socotra, and Sri Lanka.
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PHYLOGENY OF IXOROIDEAE
Included genera: Hekistocarpa, Sabicea, Tamridaea
and Virectaria.
Tribe Scyphiphoreae Kainul. & B.Bremer, trib. nov.
Type: Scyphiphora C.F.Gaertn., Suppl. Carp.: 91
(1806)
Frutices vel arbusculae. Flores 4(–5)-meri, in thyrsis
axillaribus. Calyx tubularis, brevis, persistens, lobis
indistinctis. Corolla tubularis, lobis in aestivatione
sinistrorsum contortis. Ovarium biloculare, ovulo uno
ascendenti et uno descendenti in quoque loculo. Stylus
exsertus. Fructus sicci, indehiscentes, porcati, mesocarpio extenso.
Shrubs or small trees. Flowers 4(–5)-merous,
in axillary thyrses. Calyx tubular, short, persistent,
with indistinct lobes. Corolla tubular, with leftcontorted aestivation. Ovary bilocular, with one
ascending and one descending ovule in each locule.
Style exserted. Fruits dry, indehiscent, ridged, with
extensive mesocarp.
Included genus: The monotypic Scyphiphora, occurring in tropical Asia and the western Pacific.
Tribe Sipaneeae Bremek.
For a description, see Delprete & Cortés-B. (2004).
Distribution: Central America and tropical South
America.
Included genera (here investigated): Chalepophyllum
Hook.f., Dendrosipanea Ducke, Neobertiera Wernham
and Sipanea Aubl.
Inclusion based on Delprete & Cortés-B. (2004):
Limnosipanea Hook.f., Maguireothamnus Steyerm.,
Neblinathamnus Steyerm., Pteridocalyx Wernham,
Sipaneopsis Steyerm. and Steyermarkia Standl.
Tribe Steenisieae Kainul. & B.Bremer, trib. nov.
Type: Steenisia Bakh.f., Webbia 8: 381 (1952)
Suffrutices unicaules. Flores 4–5-meri, in thyrsis axillaribus. Calyx persistens, interdum uno lobo post
anthesin expanso. Corolla rotata, lobis in aestivatione
sinistrorsum contortis. Ovarium biloculare, ovulis
numerosis horizontaliter insertis. Stylus curvatus.
Antherae appendicibus apicalibus prolongatis, connatis tubumque stamineum stylum cingentem facientibus. Fructus capsulares septicidales. Semina minuta,
complanata, testa reticulata granulata.
Unicaulous subshrubs. Flowers 4–5-merous, in axillary thyrses. Calyx persistent, sometimes with one
lobe expanding after anthesis. Corolla rotate, with
left-contorted aestivation. Ovary bilocular, with
numerous ovules horizontally inserted. Style curved.
Anthers with extended apical appendages, united and
397
forming a tube surrounding the style. Fruits septicidal capsules. Seeds minute, flattened, with a reticulate, granulate testa.
Included genus: Steenisia, with five species in
Sundaland (Borneo, Natuna Islands and Peninsular
Malaysia).
Tribe Trailliaedoxeae Kainul. & B.Bremer, trib. nov.
Type: Trailliaedoxa W.W.Sm. & Forrest, Notes Roy.
Bot. Gard. Edinburgh 10: 74 (1917)
Fruticuli erecti. Flores minuti, 5-meri, in cymis terminalibus. Calyx persistens. Corolla infundibuliformis, lobis in aestivatione sinistrorsum contortis.
Ovarium biloculare, ovulo uno pendulo in quoque
loculo. Stylus exsertus. Fructus schizocarpi.
Erect shrublets. Flowers minute, 5-merous, in terminal cymes. Calyx persistent. Corolla funnel-shaped,
with left-contorted aestivation. Ovary bilocular, with
one pendulous ovule in each locule. Style exserted.
Fruits schizocarpous.
Included genus: The monotypic Trailliaedoxa, occurring in south-western China (Sichuan, Yunnan).
Tribe Vanguerieae A.Rich. ex Dum.
For descriptions, see Robbrecht (1988) and Lantz &
Bremer (2004).
Distribution: Southern Africa, tropical Africa, Madagascar, Comores, Mascarenes, Seychelles, (sub-) tropical Asia to Australia and the Pacific.
Included genera (here investigated): Afrocanthium,
Canthium Lam., Cyclophyllum, Fadogia Schweinf.,
Keetia, Multidentia Gilli, Peponidium, Psydrax, Pyrostria, Rytigynia Blume and Vangueria Juss.
Inclusion based on Robbrecht (1988), Lantz &
Bremer (2004) and Razafimandimbison et al. (2009):
Bullockia (Bridson) Razafim., Lantz & B.Bremer,
Cuviera DC., Eriosemopsis Robyns, Everistia S.T.Reynolds & R.J.F.Hend., Fadogiella Robyns, Hutchinsonia
Robyns, Perakanthus Robyns ex Ridl., Plectroniella
Robyns, Pygmaeothamnus Robyns, Robynsia Hutch.,
Temnocalyx Robyns ex Ridl., Vangueriella Verdc. and
Vangueriopsis Robyns.
CONCLUSIONS
Here, we analysed the tribal relationships and delimitation in Ixoroideae using six plastid DNA regions and
Bayesian and parsimony methods of phylogenetic
reconstruction. Following the results of this study,
Ixoroideae can be considered as being composed of two
well-supported lineages, the Coffeeae alliance and the
Vanguerieae alliance, and a grade consisting of the
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 387–406
398
K. KAINULAINEN ET AL.
tribes Condamineeae, Henriquezieae, Mussaendeae,
Posoquerieae, Retiniphylleae, Sabiceeae, Sipaneeae
and Steenisieae. The Vanguerieae alliance comprises
Glionnetia (with unplaced tribal position) and the
tribes Aleisanthieae, Crossopterygeae, Greeneeae,
Ixoreae, Jackieae, Scyphiphoreae, Trailliaedoxeae and
Vanguerieae. The Coffeeae alliance contains Airospermeae, Alberteae, Augusteae, Bertiereae, Coffeeae,
Gardenieae, Octotropideae and Pavetteae. Molecular
data furthermore support the transfer of Abramsia
to Airosperma and Lindenia to Augusta. Future
studies should further investigate the phylogenetic
positions of Glionnetia and Hekistocarpa and the relationships of the early divergent Condamineeae and
Henriquezieae–Posoquerieae–Sipaneeae clades with
respect to the rest of the subfamily.
ACKNOWLEDGEMENTS
We thank the curators of the herbaria AAU, BR, GB,
HUH, L, MO, S and UPS for providing loans and/or
access to collections. We also thank Anbar Khodabandeh for laboratory assistance, Claes Persson for DNA
samples, Christian Puff and the Missouri Botanical
Garden for photographs and Dianxiang Zhang for
sharing unpublished information on Wendlandia. Per
Ola Karis and Philip Oswald checked the Latin diagnoses. Piero Delprete and two anonymous reviewers
provided helpful comments on the manuscript. The
Knut and Alice Wallenberg Foundation and the
Swedish Research Council provided financial support
to BB.
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APPENDIX
Overview of taxon sampling, including GenBank sequence accession numbers and voucher specimens for previously
unpublished sequences (indicated with *). Italic sequences originate from a different specimen from that indicated
Species
Voucher
matK
ndhF
rbcL
rps16
trnS-G
trnT-L-F
Afrocanthium
lactescens (Hiern)
Lantz
Airosperma
psychotrioides
K.Schum. &
Lauterb.
Airosperma sp.
Airosperma
trichotomum
(Gillespie)
A.C.Sm.
Airosperma
vanuense
S.P.Darwin
Alberta magna
E.Mey.
Aleisanthia
rupestris (Ridl.)
Ridl.
Aleisanthiopsis
distantiflora
(Merr.) Tange
Aoranthe
penduliflora
(K.Schum.)
Somers
Atractocarpus
balansaeanus
Guillaumin
Augusta
austrocaledonica
(Brongn.)
J.H.Kirkbr.
Augusta longifolia
(Spreng.) Rehder
Augusta rivalis
(Benth.)
J.H.Kirkbr.
Aulacocalyx
jasminiflora
Hook.f.
Bathysa stipulata
(Vell.) C.Presl
Bertiera aethiopica
Hiern
Luke & Luke 9045
(UPS)
HM119502*
HM164346*
HM164152*
HM164189*
HM164234*
AJ6201271
Nyman 569 (UPS)
–
HM164347*
–
–
–
HM164302*
Sands 6819 (L)
Degener &
Ordonez 15542
(S)
HM119503*
–
HM164348*
HM164349*
–
–
–
HM164190*
HM164235*
–
HM164303*
HM164304*
Smith 8214 (P)
HM119504*
AM9498452
–
FM2047002
FM2047402
FM2071082
Tonkin 200 (UPS)
HM119505*
AJ2362823
Y187083
FM2047012
FM2047412
AJ6201181
Tange 45171
(AAU)
HM119506*
–
HM164153*
AF2429024
HM164236*
HM164305*
Tange 46977
(AAU)
HM119507*
HM16435028
HM164154*
AF2429034
HM164237*
HM164306*
Iverssen & Steiner
86776 (UPS)
HM119508*
–
Y118455
HM164191*
HM164238*
HM164307*
Munzinger &
McPherson 635
(MO)
Mouly & Innocente
237 (P)
HM119509*
HM164351*
HM164155*
HM164192*
HM164239*
HM164308*
HM119510*
HM164352*
EU8174126
HM164193*
HM164240*
EU8174546
Kirkbride 5295
(BR)
McDowell 5017
(ETSU)
HM119511*
HM164353*
–
–
HM164241*
HM164309*
HM119512*
AM9498462
AM9498422
HM164194*
FM2047522
FM2071182
Schmidt et al.
1672 (MO)
HM119513*
HM164354*
EU8174136
EF2056397
FM2047532
EU8174556
Pirani & Bremer
4901 (SPF)
Dessein s.n. (BR)
FJ9053378
FJ8719478
HM164156*
FJ8846378
FJ9483028
FJ9483718
HM119514*
HM164355*
HM164157*
HM164195*
HM164242*
HM164310*
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 387–406
402
K. KAINULAINEN ET AL.
APPENDIX Continued
Species
Voucher
matK
ndhF
rbcL
rps16
trnS-G
trnT-L-F
Bertiera guianensis
Aubl.
Bertiera longithyrsa
Baker
Boholia
nematostylis
Merr.
Bremeria landia
(Poir.) Razafim. &
Alejandro
Burchellia
bubalina
(L.f.) Sims
Calycophyllum
candidissimum
(Vahl) DC.
Canthium
coromandelicum
(Burm.f.) Alston
Catunaregam
spinosa (Thunb.)
Tirveng.
Cephalanthus
occidentalis L.
Chalepophyllum
guyanense Hook.f.
Chimarrhis hookeri
K.Schum.
Andersson et al.
2029 (GB)
Kårehed et al. 256
(UPS)
Bicknell 1561A
(SUNIV)
HM119515*
AM9498472
AJ2248459
AF20098310
FM2047542
FM2071192,33
HM119516*
HM164356*
HM164158*
HM164196*
HM164243*
HM164311*
HM119517*
AM9498482
AM11721011
AM11728611
FM2047552
HM164312*
Andriambololonera
37 (MAU)
HM119518*
HM164357*
–
HM164197*
HM164244*
HM164313*
Bremer 3129
(UPS)
HM119519*
HM164358*
Z6883312
HM164198*
HM164245*
HM164314*
Sanders 1805
(FTG)
FJ9053408
AJ2362853
X8362713
FM2047122
FM2047562
AJ84739814
Andreasen 36
(UPS)
HM119520*
HM164359*
Z6885112
HM164199*
HM164246*
AJ84740114
Luke 8332A
(UPS)
HM119522*
–
AM11721411
HM164200*
HM164248*
HM164315*
Forbes s.n. (S)
AY53837715
AJ2362883
X8362913
AF00403316
–
AJ34695517
Sandwith 1346
(S)
Delprete &
Verduga 6421
(UPS)
McDowell 4613
(DUKE)
Bremer 3764
(UPS)
HM119523*
–
HM164159*
HM164201*
HM164249*
HM164316*
FJ9053448
AJ2362893
Y187123
FJ8846438
FJ9483098
FJ9483788
Z7019718
AJ23584319
X8363013
FM2047142
FM2047582
AJ34696317
HM119524*
HM164361*
AJ28669520
HM164202*
HM164250*
HM164317*
EF04421321
HM119560*
EF04421321
HM164387*
EF04421321
AJ28669220
EF04421321
HM164219*
EF04421321
HM164283*
EF04421321
HM164333*
HM119525*
HM164362*
HM164160*
HM164203*
HM164251*
HM164318*
HM119526*
EU14540922
EU14545722
AF12927223
HM164252*
EU14553222
Pennington &
Daza 17436
(MOL)
Bremer 3810
(UPS)
FJ9053478
FJ8719508
HM164161*
FJ8846458
FJ9483128
FJ9483818
HM119527*
HM164363*
AJ28671120
HM164204*
HM164253*
HM164319*
Andreasen 51
(UPS)
HM119528*
AM9498502
Z6885612
FM2047162
FM2047592
FM2071212
Bremer 3097
(UPS)
FJ9053298
AM9498512
AM11722311
FM2047172
FM2047602
FM2071232
McDowell 4427
(DUKE)
AY53838615
AM11734511
X8363213
FM2047182
FM2047612
FM2071242
Cinchona
pubescens Vahl.
Coddia rudis
(E.Mey. ex Harv.)
Verdc.
Coffea arabica L.
Coffea ebracteolata
(Hiern) Brenan
Coffea sessiliflora
Bridson
Colletoecema
dewevrei (De
Wild.)
E.M.A.Petit
Condaminea
corymbosa (Ruiz
& Pav.) DC.
Coptosperma
supra-axillare
(Hemsl.) Degreef
Cremaspora triflora
ssp. confluens
(K.Schum.) Verdc.
Crossopteryx
febrifuga (Afzel.
ex G.Don) Benth.
Cubanola
domingensis
(Britton) Aiello
Andreasen 223
(UPS)
Luke 9024
(UPS)
Lisowski 47195
(K)
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 387–406
PHYLOGENY OF IXOROIDEAE
403
APPENDIX Continued
Species
Voucher
matK
ndhF
rbcL
rps16
trnS-G
trnT-L-F
Cyclophyllum
deplanchei
Hook.f.
Dendrosipanea
spigelioides
Ducke
Dioicodendron
dioicum
(K.Schum. &
Krause) Steyerm.
Duperrea
pavettifolia (Kurz)
Pit.
Emmenopterys
henryi Oliv.
Empogona coriacea
(Sond.) Tosh &
Robbr.
Euclinia longiflora
Salisb.
Fadogia tetraquetra
K.Schum. &
Krause
Ferdinandusa
speciosa Pohl
Feretia apodanthera
Delile
Fernelia buxifolia
Lam.
Mouly &
Innocente
228 (P)
Prance et al.
16199 (S)
HM119529*
–
EU8174166
EF2056407
HM164254*
EF2056317
FJ9053248
FJ8719438
HM164162*
FJ8846278
FJ9482918
FJ9483608
Zarucchi &
Echeverry 4780
(MO)
FJ9053498
FJ8719528
HM164163*
FJ8846478
FJ9483148
FJ9483838
cult. Bergius
Botanic Garden
HM119531*
HM164365*
AJ28670920
HM164205*
HM164256*
HM164320*
Robbrecht s.n.
(UPS)
Bremer et al. 4302
(UPS)
FJ9053608
AJ2362943
Y187153
FM2047192
FM2047622
FM2071252
HM119574*
HM164401*
HM164184*
HM164228*
HM164295*
HM164340*
De Block 27 (BR)
HM119532*
HM164366*
Z6883512
HM164206*
HM164257*
AJ84739914
Bremer & Bremer
3799 (UPS)
HM119533*
HM164367*
AM11722511
HM164207*
HM164258*
AJ6201391
Malme 2442 (UPS)
HM119534*
EU14541222
AM11722611
FJ8846578
FJ9483278
EU14553422
Luke 8385 (UPS)
HM119535*
HM164368*
HM164164*
HM164208*
HM164259*
HM164321*
Nat. Bot. Gard.
Meise, no.
19940025-26
Drozd & Molem
1998-11-13
HM119536*
HM164369*
AJ28670420
AF2448924
HM164260*
EU14554022
HM119537*
AM9498522
AJ31844624
AJ32007724
FM2047632
FM2071262
Bremer 3026
(UPS)
AJ42932225
AJ01198426
L1439727
AJ43103325
–
AJ43090825
Kiehn, HBVsub
RR-420 (WU,
UPS)
Beaver 17 (S)
HM119538*
HM164370*
Z6883912
HM164209*
HM164261*
HM164322*
HM569720*
HM53621728
HM53622328 HM53622928 HM569721*
HM53623528
Larsen & Larsen
33451 (P)
Persson 141 (GB)
HM119539*
HM164371
–
EU8174396
HM164262*
EU8174596
AY53838915
FJ8719428
AY53848515
AF2429644
FJ9482898
FJ9483588,34
McPherson 16188A
(MO)
Leuwenberg 6393
(BR, K, WAG)
HM119540*
HM164372*
Y118495
HM164210*
HM164263*
HM164323*
HM119541*
HM164373*
AF33236629
AF33236729
HM164264*
HM164324*
Liesner 8531 (MO)
–
HM164374*
–
HM164211*
–
HM164325*
Ståhl 2660 (GB)
FJ9053658
FJ8719568
HM164165*
FJ8846598
FJ9483298
FJ9483978
HM164375*
HM164166*
HM164212*
HM164265*
HM164326*
Gardenia
hansemannii
K.Schum.
Gelsemium
sempervirens (L.)
J.St.-Hil.
Genipa americana
L.
Glionnetia sericea
(Baker) Tirveng.
Greenea oblonga
Craib
Guettarda speciosa
L.
Heinsia crinita
(Afzel.) G.Taylor
Hekistocarpa
minutiflora
Hook.f.
Henriquezia nitida
var. macrophylla
(Ducke) Steyerm.
Hippotis triflora
Ruiz & Pav.
Hyperacanthus
grevei Rakotonas.
& A.P.Davis
Razafimandimbison HM119542*
547 (UPS)
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 387–406
404
K. KAINULAINEN ET AL.
APPENDIX Continued
Species
Voucher
matK
ndhF
rbcL
rps16
trnS-G
trnT-L-F
Hypobathrum
racemosum
(Roxb.) Kurz
Ixora borboniae
Mouly &
B.Bremer
Ixora coccinea L.
Ridsdale 81
HM119543*
AM9498532
AJ28670520
AM11731811
HM164266*
FM2071272
Friedmann 3049
(P)
HM119552*
HM164383*
HM164173*
FJ1506856
HM164275*
FJ1506096
Bremer 2719
(UPS)
Taylor 11693 (MO)
HM119544*
HM164376*
HM164167*
EF2056417
FM2047642
EU8174646
HM119545*
HM164377*
EU8174226
EF2056427
HM164267*
EU8174656
Mouly & Innocente
222 (P)
HM119521*
HM164360*
EU8174156
EU8174366
HM164247*
EU8174566
Drozd & Molem
1998-11-13
HM119581*
HM164406*
AJ31845924
AJ32009024
HM164300*
EU8174766
Lesouef 31 (TAN)
HM119530*
HM164364*
EU8174176
EU8174376
HM164255*
EU8174576
K. S. Tan s.n.
HM119546*
HM53621328
HM53621928 HM53622528 HM164268*
HM53623128
Larsen 41627
(AAU)
HM119547*
HM164378*
HM164168*
HM164213*
HM164269*
HM164327*
Bremer et al. 4349
(UPS)
Gautier 4533 (MO)
HM119548*
HM164379*
HM164169*
HM164214*
HM164270*
AJ6201431
HM119549*
HM164380*
HM164170*
HM164215*
HM164271*
HM164328*
Bremer 3013
(UPS)
CT 870064
AJ42932425
AJ23583719
Z6882612
AJ43103525
HM164272*
AJ43091025
AJ42932525
AJ01198726
AM11724311
AJ43103625
FM2047652
AJ43091125
FJ9053698
FJ8719598
HM164171*
AF2429794
FJ9483328
FJ9484018
HM119550*
HM164381*
X8365013
HM164216*
HM164273*
HM164329*
–
HM164382*
HM164172*
AF2429814
–
FJ948361*
Bidgood et al. 845
(K)
–
–
–
–
HM164274*
AJ6201501
McPherson 16213
(MO)
Gillis 10838 (FTG)
HM119551*
AJ2363013
Y118545
FM2047212
FM2047672
FM2071282
FJ9053268
AJ1308363
X8365213
FJ8846288
FJ9482928
AJ6201161
Bremer 3001
(UPS)
de Granville 2888
(NY)
Bremer 3301
(UPS)
AY53840715
EU14541022
X8365313
AJ32008024
HM164276*
AJ34695817
–
–
–
AF2429844
–
AF15267930
AY53840815
AJ1308383
X8365613
AF00406416
HM164277*
DQ66215131
Ixora ferrea (Jacq.)
Benth.
Ixora margaretae
(N.Hallé) Mouly
& B.Bremer
Ixora
novoguineensis
Mouly &
B.Bremer
Ixora trilocularis
(Balf.f.) Mouly &
B.Bremer
Jackiopsis ornata
(Wall.) Ridsdale
Kailarsenia
tentaculata
(Hook.f.) Tirveng.
Keetia gueinzii
(Sond.) Bridson
Landiopsis
capuronii
Capuron ex
Bosser
Logania vaginalis
(Labill.) F.Muell.
Luculia gratissima
(Wall.) Sweet
Mastixiodendron
flavidum (Seem.)
A.C.Sm.
Mitriostigma
axillare Hochst.
Molopanthera
paniculata Turcz.
Multidentia
concrescens
(Bullock) Bridson
& Verdc.
Mussaenda arcuata
Poir.
Mussaenda
erythrophylla
Schumach. &
Thonn.
Nauclea orientalis
(L.) L.
Neobertiera gracilis
Wernh.
Ophiorrhiza
mungos L.
Rova &
Gustavsson 2429
(GB)
Bremer 2705
(UPS)
Williams 6861 (S)
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 387–406
PHYLOGENY OF IXOROIDEAE
405
APPENDIX Continued
Species
Voucher
matK
ndhF
rbcL
rps16
trnS-G
trnT-L-F
Oxyanthus speciosus
DC.
Paragenipa
lancifolia (Bojer
ex Baker)
Tirveng. & Robbr
Pavetta abyssinica
Fresen.
Pavetta indica L.
Bremer 4348 (S)
HM119554*
HM164384*
AM11725211
AM11733011
HM164278*
AM11737511
Persson 156 (GB)
HM119555*
HM164385*
AJ28670720
AF00406616
HM164279*
HM164330*35
De Block 6 (BR)
HM119556*
AM9498542
Z6886312
FM2047262
FM2047722
FM2071332
HM119557*
–
–
HM164217*
HM164280*
HM164331*
–
–
–
–
HM164281*
AJ6201531
FJ9053778
AJ1308393
X8366113
FJ8846688
FJ9483398
FJ9484088
FJ9053788
FJ8719648
HM164174*
FJ8846708
FJ9483418
FJ9484108
FJ9053258
AM9498552
Z6885012
FM2047282
FM2047742
FM2071352
HM119558*
HM164386*
HM164175*
HM164218*
HM164282*
HM164332*
HM119559*
AM9498562
Y118555
FM2047292
FM2047752
FM2071362
HM119561*
HM164388*
HM164176*
HM164220*
HM164284*
AJ6201611
HM119562*
HM164389*
AM11726211
AM11733811
HM164285*
AJ6201681
HM119563*
–
HM164390*
HM164392*
Z6883212
AF33165432
HM164221*
AF00407616
HM164286*
FM2047762
HM164334*
FM2071372
–
AJ23584519
Y118575
AF2430104
FJ9482908
FJ9483598,36
HM119566*
HM164393*
HM164177*
HM164222*
HM164287*
HM164335*
HM119567*
HM164394*
AM11726611
AM11734011
HM164288*
AM11738411
FJ9053858
AJ2363103
Y187163
FM2047312
FM2047772
FM2071382
–
–
HM164178*
HM164223*
HM164289*
AJ6201751
–
HM164397*
HM164180*
HM164225*
HM164292*
HM164337*
AY53842015
EU14541622
AY53850815
AF00407916
FJ9482938
FJ9483628,37
HM119568*
EU14541522
EU14545922
EU14549422
HM164290*
AJ84739614
HM119569*
HM164395*
AM11727311
HM164224*
HM164291*
AJ84738314
Andreasen 202
(UPS)
Peponidium
Labat et al. 2236
horridum Arènes
(K)
Pinckneya bracteata Massey s.n. 15F
(Bartram) Raf.
Pogonopus speciosus Meier 2548 (GB)
(Jacq.) K.Schum.
Posoqueria latifolia Andreasen 90
(Rudge) Roem. &
(UPS)
Schult.
Posoqueria
cult. Bergius
longiflora Aubl.
Botanic Garden
Pseudomussaenda
Nissen s.n. (UPS)
flava Verdc.
Psydrax obovata
Bremer & Bremer
(Klotzsch ex Eckl.
3762 (UPS)
& Zeyh.) Bridson
Pyrostria hystrix
Bremer & Bremer
(Bremek.) Bridson
3791 (UPS)
Randia aculeata L. F.G.x.1–145
Retiniphyllum
Wurdack &
pilosum (Spruce
Adderley 43270
ex Benth.) Müll.
(S)
Arg.
Rondeletia odorata Bremer &
Jacq.
Andreasen 3504
(UPS)
Rosenbergiodendron Jansen-Jacobs
densiflorum (K.
3977 (GB)
Schum.) Fagerl.
Rothmannia
Bremer et al. 4346
capensis Thunb.
(S)
Rustia
Delprete 6378
thibaudioides
(UPS)
(H.Karst.)
Delprete
Rytigynia
van den Berghen
senegalensis
8746 (BR)
Blume
Sabicea africana (P. Wieringa 3591
Beauv.) Hepper
(WAG)
Sabicea aspera
Andersson et al.
Aubl.
1941 (GB)
Sabicea diversifolia Bremer et al.
Pers.
4018-B18 (UPS)
Schizomussaenda
Puff 961116-1/1
henryi (Hutch.)
(WU)
X.F.Deng &
D.X.Zhang
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 387–406
406
K. KAINULAINEN ET AL.
APPENDIX Continued
Species
Voucher
matK
ndhF
rbcL
rps16
trnS-G
trnT-L-F
Scyphiphora
hydrophyllacea
C.F.Gaertn.
Simira cordifolia
(Hook.f.) Steyerm.
Sipanea aff. biflora
(L.f.) Cham. &
Schltdl.
Sipanea hispida
Benth. ex
Wernham
Steenisia
pleurocarpa (Airy
Shaw) Bakh.f.
Tamridaea
capsulifera (Balf.
f.) Thulin & B.
Bremer
Tennantia sennii
(Chiov.) Verdc. &
Bridson
Tocoyena pittieri
(Standl.) Standl.
Trailliaedoxa
gracilis W.W.Sm.
& Forrest
Vangueria
madagascariensis
J.F.Gmel.
Wendlandia arabica
Deflers
Wendlandia
formosana Cowan
Wendlandia
ligustroides
(Boiss. & Hohen.)
Blakelock
Wendlandia
paniculata
(Roxb.) DC.
Wendlandia
tinctoria (Roxb.)
DC.
Virectaria
multiflora (Sm.)
Bremek.
Bremer et al. 99
(S)
FJ9053278
AJ2363113
Y187173
EU8174506
FM2047792
EU8174756
Bremer 3361
(UPS)
Rova et al. 2005
(GB)
FJ9053888
FJ8719708
HM164179*
FJ8846778
FJ9483508
FJ9484198
AY53842115
EU14541322
AY53850915
AF00408516
FM2047802
FM2071412,38
Irwin et al. 34756
(UPS)
–
EU14541422
EU14545822
EU14549222
–
HM164336*
Puff BF
990619-1/4
(WU)
Thulin & Gifri
8663 (UPS)
FJ9053288
HM164396*
AM11727911
FM2047352
FM2047812
FM2071422
–
HM164398*
Y118605
FM2047362
FM2047822
FM2071432
Abdalla et al.
96/166 (P)
HM119570*
AM9498582
AM9498432
FM2047372
FM2047832
FM2071442
Rova et al. 2369
(GB)
Boufford et al.
35041 (MO)
HM119571*
AM9498592
HM164181*
FM2047382
FM2047842
FM2071452
HM119573*
HM16440028
HM16418328 HM16422728 HM164294*
HM16433928
Sanders 1798,
#62146 (FTG)
HM119575*
AJ1308403
X8367013
HM164229*
FM2047852
AJ6201841
Thulin et al.
10192 (UPS)
Chung 1403 (S)
HM119576*
HM164402*
HM164185*
HM164230*
HM164296*
HM164341*
HM119577*
HM164403*
HM164186*
HM164231*
HM164297*
HM164342*
Rechinger 183 (S)
HM119578*
HM164404*
HM164187*
AF2430364
HM164298*
HM164343*39
Ridsdale 2179
HM119579*
HM164405*
HM164188*
HM164232*
HM164299*
HM164344*
Parker 3227 (S)
HM119580*
AM9498602
FM2076492
FM2047392
FM2047862
FM2071472
Adames 606 (UPS)
HM119582*
HM164407*
Y118615
HM164233*
HM164301*
HM164345*
Published sequences: 1Lantz & Bremer (2004); 2Kainulainen et al. (2009); 3Bremer et al. (1999); 4J. H. E. Rova (unpubl.
data); 5Bremer & Thulin (1998); 6Mouly et al. (2009a); 7Mouly et al. (2007); 8Kainulainen et al. (2010); 9Andreasen,
Baldwin & Bremer (1999); 10Persson (2000); 11Bremer & Eriksson (2009); 12Andreasen & Bremer (1996); 13Bremer et al.
(1995); 14Alejandro et al. (2005); 15Andersson & Antonelli (2005); 16Andersson & Rova (1999); 17Razafimandimbison &
Bremer (2002); 18Endress et al. (1996); 19Backlund, Oxelman & Bremer (2000); 20Andreasen & Bremer (2000); 21Samson
et al. (2007); 22Rydin et al. (2008); 23Piesschaert et al. (2000); 24Novotny et al. (2002); 25Bremer et al. (2002); 26Oxelman,
Backlund & Bremer (1999); 27Olmstead et al. (1993); 28 Razafimandimbison et al. (2011); 29Dessein et al. (2001); 30Rova
et al. (2002); 31Backlund, Bremer & Thulin (2007); 32L. Andersson (unpubl. data).
Combined sequences: 33with AF152670; 34with AF152725; 35with AF152672; 36with AF152741; 37with AY538475; 38with
AF152675; 39with AF152661.
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 387–406
Birgitta Bremer