Pl. Syst. Evol. (2005)
DOI 10.1007/s00606-005-0313-9
Phylogeny of the complex Vanguerieae (Rubiaceae) genera Fadogia,
Rytigynia, and Vangueria with close relatives and a new
circumscription of Vangueria
H. Lantz1 and B. Bremer2
1
2
Department of Systematic Botany, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden
The Bergius Foundation at the Royal Swedish Academy of Sciences, Stockholm, Sweden
Received August 14, 2004; accepted February 9, 2005
Published online: May 25, 2005
Springer-Verlag 2005
Abstract. The phylogeny of the Vanguerieae genera Fadogia, Rytigynia, Vangueria, and closely
related genera is investigated using nuclear rDNA
ITS sequences and plastid trnT-F and rpl16
sequences. Individual and combined analyses
reveal several strongly supported clades. There
are indications that Fadogia, Rytigynia, Tapiphyllum, and Vangueria are para- or polyphyletic and
only Multidentia is strongly supported as monophyletic. Several taxa are found to have incongruent positions in the ITS and chloroplast
phylogenies, and possible reasons behind these
incongruencies are discussed. For Ancylanthos
rubiginosus a chloroplast capture event can explain
the incongruent position. In the Fadogia-Rytigynia
group the incongruence is more widespread and
cannot be attributed to a single taxon or a few
taxa, but hybridization and introgression is the
most likely explanation for the incongruence. It is
concluded that the genera Ancylanthos, Lagynias,
Pachystigma, and Tapiphyllum and the three
species Fadogia agrestis, Rytigynia fuscosetulosa,
and Rytigynia induta should be transferred to
Vangueria.
Key words: Fadogia, hybridization, phylogeny,
Rubiaceae, Rytigynia, taxonomy, Vangueria,
Vanguerieae.
Introduction
Until recently, the tribe Vanguerieae of the
Rubiaceae remained one of the poorest understood larger groups in the family concerning
the phylogeny of the group. Recent studies
(Lantz et al. 2002, Lantz and Bremer 2004)
have improved our knowledge and now there
is a good general knowledge of the phylogeny.
The monophyly of the tribe has rarely been
doubted (Verdcourt 1958). A very distinct and
easily recognized character, a pollen presenter
at the apex of the style is of great diagnostic
value and makes it easy to distinguish between
members of Vanguerieae and other Rubiaceae
tribes also in the field. Eastern and southern
tropical African taxa have so far received the
most attention (Verdcourt and Bridson 1991,
Bridson 1998). Around 600 species are currently recognized, but the delimitation of many
of these is uncertain, especially for the poorly
known species from Madagascar and South
East Asia.
An earlier study (Lantz and Bremer 2004)
identified one subclade of the tribe in which the
generic limits were especially unclear. Due to
H. Lantz and B. Bremer: Phylogeny of Vangueria and closely related genera
the slightly longer corolla tubes and lobes
present in this group compared to other
members of Vanguerieae, the group was given
the informal name ‘the large-flowered group’.
This group is the focus of the present study.
The large-flowered group is with few exceptions restricted to Africa south of Sahara, but
a few Rytigynia and Vangueria species are
found on Madagascar. Two subgroups of the
large-flowered group had earlier been identified (Lantz et al. 2002), i.e. the Vangueria
group and the Fadogia-Rytigynia group. Included in the Vangueria group is the type genus
of the tribe, Vangueria, together with Ancylanthos (tentatively included), Lagynias, Pachystigma, and Tapiphyllum (Lantz et al. 2002,
Lantz and Bremer 2004). These genera are
considered some of the most problematic in
the tribe, concerning delimitation of species as
well as genera (Bridson 1998). The four genera
Fadogia, Fadogiella, Hutchinsonia, and Rytigynia form the species-rich Fadogia-Rytigynia
group (Lantz et al. 2002) with just above 100
species. Cuviera, Multidentia, Pygmaeothamnus, Robynsia, Vangueriopsis and a single
species of Canthium, C. oligocarpum, also
belong to the large-flowered group, but their
phylogenetic affinities are more uncertain
(Lantz and Bremer 2004). In total, over 180
species are currently recognized in the group,
but a number of these, especially in Rytigynia,
are known from very few collections.
The work of Robyns (1928) has been
especially important for the classification of
the group. With the exclusion of Cuviera and
the large genus Canthium, Robyns revised all
species of Vanguerieae, and made over a
hundred new combinations and descriptions
of species in the large-flowered group. He also
described several new genera, of which Fadogiella, Hutchinsonia, Pygmaeothamnus, Tapiphyllum, and Vangueriopsis are known to
belong to the large-flowered group (Lantz
and Bremer 2004). Later authors (e.g. Verdcourt 1981, 1987; Bridson 1996, 1998) have
added new species to the genera in the group,
and also performed several synonymizations.
Over 180 species representing thirteen genera are currently recognized in the largeflowered group. Most of the genera are hard
to delimit morphologically, good diagnostic
characters are usually lacking. In earlier studies covering the whole tribe (Lantz et al. 2002,
Lantz and Bremer 2004), but with a rather
small sample of the large-flowered group, we
were unable to resolve the relationships in the
group. With this study we aim to resolve the
phylogeny with strong support by greatly
increasing the sample size and adding an extra
data set to the already existing data. The new
data set consists of sequences of the rpl16
intron, one of the fastest evolving chloroplast
regions (Small et al. 1998) and is likely to add
support for the close relationships in this
difficult group. We intend to use the phylogeny
to test the monophyly of the genera as
currently conceived and if necessary base a
new classification on the results. Some incongruence between chloroplast and nuclear phylogenies was noted in an earlier publication
(Lantz and Bremer 2004), and we also aim to
quantify the extent to which the different
genera are affected by this.
Material and methods
Taxon sampling. Our strategy was to include as
many species as possible from all genera known to
belong in the large-flowered clade (Lantz and
Bremer 2004). Sixty-six ingroup (of 180) taxa were
sampled. The availability of material largely determined which species were included. A majority of
the in-group species sampled occur in eastern and
southern Africa, but five species from West Africa,
one from Central Africa, and two from Madagascar are also included (see Fig. 1) . The distributions
of the taxa detailed only to major geographical
regions are given in Fig. 1. This information is
added only to give an indication of the distribution
of the taxa. The taxa are in many cases restricted to
smaller areas within these regions and can also in
some small amount occur outside of the mentioned
areas. Eight representatives of Canthium s. str.,
shown to be the closest relative of the ingroup
(Lantz et al. 2002, Lantz and Bremer 2004), were
chosen as outgroup. Several of these were only
H. Lantz and B. Bremer: Phylogeny of Vangueria and closely related genera
Table 1. Voucher information and EMBL accession numbers. Herbarium abbreviations according to
Holmgren et al. (1990). - indicates sequences not included due to sequencing difficulties. Sequences new for
this study are underlined.
Species
Voucher
EMBL number ITS/trnT-F/
rpl16
Canthium coromandelicum
(Burm. f.) Alston
Canthium glaucum
Hiern ssp. glaucum
Canthium inerme (L.f.) Kuntze
Canthium tetraphyllum
(Schweinf. ex Hiern) Baill.
Canthium armatum
(K. Schum.) Lantz
Pygmaeothamnus cf.
chamaedendrum (Kuntze)
Robyns
Canthium bugoyense
(K. Krause) Lantz
Canthium stenosepalum Lantz
Andreasen 36 (UPS)
AJ315081/AJ620122/AJ876810
Kuchar 17410 (UPS)
AJ617752/AJ620124/AJ876811
Bremer & Bremer 3686 (UPS)
Bremer 3074 (UPS)
AJ315120/AJ620125/AJ876812
AJ315083/AJ620149/AJ876813
Bremer & Bremer 3790 (UPS)
AJ315082/AJ620155/AJ876814
Bremer & Bremer 3800 (UPS)
AJ315119/AJ620165/AJ876815
Rwburindore 3536 (UPS)
AJ315084/AJ620172/AJ876816
Merello et al. 1494 (K)
AJ315085/AJ620182/AJ876817
Ancylanthos rubiginosus Desf.
Canthium oligocarpum
Hiern ssp. captum (Bullock)
Bridson
Cuviera angolensis
Welw. ex K. Schum.
Fadogia agrestis Schweinf.
ex Hiern
Fadogia ancylantha Hiern
Fadogia arenicola K. Schum.
& K. Krause
Fadogia cienkowskii Schweinf.
Fadogia elskensii De Wild.
Fadogia stenophylla Hiern
Fadogia tetraquetra K. Krause
Fadogia triphylla Baker
Fadogia verdcourtii
Tennant var. verdcourtii
Fadogiella stigmatoloba
(K. Schum) Robyns
Hutchinsonia barbata Robyns
Lagynias dryadum
(S. Moore) Robyns
Lagynias lasiantha (Sond.)
Bullock
Lagynias monteiroi (Oliv.)
Bridson
Lagynias pallidiflora Bullock
Zimba et al. 776 (UPS)
Borhidi et al. 85449 (UPS)
AJ617747/AJ620119/AJ617755/AJ620129/AJ876818
McPherson 16297 (MO)
AJ315088/AJ620134/-
Madsen 5495 (S)
AJ874980/AJ874942/AJ876819
Chapman & Chapman 9109 (UPS) AJ315103/AJ620136/AJ876820
AJ874981/AJ874943/AJ876821
Gereau et al. 6011 (UPS)
Lantz 101 (UPS)
Taylor et al. 8318 (UPS)
Mwangoka 1742 (UPS)
Bremer & Bremer 3799 (UPS)
Bidgood et al. 589 (UPS)
Gereau et al. 6010 (UPS)
-/AJ620137/AJ876822
AJ315118/AJ719191/AJ876823
-/AJ875117/AJ876824
AJ315099/AJ620139/AJ876825
AJ874982/AJ874944/AJ876826
AJ315116/AJ620140/AJ876827
Lawton 1318 (S)
AJ315100/AJ620141/AJ876828
Adam 20599 (UPS)
Bremer & Bremer 3811 (UPS)
AJ315102/AJ620142/AJ876829
AJ315090/AJ620146/AJ876830
Bremer & Bremer 3792 (UPS)
AJ315089/AJ620147/AJ876831
Bremer et al. 4297 (UPS)
AJ874983/AJ874945/AJ876832
Ntemi Sallu et al. 309 (UPS)
AJ874984/AJ874946/AJ876833
H. Lantz and B. Bremer: Phylogeny of Vangueria and closely related genera
Table 1. (Continued)
Species
Voucher
EMBL number ITS/trnT-F/
rpl16
Multidentia concrescens
Bidgood et al. 845 (K)
AJ315086/AJ620150/AJ876834
(Bullock) Bridson & Verdc.
AJ874985/AJ874947/AJ876835
Multidentia crassa (Hiern)
Lantz 150 (UPS)
Bridson & Verdc.
Multidentia fanshawei
Lovett et al. 3311 (K)
AJ315087/AJ620151/AJ876836
(Tennant) Bridson
AJ874986/AJ874948/AJ876837
Multidentia sclerocarpa
Luke 9442 (UPS)
(K. Schum.) Bridson
Pachystigma gillettii
Gilbert & Thulin 128 (UPS)
AJ874987/AJ874949/AJ876838
(Tennant) Verdc.
Pachystigma latifolium
Bremer et al. 4304 (UPS)
-/AJ874950/AJ876839
Sond.
Pachystigma loranthifolium
Luke 9464 (UPS)
AJ874988/AJ874951/AJ876840
(K. Schum.) Verdc.
Pachystigma pygmaeum
Pawek 12335 (BR)
AJ315091/AJ620152/AJ876841
Robyns
Pachystigma schumannianum
Mlangwa & Mbuso 1274 (UPS) AJ874989/AJ874952/AJ876842
(Robyns) Bridson & Verdc.
Pygmaeothamnus zeyheri (Sond.) Bremer et al. 4356 (UPS)
AJ617773/AJ620166/AJ876843
Robyns var. zeyheri
Robynsia glabrata Hutchinson
Hall & Amponsah 46545 (K)
AJ617774/AJ620170/Rytigynia adenodonta
(K. Schum.) Robyns var.
reticulata
(Robyns) Verdc.
Lantz 108 (UPS)
AJ874990/AJ874953/AJ876844
Rytigynia bagshawei
Borhidi et al. 84439 (UPS)
AJ315101/AJ620171/AJ876845
(S. Moore) Robyns
var. bagshawei
Rytigynia beniensis
Festo 1151 (UPS)
AJ874991/AJ874954/AJ876846
(De Wild.) Robyns
Rytigynia celastroides
Mwangoka & Maingo 1514 (UPS) AJ874992/AJ874955/AJ876847
(Baillon) Verdc.
AJ874993/AJ874956/AJ876848
Rytigynia decussata
Rulangaranga et al. 95 (MO)
(K. Schum.) Robyns
Rytigynia eickii (K. Schum. &
Borhidi et al. 84003 (UPS)
AJ874994/AJ874957/AJ876849
K. Krause) Bullock
Rytigynia fuscosetulosa Verdc.
Frimodt Moller et al. NG117 (K) AJ315097/AJ620173/Rytigynia hirsutiflora Verdc.
Luke et al. 9189 (UPS)
AJ874995/AJ874958/AJ876850
AJ874996/AJ874959/AJ876851
Rytigynia induta (Bullock) Verdc. Luke 9051 (UPS)
Rytigynia lichenoxenos
Luke et al. 9104 (UPS)
AJ874997/AJ874960/AJ876852
(K. Schum.) Robyns
Rytigynia longicaudata Verdc.
Borhidi & Pocs 85206 (UPS)
-/AJ874961/AJ876853
Rytigynia longipedicellata Verdc. Bidgood et al. 1577 (UPS)
-/AJ874962/AJ876854
Rytigynia monantha (K. Schum.) Hedrén et al. 308 (UPS)
-/AJ874963/AJ876855
Robyns
Rytigynia neglecta (Hiern) Robyns Gilbert et al. 7937 (UPS)
-/AJ874964/AJ876856
H. Lantz and B. Bremer: Phylogeny of Vangueria and closely related genera
Table 1. (Continued)
Species
Voucher
EMBL number ITS/trnT-F/
rpl16
Rytigynia parvifolia Verdc.
Rytigynia pseudolongicaudata Verdc.
Rytigynia sambavensis Cavaco
Rytigynia senegalensis Blume
Rytigynia seyrigii Cavaco
Rytigynia sp. L of F.T.E.A.
Rytigynia uhligii (K. Schum. &
K. Krause) Verdc.
Rytigynia umbellulata (Hiern)
Robyns
Rytigynia xanthotricha
(K. Schum.) Verdc.
Tapiphyllum cinerascens
(Welw. ex Hiern)
Robyns var. cinerascens
Tapiphyllum obtusifolium
(K. Schum.) Robyns
Tapiphyllum velutinum (Hiern)
Robyns
Vangueria apiculata K. Schum.
Vangueria esculenta S. Moore
Vangueria infausta Burch.
Vangueria madagascariensis
J. F. Gmelin
Vangueria parvifolia Sond.
Vangueria praecox Verdc.
Vangueria proschii Briq.
Vangueria randii S. Moore
Vangueria soutpansbergensis
N. Hahn
Vangueria volkensii K. Schum.
Vangueriopsis cf. longiflora Verdc.
Luke 8345 (UPS)
Kayombo 1953 (UPS)
Davis 2157 (K)
van den Berghen 8746 (BR)
Gereau et al. 5731 (MO)
Luke 9039 (UPS)
Borhidi et al. 84458 (UPS)
AJ874998/AJ874965/AJ876857
AJ874999/-/AJ875000/AJ874966/AJ315104/AJ620175/AJ876858
AJ875001/AJ874967/AJ875002/AJ874968/AJ875003/AJ874969/AJ876859
Gobbo & Gilagiza 860 (UPS)
AJ875004/AJ874970/AJ876860
Borhidi et al. 87353 (UPS)
AJ875005/AJ874971/AJ876861
Milne-Redhead 3292 (BR)
AJ315096/AJ620177/AJ876862
Gereau et al. 6669 (UPS)
AJ875006/AJ874972/AJ876863
Emanuelsson 672 (S)
AJ315098/AJ620178/AJ876864
Kårehed & Odhult 161 (UPS)
Lantz 145 (UPS)
Bremer et al. 4254 (UPS)
Bremer 3077 (UPS)
AJ315095/AJ620179/AJ876865
AJ875007/AJ874973/AJ876866
AJ617777/AJ620180/AJ876867
AJ224839/AJ620184/AJ876868
Bremer & Bremer 3771 (UPS)
Luke 9357 (UPS)
Blomberg et al. BMP 466 (UPS)
Luke 5161 (EA)
Bremer et al. 4324 (UPS)
AJ315092/AJ620181/AJ876869
AJ875008/AJ874974/AJ876870
AJ875009/AJ874975/AJ876871
AJ875010/AJ874976/AJ876872
AJ875011/AJ874977/AJ876873
Borhidi et al. 85162 (UPS)
Luke 8316 (UPS)
AJ875012/AJ874978/AJ876874
AJ617778/AJ620183/AJ876875
recently transferred to Canthium (Lantz and
Bremer 2004).
Molecular methods. DNA was extracted using
the CTAB method (Doyle and Doyle 1987) from
herbarium material, fresh, or silica-dried material.
The DNA was purified using either QiaQuick PCR
purification kit (QIAGEN) or caesium chloride/
ethidium bromide gradient centrifugation. PCR
amplification and sequencing for the ITS and trnTF region were performed as in Lantz and Bremer
(2004). Amplification and sequencing of rpl16 were
performed as for the trnT-F region, but used the
following primers: L16exon1 (Downie et al. 2000)
and 1067F (C. Asmussen; pers. comm.) for the
PCR amplification and primers1067F and rpl1618R (Asmussen 1999) for sequencing.
Phylogenetic methods. Sequences were aligned
manually. Informative insertion/deletion events
(indels) were coded manually using the simple
method of Simmons and Ochoterena (2000). The
phylogenies were constructed using parsimony with
the program PAUP* (Swofford 2002). All three
data sets (ITS, trnT-F, and rpl16) were run together
in a combined analysis as well as separately. A
chloroplast data set (trnT-F + rpl16) was also
analyzed. Incongruence between the ITS and
chloroplast data sets was assessed by the comparison of bootstrap values from the separate analyses.
H. Lantz and B. Bremer: Phylogeny of Vangueria and closely related genera
63
88
94
79
68
97
100
*
51
62
97
77
98
91
95
79
71
100
75
100
99
84
87
100
75
100
75
63
D
51
99
83
100
*
57
100
*
96
93
95
C
98
100
100
Canthium coromandelicum India
Canthium glaucum E
Canthium tetraphyllum E
Canthium armatum S, Z
Outgroup
Pygmaeothamnus cf. chamaedendrum S
Canthium inerme S, Z
Canthium bugoyense C, E, Z
Canthium stenosepalum W
Ancylanthos rubiginosus A, Z
Fadogia agrestis W
Pachystigma gillettii E
Pachystigma loranthifolium E
Pachystigma schumannianum E
Lagynias dryadum Z, S
Lagynias lasiantha S
Lagynias monteiroi S
Lagynias pallidiflora E
Pachystigma latifolium S
Pachystigma pygmaeum E, S, Z
Tapiphyllum cinerascens C, E, Z
Vangueria apiculata E, Z
Vangueria group
Vangueria volkensii E
Vangueria esculenta Z
Vangueria infausta E, S, Z
Vangueria proschii A, Z
Vangueria madagascariensis Afr.
Vangueria parvifolia S, Z
Vangueria soutpansbergensis S
Vangueria randii E, Z
Rytigynia fuscosetulosa E
Rytigynia induta E
Vangueria praecox E
Tapiphyllum obtusifolium E
Tapiphyllum velutinum Z
Canthium oligocarpum E, Z
Cuviera angolensis W
Multidentia concrescens E, Z
Multidentia crassa E, Z
Multidentia fanshawei E, Z
Multidentia sclerocarpa E
Pygmaeothamnus zeyheri C, E, Z, S
Robynsia glabrata W
Vangueriopsis cf. longiflora E
Fadogia ancylantha C, E, W, Z
Fadogia triphylla Afr.
Fadogia verdcourtii E
Fadogia arenicola E, Z
Fadogiella stigmatoloba E, Z
Fadogia cienkowskii Afr.
Fadogia elskensii C, E, Z
Fadogia stenophylla A, C, E, Z
Fadogia tetraquetra Afr.
Rytigynia umbellulata Afr.
Rytigynia adenodonta E, Z
Rytigynia celastroides E
Rytigynia parvifolia E
Rytigynia lichenoxenos E
Rytigynia sp. L E
Fadogia-Rytigynia
Rytigynia uhligii E, Z
group
Rytigynia beniensis C, E
Rytigynia neglecta E
Hutchinsonia barbata W
Rytigynia senegalensis W
Rytigynia bagshawei C, E
Rytigynia hirsutiflora E
Rytigynia longicaudata E
Rytigynia monantha E, Z
Rytigynia xanthotricha E
Rytigynia pseudolongicaudata E
Rytigynia sambavensis M
Rytigynia seyrigii M
Rytigynia decussata E
Rytigynia eickii E
Rytigynia longipedicellata E
H. Lantz and B. Bremer: Phylogeny of Vangueria and closely related genera
Table 2. Data set characteristics
Data set
Number
of taxa
ITS
67
trnT-F
Number
of characters
Informative
characters
(including indels)
Informative
indel characters
712
157
20
73
2096
111
22
rpl16
66
854
60
7
trnT-F + rpl16
73
2950
171
29
ITS + trnT-F+ rpl16
74
3662
328
49
ITS + trnT-F+ rpl16,
incongruent taxa
removed
69
3662
311
46
When strongly incongruent taxa had been identified (see results), all data sets were analyzed again
but with the incongruent taxa removed. A heuristic
search with 100 random addition replicates and
TBR branch-swapping was performed to find the
most parsimonious trees. Support was measured by
the bootstrap option as implemented by PAUP*
using 10000 bootstrap replicates, each with 5
random addition replicates, TBR branch-swapping
and MULTREES off.
Results
The number of taxa, total number of characters, number of informative characters, and
number of indel-characters for each of the six
data sets are presented in Table 2. We were
unable to get ITS sequences for seven species,
trnT-F sequences for one species, and rpl16
sequences for eight species (Table 1). The ITS
data set has the highest number of informative
characters followed by trnT-F, and rpl16. The
comparison is, however, likely influenced by
the uneven sample sizes of the different data
sets. About half of the informative characters
stem from the ITS data set. For all of the
analyses, the number of most parsimonious
trees was too large to be saved and the analyses
did not run to completion. We therefore
choose to present the majority rule consensus
trees from the bootstrap analyses. Results
from four of the analyses are presented; the
combined analysis (ITS + trnT-F + rpl16;
Fig. 1), ITS (Fig. 2), the chloroplast tree (trnTF + rpl16; Fig. 3), and a combined analysis
with strongly incongruent taxa removed
(Fig. 4 ). We found no cases of topological
incongruence between the phylogenies based
on the trnT-F and rpl16 data sets (results not
b
Fig. 1. Majority rule consensus tree from the bootstrap analysis of the combined (ITS + trnT-F + rpl16) data
set. Bootstrap support ‡50 is included above nodes. Letters in the tree refer to clades discussed in the text.
Letters added after the taxa names indicate geographical distribution (see material and methods), i.e.
Afr.=Subsaharan Africa, A=Angola with Namibia, C=Central Africa, E=East Africa, M=Madagascar,
S=South Africa, Z=Zambia with Botzwana, Malawi, Mozambique, and Zimbabwe (Zambesian distribution),
W=West Africa. Types of genera are indicated in bold. Clades which receive strong support both from the
plastid and nuclear data sets are indicated by an *
H. Lantz and B. Bremer: Phylogeny of Vangueria and closely related genera
77
57
57
92
100
55
64
84
96
95
67
54
64
65
53
82
F
100
62
98
92
E
63
G
52
96
50
58
77
100
100
72
99
54
92
92
Canthium coromandelicum
Canthium glaucum
Canthium tetraphyllum
Canthium armatum
Canthium inerme
Pygmaeothamnus cf. chamaedendrum
Canthium bugoyense
Canthium stenosepalum
Ancylanthos rubiginosus
Fadogia agrestis
Lagynias pallidiflora
Pachystigma loranthifolium
Pachystigma gillettii
Pachystigma schumannianum
Vangueria apiculata
Vangueria volkensii
Vangueria randii
Lagynias dryadum
Lagynias lasiantha
Lagynias monteiroi
Pachystigma pygmaeum
Rytigynia fuscosetulosa
Rytigynia induta
Vangueria praecox
Tapiphyllum cinerascens
Vangueria esculenta
Vangueria infausta
Vangueria proschii
Vangueria madagascariensis
Vangueria parvifolia
Vangueria soutpansbergensis
Tapiphyllum obtusifolium
Tapiphyllum velutinum
Canthium oligocarpum
Multidentia concrescens
Multidentia crassa
Multidentia fanshawei
Multidentia sclerocarpa
Cuviera angolensis
Robynsia glabrata
Fadogia ancylantha
Fadogia triphylla
Fadogia verdcourtii
Fadogia arenicola
Fadogiella stigmatoloba
Rytigynia adenodonta
Rytigynia beniensis
Rytigynia celastroides
Rytigynia parvifolia
Rytigynia sp. L
Rytigynia lichenoxenos
Rytigynia uhligii
Fadogia elskensii
Fadogia tetraquetra
Rytigynia umbellulata
Rytigynia decussata
Rytigynia eickii
Hutchinsonia barbata
Rytigynia bagshawei
Rytigynia hirsutiflora
Rytigynia pseudolongicaudata
Rytigynia xanthotricha
Rytigynia sambavensis
Rytigynia seyrigii
Rytigynia senegalensis
Pygmaeothamnus zeyheri
Vangueriopsis cf. longiflora
Outgroup
Vangueria group
Fadogia-Rytigynia
group
H. Lantz and B. Bremer: Phylogeny of Vangueria and closely related genera
shown). Since both genes are from the plastid
genome they are likely to share the same
evolutionary history. We therefore combined
the two data sets into a single chloroplast data
set and only present the results from the
bootstrap analysis of this data set. Compared
to the phylogenies of the individual (trnT-F
and rpl16) data sets, the combined chloroplast
tree has both increased resolution and support.
There are strongly supported clades in all
presented phylogenies. Comparing the ITS
and chloroplast phylogenies, both include a
similar number of strongly supported clades
(above 90% bootstrap), but only in three
instances are clades supported strongly from
both data sets (see Fig. 1). Comparisons are,
however, made difficult by the uneven sample
sizes of the chloroplast and ITS data sets.
This is especially true in the Fadogia-Rytigynia group in which seven taxa are present in
only one of the data sets (Table 1). There are
also several cases of incongruence in the
comparison between the ITS and chloroplast
phylogenies. Most incongruencies are weakly
supported (e.g. the position of Rytigynia
induta), but there are some that are more
strongly supported, i.e. situations where a
strongly supported node in one of the phylogenies is contradicted by an at least moderately supported node in the other. In the
Fadogia-Rytigynia group the positions of
Hutchinsonia barbata, Rytigynia beniensis,
and the clade consisting of R. decussata and
R. eickii are strongly incongruent. In the
Vangueria group, no taxon is strongly incongruent as defined above, but Ancylanthos
rubiginosus has significantly different positions in the two trees. In the ITS tree,
Ancylanthos rubiginosus has an internal position in the group, but is in the chloroplast
tree sister to a clade consisting not only
of the other members of the Vangueria
group but also Multidentia, Pygmaeothamnus,
Robynsia, and Vangueriopsis.
Cases where taxa have an unresolved
position in one of the phylogenies and a
resolved in the other (e.g. the positions of
Cuviera angolensis and Robynsia glabrata)
could possibly be influenced by incongruence,
but the unresolved position in one of the
phylogenies makes any comparisons uninformative. Of more importance are strongly
supported nodes which collapse when the data
sets are combined. In the Vangueria group, no
strongly supported clades present in the chloroplast or ITS phylogenies collapse in the
combined phylogeny, although clade A
(Figs. 3 and 4) is more strongly supported
(bp=96) in the chloroplast phylogeny than in
the combined phylogeny (bp=79), indicating
some conflict. Of greater concern are the
strongly supported clades present in the ITS
phylogeny for a clade in the Fadogia-Rytigynia
group (clade E; Fig. 2 ) and the moderately
supported clade of Cuviera and Robynsia
(clade F; Fig. 2 ) that collapses in the
combined phylogeny ( Fig. 1 ). These clades
are not present in the chloroplast phylogeny
(Fig. 3) and the incongruence can therefore
not be attributed to a single taxon or a single
clade such as in the above mentioned examples.
After we identified Ancylanthos rubiginosus, Hutchinsonia barbata, Rytigynia beniensis,
R. decussata, and R. eickii as strongly incongruent, these taxa were removed from further
analyses (results only shown for the combined
data set with incongruent taxa removed;
Fig. 4). Comparing the results from the combined analyses with incongruent taxa included
or excluded ( Fig. 1 and Fig. 4 resp.), little was
changed in the phylogeny for the Vangueria
group, although the support for the node
separating the clade consisting of Tapiphyllum
obtusifolium and T. velutinum from the other
taxa in the group was increased from 62 to 85
and the support for the Vangueria group from
91 to 99. In the Fadogia-Rytigynia group the
b
Fig. 2. Majority rule consensus tree from the bootstrap analysis of the ITS data set. Bootstrap support ‡ 50 is
included above nodes. Letters in the tree refer to clades discussed in the text
H. Lantz and B. Bremer: Phylogeny of Vangueria and closely related genera
72
69
76
96
89
78
100
96
71
64
86
57
62
92
54
57
87
100
73
100
95
87
69
87
100
76
98
67
73
98
67
99
100
90
82
100
62
99
59
Canthium coromandelicum
Canthium glaucum
Canthium tetraphyllum
Canthium armatum
Pygmaeothamnus cf. chamaedendrum
Canthium inerme
Canthium bugoyense
Canthium stenosepalum
Ancylanthos rubiginosus
Fadogia agrestis
Pachystigma gillettii
Lagynias dryadum
Lagynias lasiantha
Lagynias monteiroi
Lagynias pallidiflora
Pachystigma latifolium
Pachystigma pygmaeum
Tapiphyllum cinerascens
Vangueria apiculata
Vangueria esculenta
Vangueria infausta
Vangueria madagascariensis
Vangueria parvifolia
Vangueria proschii
Vangueria randii
Vangueria soutpansbergensis
Vangueria volkensii
Pachystigma loranthifolium
Pachystigma schumannianum
Rytigynia fuscosetulosa
Rytigynia induta
Tapiphyllum obtusifolium
Tapiphyllum velutinum
Vangueria praecox
Vangueriopsis cf. longiflora
Pygmaeothamnus zeyheri
Robynsia glabrata
Multidentia concrescens
Multidentia crassa
Multidentia fanshawei
Multidentia sclerocarpa
Canthium oligocarpum
Cuviera angolensis
Fadogia ancylantha
Fadogia triphylla
Fadogia verdcourtii
Rytigynia beniensis
Fadogia arenicola
Fadogia cienkowskii
Fadogia elskensii
Fadogia stenophylla
Fadogia tetraquetra
Fadogiella stigmatoloba
Rytigynia adenodonta
Rytigynia celastroides
Rytigynia parvifolia
Rytigynia lichenoxenos
Rytigynia sp. L
Rytigynia uhligii
Rytigynia neglecta
Rytigynia senegalensis
Rytigynia umbellulata
Hutchinsonia barbata
Rytigynia bagshawei
Rytigynia hirsutiflora
Rytigynia longicaudata
Rytigynia monantha
Rytigynia xanthotricha
Rytigynia decussata
Rytigynia eickii
Rytigynia longipedicellata
Rytigynia sambavensis
Rytigynia seyrigii
Outgroup
Vangueria group
Fadogia-Rytigynia
group
H. Lantz and B. Bremer: Phylogeny of Vangueria and closely related genera
changes in support and resolution were more
significant to the point of making comparisons
difficult. However, a clade of Rytigynia species
where all but R. seyrigii have long appendages
on the corolla lobes (clade C; Figs. 1 and 4) is
supported in both phylogenies, but the support is lowered from 95 to 57 when the
incongruent taxa are removed. The large clade
in which Hutchinsonia is included (clade D;
Fig. 1) has weak support (63), but this is
increased to 95 (clade D; Fig. 4) when the
incongruent taxa are removed, although these
two clades are not identical and the results are
possibly influenced not only by incongruence
but also by sampling effects.
Comparing the phylogenies based on the
individual data sets with and without incongruent taxa (results only shown for phylogenies with incongruent taxa included; Figs. 2
and 3), only minor changes in support occur
by the removal of taxa for nodes at which the
incongruent taxa were not attached, and comparisons of support can equally well be done
with the incongruent taxa included (Figs. 2
and 3).
The Vangueria group as circumscribed by
Lantz and Bremer (2004) is supported in the
ITS and combined phylogenies but not in the
chloroplast phylogeny due to the incongruent
position of Ancylanthos rubiginosus. The
Fadogia-Rytigynia group is strongly supported
in all trees. In the chloroplast phylogeny
(Fig. 3 ), the clade is sister to a clade consisting
of all other taxa, and this result is also
favoured by the combined analyses, but is
unresolved in the ITS phylogeny ( Fig. 2 ).
Rytigynia and Fadogia are polyphyletic in all
four phylogenies and there are indications that
this is true also for Pachystigma, Tapiphyllum
and Vangueria. Pygmaeothamnus is present
both in the outgroup and in the ingroup and is
thus also polyphyletic, but this has been
discussed elsewhere (Lantz and Bremer 2004)
and will not be investigated in detail here.
Within the Fadogia-Rytigynia group the situation is complex. The taxa with incongruent
positions and the low supported or unresolved
nodes hamper our ability to draw conclusions,
but Fadogia and Rytigynia are not supported
as monophyletic in any of the trees. Multidentia is the only genus which is monophyletic in
all four phylogenies, although with weak
support in the ITS phylogeny.
Discussion
We will divide the discussion into two major
parts. In the first part we discuss the results of
the phylogenetic analyses. Morphological
characters of importance for the delimitation
of the clades and genera are also discussed, but
we restrict the discussion to characters found
to be informative in Lantz and Bremer (2004).
In the second part we try to explain the
incongruencies noticed in the comparisons
between the individual analyses. We base our
discussion on the phylogeny in which the
strongly incongruent taxa have been removed
(Fig. 4), unless otherwise noted. This phylogeny exhibits increased support and resolution
in comparison to the analyses based on the
individual data sets. Although the taxa with
most strongly incongruent positions have been
removed, it is possible that the phylogeny still
is influenced by incongruence. Indeed, in two
cases did the combination of data sets with
taxa removed result in significantly lowered
bootstrap support for a node, indicating
conflicting phylogenetic signals. With this in
mind, we refrain from making changes to the
classification in situations not unequivocally
supported by all data sets, unless support from
morphology can corroborate any of the phylogenies. We often choose to use the term
b
Fig. 3. Majority rule consensus tree from the bootstrap analysis of the chloroplast (trnT-F + rpl16) data set.
Bootstrap support ‡ 50 is included above nodes. Letters in the tree refer to clades discussed in the text.
Ancylanthos rubiginosus is supported as a member of the Vangueria group in the ITS and combined trees
(Figs. 1, 2, and 4)
H. Lantz and B. Bremer: Phylogeny of Vangueria and closely related genera
65
86
93
82
67
B
97
100
60
97
79
A
85
76
98
95
78
99
78
52
100
100
98
84
100
87
100
78
72
99
95
D
71
100
51
96
G
100
83
93
75
57
C
94
Canthium coromandelicum
Canthium glaucum
Canthium tetraphyllum
Canthium armatum
Pygmaeothamnus cf. chamaedendrum
Canthium inerme
Canthium bugoyense
Canthium stenosepalum
Canthium oligocarpum
Cuviera angolensis
Fadogia agrestis
Pachystigma gillettii
Pachystigma loranthifolium
Pachystigma schumannianum
Lagynias dryadum
Lagynias lasiantha
Lagynias monteiroi
Lagynias pallidiflora
Pachystigma latifolium
Pachystigma pygmaeum
Tapiphyllum cinerascens
Vangueria apiculata
Vangueria volkensii
Vangueria esculenta
Vangueria infausta
Vangueria proschii
Vangueria madagascariensis
Vangueria parvifolia
Vangueria soutpansbergensis
Vangueria randii
Rytigynia fuscosetulosa
Rytigynia induta
Vangueria praecox
Tapiphyllum obtusifolium
Tapiphyllum velutinum
Vangueriopsis cf. longiflora
Multidentia concrescens
Multidentia crassa
Multidentia fanshawei
Multidentia sclerocarpa
Pygmaeothamnus zeyheri
Robynsia glabrata
Fadogia ancylantha
Fadogia triphylla
Fadogia verdcourtii
Fadogia arenicola
Fadogiella stigmatoloba
Fadogia cienkowskii
Fadogia elskensii
Fadogia stenophylla
Fadogia tetraquetra
Rytigynia adenodonta
Rytigynia celastroides
Rytigynia parvifolia
Rytigynia lichenoxenos
Rytigynia sp. L
Rytigynia uhligii
Rytigynia neglecta
Rytigynia umbellulata
Rytigynia senegalensis
Rytigynia bagshawei
Rytigynia hirsutiflora
Rytigynia longicaudata
Rytigynia monantha
Rytigynia xanthotricha
Rytigynia pseudolongicaudata
Rytigynia sambavensis
Rytigynia seyrigii
Rytigynia longipedicellata
Outgroup
Vangueria group
Fadogia-Rytigynia
group
H. Lantz and B. Bremer: Phylogeny of Vangueria and closely related genera
‘incongruent taxon/taxa’ rather than the bulkier but more correct ‘taxon/taxa with incongruent positions’ fully aware of the fact that a
taxon (when represented by a single terminal)
cannot be incongruent in itself, but prefer the
shorter, less cumbersome term.
The Vangueria group. This group was first
identified in Lantz et al. (2002) and also
investigated in Lantz and Bremer (2004).
Lagynias, Pachystigma, Tapiphyllum, Vangueria, and one species of Rytigynia, R. fuscosetulosa, were identified as belonging to this
clade, and also Ancylanthos rubiginosus, but
with some hesitation due to the incongruent
positions for this taxon supported by the
plastid and nuclear data sets. All of these
genera have plurilocular ovaries, a character
traditionally used to distinguish between Vangueria and the bilocular genus Canthium, the
two first described genera in the tribe. The
group is identical to ‘Gattungskomplex Vangueria’ suggested by Igersheim (1989) with the
exception of R. fuscosetulosa. In the present
study, the ITS and chloroplast phylogenies
support a similar circumscription of the Vangueria group, with the exception of
Ancylanthos rubiginosus. Of the two possible
positions for A. rubiginosus suggested by the
ITS and chloroplast phylogenies, the internal
position in the Vangueria group seen in the ITS
phylogeny is better supported by morphology.
Also in the Vangueria group are Pachystigma
pygmaeum and Tapiphyllum cinerascens. All
three are geofrutices and sometimes have
ternate leaves, and both A. rubiginosus and
T. cinerascens have short, stiff external indumentum on the corollas. Geofrutescent habit
and ternate leaves are otherwise rare features
in the Vangueria group, but external indumentum on the corollas is more common (e.g.
Bridson 1998). The inclusion of Ancylanthos in
the Vangueria group is thus supported by
morphology and by the ITS phylogeny. To
conclude, we consider the Vangueria group to
comprise the genera Ancylanthos, Lagynias,
Pachystigma, Tapiphyllum, Vangueria, and the
three species Fadogia agrestis, Rytigynia
fuscosetulosa, and R. induta.
Nine of the included Vangueria species, all
in subgenus Vangueria, form a moderately
supported clade (A; Fig. 4) together with four
species of Lagynias, Pachystigma latifolium,
P. pygmaeum, and Tapiphyllum cinerascens. A
tenth species, V. praecox, tentatively included
in Vangueria and the single member of subgenus Itigi (Verdcourt 1981), instead forms a
clade with Rytigynia fuscosetulosa and R.
induta at a more basal position in the
Vangueria group. Vangueria subgenus Vangueria has traditionally been recognized by a
combination of large leaves and lax manyflowered inflorescences, but is in the most
recent circumscription (Verdcourt 1981, Bridson 1998) morphologically heterogeneous.
Vangueria parvifolia and V. soutpansbergensis
both have small leaves and few-flowered,
shortly pedunculate and dense inflorescences
and form a moderately supported clade in the
combined phylogeny (Fig. 4). Vangueria parvifolia was earlier included in Tapiphyllum but
was found to be atypical of that genus and was
transferred (Bridson 1998) shortly after the
morphologically similar South African endemic V. soutpansbergensis was described (Hahn
1997). Two other clades formed by the Vangueria species are well delimited by type of
calyx lobes, a character earlier suggested to be
of importance in the classification of Vangueria
(Bridson 1998). The type species V. madagascariensis forms a strongly supported clade
together with V. esculenta, V. infausta, and
V. proschii, all of which have triangular to
narrowly oblong calyx lobes. Vangueria
apiculata and V. volkensii, both with narrowly
oblong to linear calyx lobes, group together
with strong support. Surprisingly V. randii, a
b
Fig. 4. Majority rule consensus tree from the bootstrap analysis of the combined data set (ITS + trnT-F +
rpl16) with putative hybrids removed. Bootstrap support ‡ 50 is included above nodes. Letters in the tree refer
to clades discussed in the text
H. Lantz and B. Bremer: Phylogeny of Vangueria and closely related genera
third species with similar elongate calyx lobes,
does not group with these species but has an
unresolved position in the same clade. Lagynias is a genus of five species distributed in
eastern and southern Africa characterized by
well-developed often oblong or narrowly
obovate calyx lobes and usually reflexed
corolla lobes in the mature flower (Bullock
1931). Two species of Lagynias, L. dryadum
and L. lasiantha, form a strongly supported
group, but Lagynias as a genus is not supported
as
monophyletic.
Tapiphyllum
cinerascens is a highly variable species (Verdcourt and Bridson 1991) which in the phylogeny (Fig. 4) is distanced from the two other
included species of Tapiphyllum. The genus is
considered ill-defined (Bridson 1998) and is
diagnosed principally by a thick indumentum,
dense inflorescences, and mostly elongate calyx
lobes.
Sister to the clade including most of the
Vangueria species (clade A; Fig. 4) is a weakly
supported clade (B; Fig. 4) consisting of three
species of Pachystigma and one representative
of Fadogia, F. agrestis. Pachystigma is thus
represented in two clades, a division supported
by type of habit. Pachystigma latifolium and
P. pygmaeum are both geofrutices while the
three other species are shrubs or small trees.
Fadogia agrestis is a West African species
obviously misplaced in Fadogia, differing from
the species of Fadogia present in the FadogiaRytigynia group by its large ovate to triangular
calyx lobes and consistently paired leaves. As
shown by the phylogeny and also supported by
morphology, Pachystigma contains smaller
groups of closely related species, but is as a
genus united by little but an absence of the
characters used to delimit Tapiphyllum and
Vangueria. The problematic circumscription of
the genus has also been discussed elsewhere
(e.g. Verdcourt 1981, Bridson 1996).
The already mentioned clade of Rytigynia
fuscosetulosa, R. induta, and Vangueria
praecox is interesting in that all three species
were tentatively included in their genera, but a
close relationship between the three has never
been proposed. Rytigynia fuscosetulosa is a
member of the small (two species) subgenus
Sali (Verdcourt 1987, Verdcourt and Bridson
1991) and was when described mentioned as
intermediate between several genera and with
pyrenes similar to Vangueria (Verdcourt 1981).
Rytigynia induta has been suggested to be
misplaced in the genus (D. Bridson, pers.
comm.) and Vangueria praecox was tentatively
included in Vangueria (Verdcourt 1981). All
three species have few-flowered and shortly
pedunculate inflorescences, but this is not
unknown from other species in the Vangueria
group (e.g. Vangueria parvifolia and V. soutpansbergensis) and we can find no unique
morphological synapomorphy for the clade.
Two species of Tapiphyllum form a
strongly supported clade as sister to the other
taxa of the Vangueria group. Tapiphyllum
obtusifolium is restricted to Tanzania and
T. velutinum has a Zambesian distribution.
These species are both shrubs or small trees in
contrast to the type species of Tapiphyllum, the
geofrutex T. cinerascens (clade B; Fig. 4). They
otherwise share a number of features with
T. cinerascens such as a thick indumentum on
the leaves, dense inflorescences, and elongate
often linear calyx lobes, and would based on
morphology be suspected to be more closely
related.
None of the genera in the Vangueria group
are supported as monophyletic, and indeed,
the weak internal nodes in the clade do not
either enable us to tell with certainty if the
genera are paraphyletic or polyphyletic. However, there are indications that Pachystigma,
Tapiphyllum, and Vangueria are not monophyletic. Moreover, there is little morphological
support for the current circumscriptions of the
genera. The genera are not homogeneous in
their current circumscriptions. All genera
include groups of species clearly closely related
but there are also a number of species often
tentatively included and clearly dissimilar from
the other species. These are also quite often
intermediate in generic characters. The here
included Vangueria parvifolia and V. soutpansbergensis, or Lagynias monteiroi, are examples
of such species but there are more we have not
H. Lantz and B. Bremer: Phylogeny of Vangueria and closely related genera
been able to include such as Tapiphyllum
schliebenii Verdc., a species of Tapiphyllum
with lax inflorescences. With the addition of
two species currently included in Rytigynia and
one in Fadogia, as discussed earlier, the generic
characters of the genera in the Vangueria
group break down even further. The problematic circumscription of these genera has also
been noted by other authors. Verdcourt (1981)
wrote (about Pachystigma) ‘There are no
constant technical characters to distinguish it
from Vangueria save facies.’. He goes on to
state that ‘Tapiphyllum is no more than a
velvety Pachystigma and some South African
species are certainly intermediate in character…’. Bridson (1996) noted in the discussion
on Ancylanthos monteiroi Oliv. (now Lagynias
monteiroi (Oliv.) Bridson) that ‘The distinction
between Pachystigma and Lagynias is in need
of clarification…’. We agree with these views
and consider a new classification for the genera
in the Vangueria group to be desirable. The
best solution is to consider the whole Vangueria group as one genus; a classification that
receives support both from the phylogeny and
from morphological characters. Vangueria is
the oldest name in the group (Jussieu 1789),
and would have priority. With the exception of
Ancylanthos, this clade is present in all phylogenies. An alternative solution would be to
recognize the smaller clades present (i.e. A, B
etc; Fig. 4 ) as genera, but these clades are
likely to change with the addition of new
species and we are also unable to find morphological support for any of the clades.
Vangueria in this new sense is recognized by
a combination of the following characters:
domatia rarely present, inflorescences usually
borne at nodes from which the leaves have
fallen, bracteoles small (present on secondary
branches, usually not more than 1 mm in
length), smooth retrorse hairs in the corolla
(Lantz and Bremer 2004), and large fruits
(above 1 cm in length) with 3 to 5 locules. This
combination of characters is not known from
any other currently recognised genus in the
tribe and will greatly facilitate the identification of Vanguerieae genera. Below, we make
combinations at the genus level and also at the
species level for all currently recognised species.
The Fadogia-Rytigynia group. This group
was identified by Lantz et al. (2002), and is
identical in circumscription to ‘Gattungskomplex Rytigynia’ suggested by Igersheim (1989)
on morphological grounds. For this group
there exists no conflict as regards the circumscription, it is strongly supported in all phylogenies (Figs. 1, 2, 3, and 4). Internally
however, the phylogeny is strongly affected
by incongruence between the chloroplast and
ITS data sets as enumerated above. The great
extent of these incongruencies greatly hinders
our ability to draw conclusions about the
phylogeny of the group. We can, however,
make comparisons with morphology and see
to which extent the phylogenies support the
current classification. As a general rule, the
Fadogia-Rytigynia group can be distinguished
from the Vangueria group or any of the other
genera in the large-flowered clade by a presence of domatia and a calyx without or with
poorly developed calyx lobes, although this
rule is not without exceptions.
None of the included genera are supported
as monophyletic in any of the phylogenies, but
the small genera Fadogiella (three species) and
Hutchinsonia (two species) are both sampled
by one species each and we are thus unable to
test the monophyly of these genera. Fadogiella
stigmatoloba was in an earlier analysis with a
smaller sample (Lantz et al. 2002) nested
within Fadogia, but this result is not corroborated here. It groups with Fadogia arenicola
with weak support in the ITS and combined
analysis, a position supported by the thick
indumentum of both species. Hutchinsonia is
morphologically close to Rytigynia and is
mainly distinguished by its long and slender
corolla tubes. Fadogia and Rytigynia are the
two largest genera in the group, both comprising at least 50 species. Fadogia is diagnosed
by a geofrutescent habit and leaves at least
sometimes in whorls of three (or more).
Rytigynia is much harder to diagnose and is
recognized mainly by a shrubby habit and
H. Lantz and B. Bremer: Phylogeny of Vangueria and closely related genera
absence of the characters typical of the genera
in the Vangueria group or Fadogia. As shown
here, and earlier (Lantz et al. 2002, Lantz and
Bremer 2004), Rytigynia is polyphyletic with
species included also in the spiny group (the
present outgroup) and in the Vangueria-group.
The majority of the currently recognized
species in Rytigynia belong in the FadogiaRytigynia group and we consider these to
constitute Rytigynia s. str. The characters most
useful to distinguish between Rytigynia s.str.
and the species incorrectly included in Rytigynia (such as the here sampled R. fuscosetulosa
and R. induta) is the development of the calyx
lobes and the size of the fruits. Rytigynia s. str.
has a truncate or very shortly toothed calyx
and fruits rarely more than 10 mm in diameter. Rytigynia induta has short calyx lobes and
is in many ways morphologically similar to
Rytigynia s. str. but has much larger fruits
(20 mm in diameter compared to usually
below 10 mm). R. fuscosetulosa has elongate
calyx lobes. As often is the case in Vanguerieae, even distantly related species can be
closely similar morphologically and it is only
with the aid of a phylogeny the distinguishing
characters can be found.
A clade consisting of Fadogia ancylantha,
F. triphylla, and F. verdcourtii is consistently
recovered in all phylogenies although with the
addition of Rytigynia beniensis in the chloroplast phylogeny. All three Fadogia species have
corollas of 5 mm or more and have in contrast
to the other included species of Fadogia
sometimes paired leaves, especially on the
younger parts of the branches. This character
has not been considered of importance earlier,
but is strongly supported here. Fadogiella
stigmatoloba is the only geofrutex sampled
here which otherwise has both paired or
whorled leaves. Rytigynia beniensis does not
share any of these characters or any other
characters used to delimit Fadogia. The ITS
phylogeny groups R. beniensis with several
species of Rytigynia in a weakly supported
clade (clade G; Fig. 1 ), a position much better
supported by morphology. Also included in
the same clade is R. celastroides, a species
which shares the rare character branches
sometimes in whorls of three with R. beniensis.
However, R. umbellulata, considered very close
to R. beniensis (Verdcourt 1987), instead forms
a moderately supported clade with Fadogia
elskensii and F. tetraquetra in the same phylogeny. The two Fadogia species are considered
close (Verdcourt 1981) but the relationship
with R. umbellulata is quite unexpected. In the
combined analysis (Fig. 4) F. tetraquetra
groups with F. stenophylla with strong support,
F. elskensii forms a moderately supported
clade with F. cienkowskii, and R. umbellulata
has unresolved position in a moderately supported clade. Fadogia cienkowskii and F. stenophylla were, however, not sequenced for ITS.
The clade in which R. beniensis was supported
to belong by the ITS phylogeny receives strong
support in both of the combined analyses
(clade G; Figs. 1 and 4), and the support is
strongest when the incongruent taxa are not
included (Fig. 4). None of the taxa in the clade
have long appendages (over 2 mm) on the
corolla lobes, a character otherwise common in another clade (C; Fig. 4). Appendages
are also missing from R. longipedicellata, R.
neglecta, R. senegalensis, R. umbellulata, and
two of the taxa identified as strongly incongruent, R. decussata and R. eickii. Rytigynia
longipedicellata is morphologically similar to
R. eickii, and forms a strongly supported clade
with this species in the chloroplast phylogeny
(Fig. 3), but was not sequenced for ITS and
the position in the combined phylogeny
(Fig. 4) as sister to the clade with long
appendages is thus only based on chloroplast
data. Hutchinsonia barbata also has appendages on the corolla lobes and the position
indicated by the ITS phylogeny ( Fig. 2 ) is
thus better supported by morphology. The two
Malagasy specimens R. sambavensis and R.
seyrigii group together in all phylogenies, but
only with weak support in the chloroplast
phylogeny. The clade is strongly supported as
sister to the other taxa in the appendaged clade
by the combined phylogeny with incongruent
taxa included (Fig. 1), but this support is
greatly decreased when the incongruent taxa
H. Lantz and B. Bremer: Phylogeny of Vangueria and closely related genera
are removed (Fig. 4). In the combined analysis
with incongruent taxa removed, the FadogiaRytigynia group is divided into two clades, one
of which is strongly supported (clade D; Fig. 4.
Apart from the partial congruence with presence or absence of appendages on the corolla
lobes, we see little support for this division
from morphology.
We can thus find morphological support
for clades present in both the chloroplast and
ITS phylogenies and none of the two phylogenies agree with morphology better than the
other. The widespread incongruence for these
genera puts all phylogenies in some doubt, and
we are not prepared to make any changes to
the classification. The phylogenies do not
enable us to present any classification which
would result in monophyletic and unequivocally supported genera. In addition, several of
the strongly supported clades lack morphological support. The inclusion of the whole clade
in one genus would result in a monophyletic
but morphologically heterogeneous genus. At
this point, when a number of the currently
recognized species are poorly known, especially those occurring in West and Central
Africa, we prefer to stress the morphological
and geographical variation present within the
group by retaining the genera rather than hide
it within one very large genus.
Other genera in the large-flowered group.
In the chloroplast and combined phylogenies,
Canthium oligocarpum, Cuviera, Multidentia,
Pygmaeothamnus zeyheri, Robynsia, and Vangueriopsis form a weakly to moderately supported clade together with the Vangueria
group as sister to the Fadogia-Rytigynia group.
Their relationships to the Vangueria group or
to each other are however weakly supported.
The only relationship which receives support
here is the moderately supported clade formed
by Cuviera and Robynsia in the ITS phylogeny
(clade F, Fig. 2 ). Cuviera is a morphologically
distinct genus centred in West Africa but with
some few representatives also in central and
East Africa. Diagnostic for the genus are large
and many-flowered inflorescences with linear
to lanceolate or even elliptic bracts and
bracteoles, and many species also have hairs
on the styles, sometimes in combination with
peculiar swellings (Hallé 1959). The calyx lobes
are also often large and foliose, usually similar
to the bracts and bracteoles. Today the genus
includes around 20 species (Bridson 1998). The
monotypic genus Robynsia (Hutchinson 1931)
has very similar inflorescences to Cuviera, but
has long and slender corolla tubes not known
in Cuviera. A relationship between Cuviera and
Robynsia is thus supported by morphology,
but the clade collapses in the combined
phylogenies, possibly due to incongruence.
Canthium oligocarpum is a member of the
small (three species) subgenus Lycioserissa. It
is clearly distanced both from the type species
of Canthium, C. coromandelicum and the type
species of subgenus Lycioserissa, C. inerme,
both of which are represented in the outgroup, but is of uncertain position in the
large-flowered group. It is similar in leaf
morphology to some species of Multidentia
(e.g. M. sclerocarpa), and is in the ITS
phylogeny ( Fig. 2 ) weakly supported as
sister to that genus, but lacks the morphological synapomorphies of Multidentia and
should no be transferred until its phylogenetic
position can be ascertained with better support.
Multidentia is one of the best delimited
genera in Vanguerieae (Bridson 1987). Eleven
species are known, and the genus has a wide
distribution in tropical Africa. The genus is
easily recognized by a combination of vague
tertiary nerves, a well-developed calyx limb
tube, and thickly woody pyrenes. The sample
here includes most of the morphological variation in the genus and the monophyly of
Multidentia is strongly supported.
Pygmaeothamnus is a genus of two geofrutices of which P. chamaedendrum is restricted
to South Africa and P. zeyheri has a wide
essentially Zambesian distribution. A combination of a geofrutescent habit and bilocular
ovaries is the major morphological character
used to delimit the genus. The genus is
polyphyletic and is represented both in the
outgroup and in the large-flowered group.
H. Lantz and B. Bremer: Phylogeny of Vangueria and closely related genera
Vangueriopsis includes four species and is
recognized by long (over 15 mm) and linear
corolla lobes, long exserted stamens, and hairs
usually present on stamens. The specimen here
sampled is a fruiting specimen tentatively
identified to Vangueriopsis longiflora (see also
Lantz and Bremer 2004) but is without doubt a
member of the genus.
Even though not really tested here, we find
it highly unlikely that the Vangueria group is
nested within any of these genera. The monophyly of Multidentia is strongly demonstrated
here (Fig. 4), Cuviera and Vangueriopsis are
strongly delimited in a morphological sense,
Robynsia is monotypic and Pygmaeothamnus is
known to be represented only by the type
species P. zeyheri in the large-flowered group.
The phylogenetic affinities of Canthium
oligocarpum remain unknown and, as was
concluded also in an earlier study (Lantz and
Bremer 2004), the species cannot remain in
Canthium but neither morphology nor phylogeny enables us to suggest how to deal with the
species.
Incongruencies. As discussed above, the
ITS ( Fig. 2) and chloroplast (Fig. 3) trees
are partly incongruent. Phylogenetic incongruence can be caused by a number of phenomena, some reflecting biological processes such
as hybridization or lineage sorting, but there
are also technical causes such as taxon sampling or insufficient data which can lead to
incongruence (Wendel and Doyle 1998). A
common case of incongruence is when weakly
supported clades contradict each other. An
example of this is the position of Rytigynia
induta. Such weakly supported results are not
necessarily reflecting the evolutionary history
of the taxa studied, but can be the result of
homoplasy (e.g. Kellogg et al. 1996) and are
therefore usually not taken into account in a
discussion on phylogeny. However, there are
also some strongly supported incongruencies
in this study, and these cannot easily be
dismissed as artefacts caused by technical
phenomena.
In the Vangueria group we are able to
identify a single taxon, Ancylanthos
rubiginosus, as incongruent in the comparison
between the ITS and chloroplast phylogenies.
Based on comparisons with morphology (see
above) the internal position in the Vangueria
group suggested by the ITS phylogeny is the
most likely for the organism. The incongruent
position of Ancylanthos rubiginosus in the
chloroplast phylogeny in comparison to the
position supported by both the nuclear phylogeny and morphology can be explained by a
chloroplast capture event (e.g. Soltis et al.
1996). In chloroplast capture, hybridization
and introgression results in a cytoplasmic
transfer with little or no transfer of nuclear
DNA (Rieseberg and Soltis 1991). An additional factor that potentially could explain the
incongruence is the different ITS paralogues
known to exist for this species (Lantz and
Bremer 2004). As these paralogues do not
share the same evolutionary history, their
presence can result in erroneous phylogenies
(Sanderson and Doyle 1992, Buckler et al.
1997). However, it was concluded that the
variation did not pass the species boundary
(Lantz and Bremer 2004; see also Razafimandimbison et al. 2004 for a similar situation). It
is therefore unlikely that it is the presence of
different ITS paralogues that are causing the
incongruence.
The incongruence in the Fadogia-Rytigynia
group is more complex, especially if comparisons with morphological characters also are
made. Four taxa, i.e. Hutchinsonia barbata,
Rytigynia beniensis, R. decussata, and R. eickii
have strongly supported incongruent positions
in the ITS ( Fig. 2) and chloroplast (Fig. 3)
phylogenies. There are also strongly supported
nodes present in the individual phylogenies
which collapse when the data sets are combined. Morphological support exists for some
of the strongly supported clades, but not all. In
the Fadogia-Rytigynia group, we cannot find a
single plausible explanation for the incongruence as we could in the Vangueria group, but
we find it most likely that the incongruence has
a similar origin; hybridization and introgression. Chloroplast capture is also in this group a
possibility, and there is also an additional
H. Lantz and B. Bremer: Phylogeny of Vangueria and closely related genera
phenomenon known to exist for repetitive
DNA such as ITS. The ITS region exists in a
multitude of copies, and concerted evolution
operates on these copies to homogenize them
(e.g. Baldwin 1992). Following a hybridization
it is likely that the hybrids have a mix of the
paralogues present in the parent species, and if
the concerted evolution homogenizes the ITS
region to different paralogues in different
hybrid lineages, phylogenies based on these
paralogous ITS sequences are likely to give
misleading inferences of the organismal phylogenies. This has been shown to occur in
Gossypium (Wendel et al. 1995). Concerted
evolution can also cause DNA to be exchanged
between the paralogues, creating even more
complex reticulate relationships between the
paralogues (Hillis et al. 1991). A process which
does not include hybridization but is known to
cause incongruence is lineage sorting (Pamilo
and Nei 1988, Wendel and Doyle 1998). In this
process an ancestral polymorphism fails to
survive a speciation event, so that not all of the
descendant species share the polymorphism.
As a result of this, alleles (or paralogues in the
case of ITS) from different species may be
more closely related to each other than alleles
within the same species.
A study including also other parts of the
tribe (Lantz and Bremer 2004) using ITS and
trnT-F data did not find any incongruencies
outside of the large-flowered group. An interesting correlation between phylogeny and
morphology is that most of the genera in the
large-flowered group are known to have a
special kind of pollen presenter (type 2; Igersheim 1993). Genera in the large-flowered
group known to have this type are Ancylanthos, Fadogia, Fadogiella, Lagynias, Pachystigma, Tapiphyllum, Vangueria, and part of
Rytigynia (Igersheim 1989, Bridson 1996).
Before the flower bud opens, when the pollen
is deposited on the presenter, the stigmatic
lobes are exposed but covered by sterile apical
appendages present on the anthers (Igersheim
1993). This is in contrast to type 1 (Igersheim
1993), where the stigmatic lobes are tightly
pressed together and do not open until the
flower has opened and the style is fully
elongated. This correlation between exposed
stigmatic lobes and the presence of incongruence for these genera raises the question
whether the exposed stigmatic lobes somehow
might facilitate hybridization. We cannot see
why this would be the case unless the type 2
pollen presenter is also coupled with weak
barriers to hybridization. No studies on
hybridization in Vanguerieae have been performed, so we can only guess that this could be
the case. However, it is more likely that the
exposed stigmatic lobes could increase the
possibility for self-fertilization. The pollen sacs
of the anthers and the stigmatic surfaces are
spatially separated (Igersheim 1993), but the
pollen sacs are nevertheless close and if the
sterile apical appendages of the anthers fail to
cover the stigmatic surfaces completely, it is
possible that pollen could be deposited there in
the bud stage. Selfing has been suggested to
promote establishment of hybrid species (see
e.g. discussion in Rieseberg 1997) and this
could in part explain why we see possible cases
of hybridization in the large-flowered group
and not in other parts of Vanguerieae. At
present, this is little more than speculation,
since it is not known whether any Vanguerieae
species are self-fertilizing or whether they are
self-compatible or not.
We can thus conclude that the Vangueria
group, as circumscribed here, should be given
generic rank (as Vangueria). In the FadogiaRytigynia group, the presence of several taxa
with incongruent positions complicates any
conclusions about the phylogeny. Fadogia
(including Fadogiella) is morphologically distinct, and should not be combined with Rytigynia before the reasons behind the
incongruencies are known. We consider diagnosability to be a major desirable feature of
classification, second only to the criterion of
monophyly and would prefer to describe morphologically well-delimited genera. The phylogenies present some possible answers to why
the genera and species of the Fadogia-Rytigynia
group have proven to be difficult to delimit
using morphological criteria (Verdcourt 1987).
H. Lantz and B. Bremer: Phylogeny of Vangueria and closely related genera
Hybridization can lead to intermediate morphologies (McDade 1990) and this could
explain why these species and genera are hard
to delimit morphologically. Surprisingly enough, the possibility for hybridization in Vanguerieae has rarely been discussed. We know of
only a single report of a possible hybrid in
Vanguerieae (between Vangueria apiculata and
V. madagascariensis; Verdcourt 1981). However, the hybridization events may be old and
the species might not hybridize today.
Nevertheless, studies on self-compatibility and
hybridization in Vanguerieae would be a most
welcome addition to the complex issue of the
evolution of Vanguerieae.
Taxonomy of Vangueria
Vangueria Juss., Gen. pl.: 206. 1789. Type: V.
madagascariensis Gmelin in Syst. Nat., ed. 13,
2: 367. 1791.
Ancylanthos Desf., Mém. Mus. Hist. Nat.
4: 5. 1818, syn. nov. Type: A. rubiginosus Desf.
Pachystigma Hochst., Flora 25: 234. 1842,
syn. nov. Type: P. venosum Hochst.
Tapiphyllum Robyns, Bull. Jard. Bot. État.
11: 101. 1928, syn. nov. Type: T. cinerascens
(Hiern) Robyns.
Lagynias E. Mey. ex Robyns, Bull. Jard.
Bot. État. 11: 312. 1928, syn. nov. Type: L.
lasiantha (Sond.) Bullock.
Lagynias E. Mey. ex Robyns subgen.
Bembea Verdc. in Kew Bull. 42: 141. 1987,
syn. nov. Type: L. rufescens (E.A. Bruce)
Verdc.
Vangueria Juss. subgen. Itigi Verdc. in Kew
Bull. 42: 186. 1987, syn. nov. Type: V. praecox
Verdc.
Small trees, shrubs, or geofrutices. Unarmed, or very rarely with paired spines.
Leaves usually deciduous, paired or (for geofrutices) in whorls of three, glabrous to thickly
pubescent; domatia absent, or very rarely
present; stipules triangular or with a broad
base and a narrow apex, hairs present within.
Flowers 5(6)-merous in axillary pedunculate or
rarely fasciculate inflorescences, secondary
axes well-developed or not, with 1–30 flowers;
bracts and bracteoles inconspicuous. Calyx
glabrous to densely pubescent, limb tube short,
not equalling disk or more developed exceeding the disk; lobes variable but always well
developed, triangular, oblong, lanceolate, spatulate, or linear. Corolla usually white to green,
less often yellow or orange, externally glabrous
to densely pubescent; tube cylindrical to campanulate, with diffusely spreading hairs at
throat and retrorse straight hairs in a well
defined ring inside, usually clearly distanced
from hairs present at throat; lobes equalling
tube or shorter, rarely longer, often apiculate
or shortly appendaged. Stamens inserted at
throat; anthers ovate or oblong, apiculate,
usually shortly exserted. Ovary 3-5-locular,
each locule with a single pendulous ovule; style
shortly exserted or sometimes long exserted;
pollen presenter cylindrical or sometimes coroniform. Fruit large, above 1 cm in length,
only rarely below 1 cm, subglobose or globose,
glabrous or pubescent, calyx lobes often persistent; 3–5 pyrenes, or rarely less due to faulty
development.
A genus of over 50 species distributed in
Africa south of the Sahara with one species
occurring in Madagascar (V. madagascariensis). The centre of diversity is in East Africa
(Kenya, Tanzania) and it is rare in West
Africa.
Robyns (1928) revised all of the then
recognized species and later also described
additional species, especially in Tapiphyllum
(Robyns 1931, 1962). The East African and
Zambesian species were revised in conjunction
with the production of the Vanguerieae volumes for Flora of Tropical East Africa and
Flora Zambesiaca (Verdcourt 1981, 1987;
Verdcourt and Bridson 1991; Bridson 1996,
1998), but the other species have not recently
been revised. Several of these taxa are poorly
known, especially the ones from Angola and
Western/Central Africa, and are possibly not
worth maintaining. Unless suggested by other
authors (see V. infausta, V. macrocalyx, and
V. venosa), we do not address the delimitation
of any of the included species here, but it
should be noted that further studies are
H. Lantz and B. Bremer: Phylogeny of Vangueria and closely related genera
certainly needed. The genus is in this circumscription made more variable in comparison to
how it earlier was conceived, especially concerning inflorescence and floral morphology.
However, the genus is now easily distinguished
from its closest relatives by the following
combination of characters (also listed above):
domatia rarely present, inflorescences usually
borne at nodes from which the leaves have
fallen, bracteoles small (present on secondary
branches, usually not more than 1 mm in
length), smooth retrorse hairs in the corolla
(Lantz and Bremer 2004), and large fruits
(above 1 cm in length) with 3 to 5 locules.
Here follows a list of all currently recognized species of Vangueria in the circumscription suggested above. New combinations are
made when necessary, but infraspecific names
are given only for taxa here transferred to
Vangueria. Basionyms and most recently accepted names are listed, full synonyms are not
included.
Vangueria apiculata K. Schum. in Pflanzenw. Ost-Afrikas, C: 384. 1895.
Vangueria agrestis (Schweinf. ex Hiern)
Lantz, comb. nov. Fadogia agrestis Schweinf.
ex Hiern in Fl. trop. Afr. 3: 154. 1877.
Vangueria albosetulosa (Verdc.) Lantz,
comb. nov.
Pachystigma albosetulosum Verdc. in Kew
Bull. 42: 139. 1987.
Vangueria bicolor K. Schum. in Bot. Jahrb.
Syst. 34: 332. 1904.
Vangueria bowkeri (Robyns) Lantz, comb.
nov.
Pachystigma bowkeri Robyns in Bull. Jard.
Bot. État. 11: 128. 1928.
Vangueria burnettii (Tennant) Lantz, comb.
nov.
Tapiphyllum burnettii Tennant in Kew Bull.
19: 280, Fig. 1. 1965.
Vangueria burttii (Verdc.) Lantz, comb.
nov.
Pachystigma burttii Verdc. in Kew Bull. 36:
545, Fig. 11. 1981.
subsp. burttii.
subsp. hirtiflora (Verdc.) Lantz, comb. nov.
Pachystigma burttii subsp. hirtiflorum Verdc. in in Fl. Trop. E. Afr., Rubiaceae: 769. 1991.
Vangueria chariensis A. Chev. ex Robyns in
Bull. Jard. Bot. État. 11: 299.
Vangueria cinerascens (Welw. ex Hiern)
Lantz, comb. nov.
Ancylanthos cinerascens Welw. ex Hiern in
Fl. trop. Afr. 3: 159. 1877.
Tapiphyllum cinerascens (Welw. ex Hiern)
Robyns in Bull. Jard. Bot. État. 11: 107. 1928.
var. cinerascens.
var. inaequalis (Robyns) Lantz, comb. nov.
Tapiphyllum inaequale Robyns in Bull. Jard.
Bot. Brux. 32: 145. 1962.
Tapiphyllum cinerascens var. inaequale
(Robyns) Verdc. in Kew Bull. 42: 144. 1987.
var. laeta (Robyns) Lantz, comb. nov.
Tapiphyllum laetum Robyns in Bull. Jard.
Bot. Brux. 32: 143. 1962.
Tapiphyllum cinerascens var. laetum (Robyns) Verdc. in Kew Bull. 42: 145. 1987.
var. laevior (K. Schum.) Lantz, comb. nov.
Vangueria velutina Hiern var. laevior K.
Schum. in Bot. Jahrb. Syst. 28: 494. 1900.
Tapiphyllum cinerascens var. laevius (K.
Schum.) Verdc. in Kew Bull. 42: 144. 1987.
var. richardsii (Robyns) Lantz, comb. nov.
Tapiphyllum richardsii Robyns in Bull. Jard.
Bot. Brux. 32: 142. 1962.
Tapiphyllum cinerascens var. richardsii
(Robyns) Verdc. in Kew Bull. 42: 145. 1987.
Vangueria cistifolia (Welw., ex Hiern)
Lantz, comb. nov.
Ancylanthus cistifolius Welw. ex Hiern in
Fl. trop. Afr. 3: 159. 1877. Tapiphyllum
cistifolium (Welw.) Robyns in Bull. Jard. Bot.
État. 11: 108. 1928.
var. cistifolia.
var. latifolia (Verdc.) Lantz.
Tapiphyllum cistifolium (Welw. ex Hiern)
Robyns var. latifolium Verdc. in Fl. Zamb.
259. 1998.
Vangueria coerulea (Robyns) Lantz, comb.
nov. Pachystigma coeruleum Robyns in Bull.
Jard. Bot. État. 11: 129. 1928.
Vangueria cyanescens Robyns in Bull. Jard.
Bot. État. 11: 284. 1928.
H. Lantz and B. Bremer: Phylogeny of Vangueria and closely related genera
Vangueria discolor (De Wild.) Lantz, comb.
nov.
Fadogia discolor De Wild. in Feddes Repert. 13: 138. 1914.
Tapiphyllum discolor (De Wild.) Robyns in
Bull. Jard. Bot. État. 11: 105. 1928.
Vangueria dryadum S. Moore in J. Linn.
Soc., Bot. 40: 93. 1911.
Lagynias dryadum (S. Moore) Robyns in
Bull. Jard. Bot. État. 11: 315. 1928.
Vangueria esculenta S Moore in J. Linn.
Soc., Bot. 40: 91. 1911.
Vangueria fulva (Robyns) Lantz, comb.
nov.
Tapiphyllum fulvum Robyns in J. Bot. 69:
186. 1931.
Vangueria fuscosetulosa (Verdc.) Lantz,
comb. nov.
Rytigynia fuscosetulosa Verdc. in Fl. Trop.
E. Afr., Rubiaceae: 836. 1991.
Vangueria gillettii (Tennant) Lantz, comb.
nov.
Rytigynia gillettii Tennant in Kew Bull. 19:
279. 1965.
Pachystigma gillettii (Tennant) Verdc. in
Kew Bull. 42: 140. 1987.
Vangueria gossweileri (Robyns) Lantz,
comb. nov.
Tapiphyllum gossweileri Robyns in J. Bot.
69: 185. 1931.
Vangueria induta (Bullock) Lantz, comb.
nov.
Rytigynia induta (Bullock) Verdc. & Bridson in Kew Bull. 42: 169. 1987.
Canthium indutum Bullock in Kew Bull.
1932: 366. 1932.
Vangueria infausta Burchell in Trav. S.
Africa 2: 258. 1824.
Vangueria velutina Hook. in Bot. Mag. 57,
t. 3014. 1830, syn. nov.
Vangueria velutina Hook. has been suggested earlier (Verdcourt 1981) to be a
synonym of V. infausta Burchell, but has
not been formally listed as such. From the
excellent illustration in Hooker’s description
with detail of the calyx lobes there can be no
doubt that the specimen depicted indeed
is the same taxon as Vangueria infausta
Burchell. See also Vangueria zambesiaca
Lantz below.
Vangueria lasiantha (Sond.) Sond. in Fl.
Cap. 3: 14. 1865.
Pachystigma lasianthum Sond. in Linnaea
23: 55. 1850.
Lagynias lasiantha (Sond.) Bullock in Bull.
Misc. Inform. Kew 1931: 274. 1931.
Vangueria latifolia (Sond.) Sond. in Fl.
Cap. 3: 15. 1864.
Pachystigma latifolium Sond. in Linnaea
23: 56. 1850.
Vangueria loranthifolia K. Schum. in Pflanzenw. Ost-Afrikas, C: 385. 1895.
Pachystigma loranthifolium (K. Schum.)
Verdc. in Kew Bull. 42: 140. 1987.
subsp. loranthifolia.
subsp. salaense (Verdc.) Lantz, comb. nov.
Pachystigma lorantifolium subsp. salaense
Verdc. in Kew Bull. 42: 140. 1987.
Vangueria macrocalyx Sond. in Linnaea 23:
59. 1850.
Vangueria caffra Sim in Forest fl. Cape:
244. 1907, syn. nov.
Pachystigma caffrum (Sim) Robyns in Bull.
Jard. Bot. État. 11: 120. 1928, syn. nov.
Pachystigma macrocalyx (Sond.) Robyns in
Bull. Jard. Bot. État. 11: 130. 1928.
We agree with the view in Retief (2003)
that Pachystigma caffrum (Sim) Robyns should
be considered a synonym of Pachystigma
macrocalyx (Sond.).
Vangueria madagascariensis J.F. Gmelin in
Syst. Nat., ed. 13, 2: 367. 1791.
Vangueria micropyren (Verdc.) Lantz,
comb. nov. Pachystigma micropyren Verdc. in
Kew Bull. 42: 139. 1987.
Vangueria mollis (Robyns) Lantz, comb.
nov. Tapiphyllum molle Robyns in J. Bot. 69:
186. 1931.
Vangueria monteiroi (Oliv.) Lantz, comb.
nov.
Ancylanthos monteiroi Oliv. in Icon. pl. 8:
7. 1877.
Lagynias monteiroi (Oliv.) Bridson in Kew
Bull. 51: 351. 1996.
Vangueria obtusifolia K. Schum. in Bot.
Jahrb. Syst. 28: 493. 1900.
H. Lantz and B. Bremer: Phylogeny of Vangueria and closely related genera
Tapiphyllum obtusifolium (K. Schum.)
Robyns in Bull. Jard. Bot. État. 11: 115. 1928.
Vangueria pachyantha (Robyns) Lantz,
comb. nov.
Tapiphyllum pachyanthum Robyns in Bull.
Jard. Bot. Brux. 32: 150. 1962.
Vangueria pallidiflora (Bullock) Lantz,
comb. nov.
Lagynias pallidiflora Bullock in Kew Bull.
1931: 273. 1931.
Vangueria parvifolia Sond. in Linnaea 23:
58. 1850.
Vangueria praecox Verdc. in Kew Bull. 36:
554. 1981.
Vangueria proschii Briq. in Annuaire Conserv. Jard. Bot. Genève. 6: 7. 1902.
Vangueria psammophila (K. Schum.) Lantz,
comb. nov.
Fadogia psammophila K. Schum. in Bot.
Jahrb. Syst. 32: 147. 1902.
Tapiphyllum psammophilum (K. Schum.)
Robyns in Bull. Jard. Bot. État. 11: 105. 1928.
Vangueria pygmaea Schlecht. in J. Bot. 35:
342. 1897.
Pachystigma pygmaeum (Schlecht.) Robyns
in Bull. Jard. Bot. État. 11: 122. 1928.
Vangueria quarrei (Robyns) Lantz, comb.
nov.
Tapiphyllum quarrei Robyns in Bull. Jard.
Bot. Brux. 32: 144. 1962.
Vangueria randii S. Moore in J. Bot. 40:
252. 1902.
Vangueria rhodesiaca (Tennant) Lantz,
comb. nov.
Ancylanthos rhodesiacus Tennant in Kew
Bull. 19: 283. 1965.
Tapiphyllum rhodesiacum (Tennant) Bridson in Kew Bull. 51: 351. 1996.
Vangueria rubiginosa (Desf.) Lantz, comb.
nov.
Ancylanthos rubiginosus Desf. in Mém.
Mus. Hist. Nat. 4: 5 1818, (as rubiginosa).
Vangueria rufescens (E.A. Bruce) Lantz,
comb. nov.
Ancylanthos rufescens E.A. Bruce in Kew
Bull. 1936: 477. 1936.
Lagynias rufescens (E.A. Bruce) Verdc. in
Kew Bull. 42: 143. 1987.
subsp. rufescens.
subsp. angustiloba (Verdc.) Lantz, comb.
nov.
Lagynias rufescens (E.A. Bruce) Verdc.
subsp. angustiloba Verdc. in Kew Bull. 42:
143. 1987.
Vangueria schliebenii (Verdc.) Lantz, comb.
nov.
Tapiphyllum schliebenii Verdc. in Kew Bull.
36: 534. 1981.
Vangueria schumanniana (Robyns) Lantz,
comb. nov.
Tapiphyllum schumannianum Robyns in
Bull. Jard. Bot. État. 11: 109. 1928. Pachystigma schumannianum (Robyns) Bridson & Verdc. in Fl. Trop. E. Afr., Rubiaceae: 768. 1991.
subsp. schumanniana subsp. mucronulata
(Robyns) Lantz, comb. nov.
Pachystigma schumannianum (Robyns)
Bridson & Verdc. subsp. mucronulatum in Fl.
Trop. E. Afr., Rubiaceae: 768. 1991.
Vangueria solitariiflora (Verdc.) Lantz,
comb. nov.
Pachystigma solitariiflorum Verdc. in Kew
Bull. 36: 541, Fig. 9. 1981.
Vangueria soutpansbergensis N. Hahn in
Bothalia 27: 45. 1997.
Vangueria thamnus (Robyns) Lantz, comb.
nov.
Pachystigma thamnus Robyns in Bull. Jard.
Bot. État. 11: 121. 1928.
Vangueria triflora (Robyns) Lantz, comb.
nov.
Pachystigma triflorum Robyns in Bothalia
3: 184. 1937.
Vangueria venosa (Hochst.) Sond. in Fl.
Cap. 3: 14. 1864.
Pachystigma venosum Hochst. in Flora 25:
235. 1842.
Pachystigma cymosum Robyns in Bull.
Jard. Bot. État. 11: 127. 1928, syn. nov.
Pachystigma cymosum Robyns is listed as a
synonym of Pachystigma venosum Hochst. in
Retief (2003), and we agree with that view.
Vangueria verticillata (Robyns) Lantz,
comb. nov.
Tapiphyllum verticillatum Robyns in Bull.
Jard. Bot. Brux. 32: 141. 1962.
H. Lantz and B. Bremer: Phylogeny of Vangueria and closely related genera
Vangueria volkensii K. Schum. in Pflanzenw. Ost-Afrikas, C: 384. 1895.
Vangueria zambesiaca Lantz, nom. nov.
Vangueria velutina Hiern in Fl. trop. Afr. 3:
151. 1877, nom. illegit. Tapiphyllum velutinum
(Hiern) Robyns Bull. Jard. Bot. État. 11: 111.
1928.
Vangueria velutina Hook. (1830) precedes
Vangueria velutina Hiern (1877) and the latter
name is thus a later homonym and should not
be used. The species epithet used here is
derived from the strictly Zambesian distribution of the species (Bridson, 1998). Vangueria
velutina Hook. is above combined under V.
infausta Burchell.
The authors would like to thank K. Bremer, B.
Oxelman, M. Popp, M. Thulin, and L. Tibell for
suggestions and comments on the manuscript.
Plant material was received from the BR, K, LISC,
MO, NYBG, S, TEF, and UPS herbaria, their help
is greatly appreciated. DNA material was also
received from R. Gereau and A. Davis whose help
we gratefully acknowledge. Diane Bridson kindly
shared with us her view on the classification of
Vanguerieae, and for this we are very thankful.
Thanks also go to A. Bauer and N. Heidari for help
with sequencing. Financial support was received
from the Swedish Research Council (to B. B.),
which is gratefully acknowledged.
References
Asmussen C. B. (1999) Toward a chloroplast DNA
phylogeny of the tribe Genomeae (Palmae).
Mem. New York Bot. Gard. 83: 121–129.
Baldwin B. G. (1992) Phylogenetic utility of the
internal transcribed spacers of nuclear ribosomal
DNA in plants: an example from the Compositae. Molec. Phylogenet. Evol. 1:3–16.
Bridson D. M. (1987) The recognition and recircumscription of the African genus Multidentia
(Rubiaceae-Vanguerieae). Kew Bull. 42: 641–654.
Bridson D. M. (1996) The tropical African genus
Ancylanthos (Rubiaceae-Vanguerieae) reconsidered. Kew Bull. 51: 343–352.
Bridson D. M. (1998) Rubiaceae (Tribe Vanguerieae). In: Pope G. V. (ed.) Flora Zambesiaca. Royal Botanic Gardens, Kew, London, pp.
211–377.
Buckler IV E. S., Ippolito A., Holtsford T. P.
(1997) The evolution of ribosomal DNA: divergent paralogues and phylogenetic implications.
Genetics 145: 821–832.
Bullock A. A. (1931) Tropical African Plants: VIII.
Bull. Misc. Inform. No. 5: 270–275.
Desfontaines M. (1818) Nouveau genre de la
famille des Rubiacées: Ancylanthos. Mém. Mus.
Hist. Nat. 4: 5–7.
Downie S. R., Katz-Downie D. S., Watson M. F.
(2000) A phylogeny of the flowering plant family
Apicaeae based on chloroplast DNA rpl16 and
rpoc1 intron sequences: towards a suprageneric
classification of subfamily Apioideae. Amer. J.
Bot. 87: 273–292.
Doyle J. J., Doyle J. L. (1987) A rapid DNA
isolation procedure for small quantities of fresh
leaf tissue. Phytochem. Bull. Bot. Soc. Amer. 19:
11–15.
Hahn N. (1997) Rubiaceae: A new species of
Vangueria from the Soutpansberg. Bothalia 27:
45–48.
Hallé N. (1959) Sur les Cuviera (Rubiacées) d’Afrique intertropicale et description pour ce genre
de deux espèces et de deux variétés nouvelles.
Bull. Soc. Bot. France 7–8: 342–348.
Hillis D. M., Moritz C., Porter C. A., Baker R. J.
(1991) Evidence for biased geneconversion in
concerted evolution of ribosomal DNA. Science
251: 308–309.
Holmgren P. K., Holmgren N. H., Barnett L. C.
(1990) Index herbariorum, Part 1: The herbaria
of the world, 8th edn. New York Botanical
Garden, New York.
Hutchinson J. (1931) Robynsia. In: Hutchinson J.,
Dalziel J. M. (eds.) Flora of West Tropical
Africa. The Crown Agents for the Colonies,
London, pp. 108–109.
Igersheim A. F. (1989) Beiträge zur Klärung der
Gattungsabgrenzungsprobleme innerhalb der
Rubiaceae-Vanguerieae. Ph. D. Thesis. Universität Wien.
Igersheim A. F. (1993) Gynoecium development in
Rubiaceae-Vanguerieae, with particular reference to the ‘‘stylar-head’’-complex and secondary pollen presentation. Pl. Syst. Evol. 187: 175–
190.
Jussieu A. L. de (1789) Genera Plantarum Secundum Ordines Naturales Disposita. Paris.
Kellogg E. A., Appels R., Mason-Gamer R. J.
(1996) When genes tell different stories: the
H. Lantz and B. Bremer: Phylogeny of Vangueria and closely related genera
diploid genera of Triticeae (Gramineae). Syst.
Bot. 21: 321–347.
Lantz H., Andreasen K., Bremer B. (2002) Nuclear
rDNA ITS data used to construct the first
phylogeny of Vanguerieae (Rubiaceae). Pl. Syst.
Evol. 230: 173–187.
Lantz H., Bremer B. (2004) Phylogeny inferred
from morphology and DNA data: characterizing
well-supported groups in Vanguerieae (Rubiaceae). Bot. J. Linn. Soc. 146: 257–283.
McDade L. (1990) Hybrids and phylogenetic systematics I. Patterns of character expression in
hybrids and their implications for cladistic analysis. Evolution 44: 1685–1700.
Pamilo P., Nei M. (1988) Relationships between
gene trees and species trees. Mol. Biol. Evol. 5:
568–583.
Razafimandimbison S., Kellogg E., Bremer B.
(2004) Recent origin and phylogenetic utility of
divergent ITS putative pseudogenes: a case study
from Naucleeae (Rubiaceae). Syst. Biol. 53: 177–
192.
Retief E. (2003) Rubiaceae. In: Germishuizen G.,
Meyer N. L. (eds.) Plants of southern Africa: an
annotated checklist. Strelitzia 14: 825–841. National Botanical Institute, Pretoria.
Rieseberg L. H., Soltis D. E. (1991) Phylogenetic
consequences of cytoplasmic gene flow in plants.
Evol. Trends Pl. 5: 65–84.
Rieseberg L. H. (1997) Hybrid origins of plant
species. Annual Rev. Ecol. Syst. 28: 359–389.
Robbrecht E. (1988) Tropical woody Rubiaceae.
Opera Bot. Belg. 1: 1–271.
Robyns W. (1928) Tentamen Monographiae Vanguerieae Generumque Affinium. Bull. Jard. Bot.
État. 11: 1–359.
Robyns W. (1931) Vanguerieae Gossweilerianae.
J. Bot. 69: 189–190.
Robyns W. (1962) Contribution a l’étude du genre
Tapiphyllum Robyns. Bull. Jard. Bot. État. 32:
133–153.
Sanderson M. J., Doyle J. J. (1992) Reconstruction
of organismal and gene phylogenies from data
on multigene families: concerted evolution,
homoplasy, and confidence. Syst. Biol. 41: 4–17.
Simmons M. P., Ochoterena H. (2000) Gaps as
characters in sequence-based phylogenetic analyses. Syst. Biol. 49: 369–381.
Small R. L., Ryburn J. A., Cronn R. C.,
Seelanan T., Wendel J. F. (1998) The tortoise
and the hare: choosing between noncoding
plastome and nuclear ADH sequences for
phylogeny reconstruction in a recently
diverged plant group. Amer. J. Bot. 85:
1301–1315.
Soltis D. E., Johnson L. A., Looney C. (1996)
Discordance between ITS and chloroplast topologies in the Boykinia group (Saxifragaceae).
Syst. Bot. 21: 169–185.
Swofford D. L. (2002) PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods).
Version 4. Sinauer Associates, Sunderland, Massachusetts.
Verdcourt B. (1958) Remarks on the classification
of the Rubiaceae. Bull. Jard. Bot. État. 28: 209–
281.
Verdcourt B. (1981) Notes on African Rubiaceae.
Kew Bull. 36: 493–557.
Verdcourt B. (1987) Notes on African RubiaceaeVanguerieae. Kew Bull. 42: 123–199.
Verdcourt B., Bridson D. M. (1991) Rubiaceae
(Part 3). In: Polhill R. M. (ed.) Flora of Tropical
East Africa. A.A. Balkema, Rotterdam/Brookfield, pp. 749–956.
Wendel J. F., Schnabel A., Seelanan T. (1995)
Bidirectional interlocus concerted evolution following allopolyploid speciation in cotton (Gossypium). Proc. Natl. Acad. Sci. USA 92: 280–
284.
Wendel J. F., Doyle J. J. (1998) Phylogenetic
incongruence: window into genome history and
molecular evolution. In: Soltis P. S., Soltis D. E.,
Doyle J. J. (eds.) Molecular systematics of
plants, 2nd edn. Chapman and Hall, New York,
pp. 265–296.
Addresses of the authors: Henrik Lantz (email: henrik.lantz@ebc.uu.se), Department of
Systematic Botany, Evolutionary Biology Centre,
Uppsala University, Norbyvägen 18D, 75236,
Uppsala, Sweden.
Birgitta Bremer (e-mail:
birgitta.bremer@ bergianska.se) The Bergius
Foundation at the Royal Swedish Academy of
Sciences, P. O. Box 50017, 10405 Stockholm,
Sweden.