TAXON 60 (4) • August 2011: 941–952
Razafimandimbison & al. • A basal grade in the Vanguerieae alliance
M O L E C U L A R PH Y LO G E N E T I C S A N D B I O G E O G R A PH Y
Molecular support for a basal grade of morphologically distinct,
monotypic genera in the species-rich Vanguerieae alliance (Rubiaceae,
Ixoroideae): Its systematic and conservation implications
Sylvain G. Razafimandimbison,1 Kent Kainulainen,1,2 Khoon M. Wong, 3 Katy Beaver4 & Birgitta Bremer1
1 Bergius Foundation, Royal Swedish Academy of Sciences and Botany Department, Stockholm University, 10691 Stockholm, Sweden
2 Department of Botany, Stockholm University, 10691, Stockholm, Sweden
3 Singapore Botanic Gardens, 1 Cluny Road, Singapore 259569
4 Plant Conservation Action Group, P.O. Box 392, Victoria, Mahé, Seychelles
Author for correspondence: Sylvain G. Razafimandimbison, sylvain.razafimandimbison@bergianska.se
Abstract Many monotypic genera with unique apomorphic characters have been difficult to place in the morphology-based
classifications of the coffee family (Rubiaceae). We rigorously assessed the subfamilial phylogenetic position and generic status
of three enigmatic genera, the Seychellois Glionnetia, the Southeast Asian Jackiopsis, and the Chinese Trailliaedoxa within
Rubiaceae, using sequence data of four plastid markers (ndhF, rbcL, rps16, trnTF). The present study provides molecular
phylogenetic support for positions of these genera in the subfamily Ixoroideae, and reveals the presence of a basal grade of
morphologically distinct, monotypic genera (Crossopteryx, Jackiopsis, Scyphiphora, Trailliaedoxa, and Glionnetia, respectively)
in the species-rich Vanguerieae alliance. These five genera may represent sole representatives of their respective lineages and
therefore may carry unique genetic information. Their conservation status was assessed, applying the criteria set in IUCN Red
List Categories. We consider Glionnetia and Jackiopsis Endangered. Scyphiphora is recognized as Near Threatened despite
its extensive range and Crossopteryx as Least Concern. Trailliaedoxa is poorly known (Data Deficient). Finally, the generic
status of Glionnetia, Jackiopsis, and Trailliaedoxa and the monogeneric tribe Jackieae as defined by Ridsdale are supported.
Keywords conservation; Crossopteryx; Glionnetia; Jackiopsis; molecular systematics; Scyphiphora; Trailliaedoxa
INTRODUCTION
Rubiaceae (or the coffee family) are one of the most
species-rich flowering plant families with a particularly high
number of monotypic genera, which represent 34.5% of the
genera (Davis & al., 2009). The majority of these genera have
been studied in previous molecular phylogenetic investigations of the family, and their generic status, systematic positions, and phylogenetic relationships have been assessed.
Some monotypic genera have been synonymized, as they
were shown to be part of much larger and well-defined genera (e.g., Aphaenandra Miq. now included in Mussaenda L.,
Alejandro & al., 2005; Hymenocnemis Hook. f. now included
in Gaertnera Lam., Malcomber & Davis, 2005; Litosanthes
Blume now included in Lasianthus Jack, Xiao & Xhu, 2008;
Rhopalobrachium Schltr. & K. Krause now included in Cyclo
phyllum Hook. f., Mouly & al., 2007; Schizostigma Arn. ex
Meisn. now included in Sabicea Aubl., Khan & al., 2008;
Neoleroya Cavaco and Scyphochlamys Balf. f. now included
in Pyrostria Comm. ex A. Juss., Razafimandimbison & al.,
2009). In contrast, the generic status of some monotypic genera (e.g., Strumpfia Jacq., Bremer & al., 1995; Crossopteryx
(Afzel. ex G. Don) Benth., Razafimandimbison & Bremer,
2001; Burttdavya Hoyle, Razafimandimbison & Bremer,
2002; Landiopsis Capuron ex Bosser, Alejandro & al., 2005;
Dunnia Tutcher, Rydin & al., 2008) has been retained, because
they are not nested within well-defined genera. Furthermore,
they have at least one autapomorphic character allowing them
to be easily identified (Backlund & Bremer, 1998). The systematic placement of a few rubiaceous monotypic genera with
particularly unique morphology remains either unknown or
controversial due to the lack of sequenceable material. The
present study focuses on the enigmatic genera Trailliaedoxa
W.W. Sm. & Forrest, Jackiopsis Ridsdale, and Glionnetia
Tirvengadum (Fig. 1A–J).
Jackiopsis was originally described by Wallich (in Roxburgh, 1824) as Jackia Wall., but this latter name was already used for another genus Jackia Blume in the family
Polygalaceae. As a result, Ridsdale (1979) proposed the name
Jackiopsis for Wallich’s intended genus. When establishing
Jackia ornata Wall. (= Jackiopsis ornata (Wall.) Ridsdale)
Wallich (in Roxburgh, 1824) wrote a very detailed description based on individual plants in flower and immature fruit
that he had discovered “on several of the small islands in the
immediate vicinity of Singapore”. Jackiopsis is a large tree
up to 35 m tall with spreading buttresses. The stipules are
large, persistent, and connate into a sheath with 8 to 15 stiff,
filiform lobes (Fig. 1D). Its inflorescences are axillary, large,
pendulous, and paniculate with scorpioid lateral branches.
The peduncles are typically flattened, articulated, and are
composed of a primary peduncle unit, a secondary node, a
secondary peduncle unit, a tertiary node, and a tertiary peduncle unit. Each secondary node bears a sheathed bract, and
a pair of reduced leaves; each tertiary node bears a sheathed
941
Razafimandimbison & al. • A basal grade in the Vanguerieae alliance
bract and is typically terminated by up to eight scorpioid
inflorescences in umbel-like arrangement. Corolla lobe aestivation is valvate. Ovaries are bilocular with 2–5 ovules in
each locule; the ovules are basally attached on ascending,
stalked placentae. Fruits are dry, dehiscent, winged nutlets
with persistent, reticulate, and accrescent calyx lobes (pterophylls) (Fig. 1E), commonly with only one seed per locule, as
the remaining ovules are aborted (Wallich in Roxburgh, 1824;
Ridsdale, 1979).
Korthals (1851) was the first to classify Jackiopsis (as
Jackia) at tribal level. He placed the genus in his new tribe
TAXON 60 (4) • August 2011: 941–952
Jackieae (as Jackiae) along with four other genera, Tricaly
sia A. Rich. and Diplospora DC. (now in tribe Coffeeae),
Hypobathrum Blume (now in Octotropideae), and Scyphiphora
Gaertn., all presently placed in the subfamily Ixoroideae.
Hooker (1873) erroneously considered the corolla aestivation
of Jackiopsis to be contorted and its fruits to be drupes with 5
to 7 pyrenes, and accordingly placed the genus in Retiniphylleae, now in subfamily Ixoroideae. Baillon (1878) postulated
a close affinity between Jackiopsis, Cruckshanksia Hook.
& Arn., and Carphalea Juss. based on similarities in ovary
structure, placentation, and fruits with reticulate pterophylls.
Fig. 1. Illustrations showing the morphological synapomorphies or characteristics of Trailliaedoxa, Jackiopsis, and Glionnetia. A–C, Trailliae
doxa gracilis: A, leafy twig; from Boufford & al. 35041 (MO); B, immature fruit; from Yü 1348 (HUH); C, flower showing partly exserted anthers
and a fully exserted stigma; from Forrest 12638 (S). D–F, Jackiopsis ornata: D, large, densely pubescent stipule with filiform lobes; from Kalat
& al. s.n. 1993-05-11 (L); E, dry, indehiscent fruit with three unequal lobes; from Van Balooy 6109 (MO); F, densely pubescent flower with three
calyx lobes and a very long style; from Rahmat Si Toroes 3424 (S). G–J, Glionnetia sericea: G, habit showing a very long, convolute terminal
vegetative bud (young stipule); from Beaver 03 (S); H, long, convolute stipule; from Beaver 03 (S); I, mature capsular fruit; from Beaver 17 (S);
J, flower showing partly exserted anthers; from Beaver 17 (S). Scale bars: thin, 2 mm; medium, 5 mm; thick, 20 mm.
942
TAXON 60 (4) • August 2011: 941–952
The latter two genera are currently placed in the tribes Coussareeae and Knoxieae, respectively, in the subfamily Rubioideae. Schumann (1891) associated Jackiopsis with Rubioideae,
viz. Oldenlandieae. More recently, Ridsdale (1979) narrowly
recircumscribed Jackieae to include only the genus Jackiopsis
and tentatively placed the tribe in the subfamily Cinchonoideae. Finally, the recent discovery of intra-ovarian trichomes in Jackiopsis (Puff & Igersheim, 1994) and in some
Malagasy species of Tricalysia (Ranarivelo-Randriamboavonjy & al., 2007) could be taken as an indication of a close
relationship between the two genera and would imply placing
the former in the tribe Coffeeae of Ixoroideae.
Trailliaedoxa is an ericoid, erect subshrub (up to 60 cm
tall), with a broom-like branching and small, tough leaves
(Robbrecht, 1988). According to the protologue (Smith, 1917),
the genus grows in the rocky habitats and thickets on dry
mountain slopes of Sichuan, China, between 1450 and 3000 m
elevation. Trailliaedoxa is very distinct from other Rubiaceae
in its ericoid habit, pubescent styles, and schizocarpous fruits.
The genus is presently unclassified at tribal level in Rubiaceae (Robbrecht, 1988). Smith (1917) thought that the floral
structure of the genus is similar to that of Alberteae, now in
Ixoroideae. On the other hand, its ericoid habit is also comparable to that of Spermadictyon Roxb. of the tribe Paederieae
in the subfamily Rubioideae (Smith, 1917). Robbrecht (1988)
tentatively placed Trailliaedoxa in the subfamily Antirheoideae, which was shown to be highly polyphyletic (e.g., Bremer
& al., 1995).
Finally, the genus Glionnetia was originally described by
Tirvengadum (1984) to accommodate the Seychellois Randia
sericea (Baker) Hemsl. (Hemsley, 1916: 18) that he excluded
from the Neotropical genus Randia L. This monotypic genus
is restricted to Mahé and Silhouette Islands of the Seychelles
Archipelago; it is distinct by its large, long, intrapetiolar, and
convolute stipules and can additionally be characterized by a
combination of the following features: glabrous, coriaceous
leaves clustered at the apex of the branches, corollas 6–7 cm
long, left-contorted aestivation, and capsular fruits with loculicidal dehiscence (Fig. 1G–J). Tirvengadum (1984) originally
classified Glionnetia in Rondeletieae of the subfamily Cinchonoideae. Robbrecht (1988), and more recently Rova & al.
(2009) and Manns & Bremer (2010), tentatively followed this
classification. None of the discussed hypotheses regarding
systematic positions within Rubiaceae have been tested with
molecular data.
We rigorously investigated the phylogenetic positions of
Glionnetia, Jackiopsis, and Trailliaedoxa in Rubiaceae and
assessed their generic status, using sequence data from four
plastid markers (ndhF, rbcL, rps16 intron, trnTF). We found
that these genera belong in the subfamily Ixoroideae, and that
Crossopteryx, Jackiopsis, Scyphiphora, Trailliaedoxa, and
Glionnetia, respectively, form a paraphyletic assemblage at
the base of the species-rich Vanguerieae alliance. These results
allowed us to hypothesize that these monotypic genera may
represent sole representatives of their respective lineages. We
discuss the systematic and conservation implications of these
findings.
Razafimandimbison & al. • A basal grade in the Vanguerieae alliance
MATERIALS AND METHODS
Taxon sampling and laboratory work. — We extracted
silica-gel leaf samples from three individuals of Jackiopsis
ornata (from the Malay Peninsula), three individuals of Glion
netia sericea (from the Island of Mahé in the Seychelles Archipelago), and two individuals of Trailliaedoxa gracilis (from
Yunnan, China), following the protocol outlined in Razafimandimbison & al. (2008). The extracted DNA was amplified
and sequenced for four chloroplast regions (ndhF, rbcL, rps16
intron, trnTF), using the primers of Razafimandimbison & al.
(2008) and Rydin & al. (2008).
Phylogenetic analyses. — Sequences were preliminary
aligned using the Clustal W (default settings; Thompson & al.,
1994), as implemented in BioEdit v.7.0.9 (Hall, 1999), and subsequently edited manually. We initially performed maximum
parsimony (MP) and Bayesian analyses of 120 rbcL sequences
of Rubiaceae (including all major lineages in the three subfamilies of Rubiaceae and the tribes Luculieae and Coptosapelteae,
which do not belong in any of the three subfamilies) in order to
pinpoint the subfamilial position(s) of the three genera within
the family. Eight taxa from the other families of the order Gentianales (Apocynaceae, Gentianaceae, Gelsemiaceae, Loganiaceae) were utilized as outgroups following Bremer & Eriksson
(2009). Bayesian analysis of the rbcL dataset was performed
using the GTR + G + I model. We refer to these MP and Bayesian
rbcL analyses hereafter as the “Family-Wide-rbcL” analyses.
The results of the Family-Wide-rbcL analyses allowed us to
narrow down our sampling to include only the three targeted
genera and their more closely related groups and select the outgroup taxa from within Rubiaceae (Cinchona L. and Cubanola
Aiello [subfamily Cinchonoideae], Morinda L. [subfamily Rubioideae], and Luculia Sweet [Luculieae]). MP and Bayesian
analyses of 71 taxa based on combined sequence data from the
chloroplast markers ndhF, rbcL, rps16 intron, and trnTF were
subsequently performed, of which 67 species represented all
tribes currently recognized in Ixoroideae (with the exception of
Henriquezieae) (see Appendix). We refer to these analyses hereafter as the “Ixoroideae-Four-Locus” analyses. We hoped that
we could better resolve the position of these genera within subfamily Ixoroideae, by combining the two more rapidly evolving
non-coding regions (rps16 intron, trnTF) and the two coding
regions (ndhF, rbcL) in a single data matrix.
Separate and combined MP analyses of the ndhF, rbcL,
rps16, and trnTF datasets of the 71 taxa were conducted using
the program PAUP* v.4.0B10 (Swofford, 2002). MP analyses
consisted of a heuristic search with the TBR branch swapping
algorithm, Multrees on, 1000 random sequence addition replicates and a maximum of 10 trees saved per replicate. Clade
bootstrap support (BS) was estimated using the same settings
and three random sequence additions per replicate.
The combined dataset was also analyzed using Bayesian
inference (BI), using the program MrBayes v.3.1.2 (Huelsenbeck & Ronquist, 2001; Ronquist & Huelsenbeck, 2003). The
combined data were partitioned in a protein-coding (rbcL,
ndhF) partition and a non-coding (rps16 intron, trnTF) partition; these were unlinked and analyzed under the GTR + G + I
943
Razafimandimbison & al. • A basal grade in the Vanguerieae alliance
and GTR + G models, respectively, which were suggested as
best-fit to the data under the corrected Akaike information
criterion (AICc). The Bayesian rbcL analysis of the 120 taxa
and combined Bayesian analyses of the 71 taxa each comprised
two runs of four chains, which were monitored for 15 × 106 generations, with every 1000th generation being sampled, and the
temperature coefficient of the chain-heating scheme set to 0.15.
Stationarity and convergence of runs, as well as the correlation
of split frequencies between the runs were checked using the
TAXON 60 (4) • August 2011: 941–952
program AWTY (Nylander & al., 2008). Trees sampled before
the posterior probability (PP) of splits stabilized, were excluded
from consensus as a burn-in phase. The effective sample size
(ESS) of parameters was checked using the program Tracer
v.1.4.1 (Rambaut & Drummond, 2007).
Finally, we assessed the conservation status of Crossop
teryx, Glionnetia, Jackiopsis, Scyphiphora, and Trailliaedoxa,
applying the criteria set in World Conservation Union (IUCN)
Red List Categories (Version 3.1; IUCN, 2001).
Alstonia
Kopsia
Gelsemium
Mostuea
Strychnos
Spigelia
Gentiana
Anthocleista
1
1
1
1
1
100
0.53
outgroups
Luculieae (3 spp.)
1
93
Coptosapelteae (5 spp.)
0.99
Subfamily Rubioideae
(63 spp.)
1
99
1
100
Rubiaceae
1
96
Subfamily Cinchonoideae
(11 spp.)
0.78
1
99
1
1
93
1
82
Subfamily Ixoroideae
(30 spp.)
0.77
0.91
1
0.51
1
97
0.72
0.81
0.63
Fig. 2. A Bayesian majority rule consensus tree of the coffee family from the
rbcL sequence data of 120 taxa. Posterior probabilities and bootstrap support
percentages are above and below the
nodes, respectively. The outgroup taxa
are delimited by a vertical line. Numbers in parentheses correspond to the
number of species sequenced.
944
0.87
1
86
1
100
0.53
0.72
1
71
1
0.96
0.86
61
55
0.93
1
0.84
67
Mussaenda erythrophylla
Sipanea biflora
Sipanea hispida
Virectaria major
Sabicea diversifolia
Sabicea aspera
Ferdinandusa speciosa
Calycophyllum candidissimum
Emmenopterys henryi
Condaminea corymbosa
Pyrostria hystrix
Vangueria madagascariensis
Retiniphyllum pilosum
Ixora coccinea
Glionnetia sericea 1
Glionnetia sericea 2
Glionnetia sericea 3
Crossopteryx febrifuga
Trailliaedoxa gracilis 1
Trailliaedoxa gracilis 2
Alberta magna
Jackiopsis ornata
Razafimandimbisonia sambiranensis
Aidia micrantha
Bertiera guianensis
Tricalysia cryptocalyx
Coffea arabica
Diplospora polysperma
Cremaspora triflora
Fernelia buxifolia
Feretia aeruginescens
Kraussia floribunda
Pouchetia gilletii
TAXON 60 (4) • August 2011: 941–952
Razafimandimbison & al. • A basal grade in the Vanguerieae alliance
RESULTS
Separate analyses. — The Family-Wide-rbcL analyses
based on the 120 rbcL sequence data placed all sampled Glion
netia, Jackiopsis, and Trailliaedoxa in the subfamily Ixoroideae
(PP = 1.00; BS = 82%). The monophyly of Ixoroideae and its
sister-group relationship with the subfamily Cinchonoideae is
consistent with other published Rubiaceae studies (e.g., Robbrecht & Manen, 2006; Bremer & Eriksson, 2009; Rydin & al.,
2009). Glionnetia and Trailliaedoxa formed a poorly supported
clade with Crossopteryx, while Jackiopsis was left unresolved
in the poorly supported Coffeeae alliance (PP = 0.53) (Fig. 2).
A summary of the tree data and statistics from the analyses
is given in Table 1. In the separate Ixoroideae analyses of the
71-taxa datasets, the incongruent nodes between the separate
cpDNA markers generally received weak support (trees not
shown), with the exception of a node inferred from the trnT
F data: a clade consisting of Condamineeae, Sipaneeae and
Posoquerieae, as sister to the rest of the Ixoroideae (BS = 81%;
PP = 0.96) excluding Mussaendeae and Sabiceeae (inferred as
sister groups in a basal clade).
Combined analyses. — The phylogenetic hypotheses inferred from the MP and BI analyses of the Ixoroideae-FourLocus datasets were in general agreement, with the exception
of the position of Tocoyena pittieri, resolved as sister to Gar
denia hansemanii in the former (BS = 53%), and as sister to
Aulacocalyx jasminiflora in the latter (PP = 0.89).
The uncorrected potential scale reduction factor (PSRF;
Gelman & Rubin, 1992) of the summarized parameters approached 1.0, and the split frequencies between the runs were
highly correlated, indicating that the runs had converged. The
ESS of all model parameters were > 200, as recommended by
Drummond & al. (2007) for adequate representation of the
posterior probability. The 50% majority-rule consensus tree
inferred from the BI analysis of the Ixoroideae-Four-Locus
data is shown in Fig. 3.
The sampled specimens of Glionnetia, Jackiopsis, and
Trailliaedoxa formed, respectively, highly supported clades (PP
= 1.00; BS = 100) and were all nested in the highly supported
Vanguerieae alliance (Fig. 3). Within this alliance the monotypic
African genus Crossopteryx was the first to branch off, followed
by Jackiopsis, Scyphiphora, Trailliaedoxa, and Glionnetia, respectively. Glionnetia was in turn resolved with poor support as
sister to a poorly supported large clade containing Vanguerieae,
Greeneeae, Aleisanthieae, and Ixoreae. Within this latter clade
Aleisanthieae and Ixoreae formed a sister group, which in
turn was sister to Greeneeae. The (Greeneeae(AleisanthieaeIxoreae)) clade was sister to Vanguerieae.
DISCUSSION
Subfamilial position of Glionnetia, Jackiopsis and Trailliaedoxa within Rubiaceae: New circumscription of the
Vanguerieae alliance. — The present study is the first molecular phylogenetic investigation of the Seychellois genus Glion
netia, the Southeast Asian Jackiopsis, and the Chinese genus
Trailliaedoxa. The results of the Family-Wide-rbcL analysis
(Fig. 2) support the placement of these monotypic genera in
the subfamily Ixoroideae sensu Bremer & Eriksson (2009).
The phylogenetic hypothesis from the Ixoroideae-Four-Locus
analyses (Fig. 3) reveals that the Vanguerieae alliance of the
subfamily Ixoroideae contains the following major lineages: the
African Crossopteryx (Crossopterygeae), Jackiopsis (Jackieae
sensu Ridsdale), the mangrove genus Scyphiphora, Trailliae
doxa, Glionnetia, all currently unplaced at tribal level, and the
tribes Vanguerieae, Aleisanthieae, Greeneeae, and Ixoreae.
This alliance is species-rich and morphologically diverse, and
contains over 1100 species of shrubs and small trees; it does not
seem to have any obvious synapomorphic character, however
the majority of its members (i.e., those of the species-rich tribes
Ixoreae and Vanguerieae) have flowers showing secondary
pollen presentation, drupaceous fruits, and one-seeded carpels. Ixoreae is pantropical, while the remaining lineages are
paleotropical. An overview of the morphological and ecological characteristics of these major lineages of the Vanguerieae
alliance is shown in Table 2.
Tribal positions and generic status of Glionnetia, Jackiopsis and Trailliaedoxa. — The morphologically unique genera
Glionnetia, Jackiopsis, and Trailliaedoxa represent a paraphyletic basal assemblage within the Vanguerieae alliance (Fig. 3).
Assessment and recognition of these monotypic genera and
their tribal positions are discussed on the basis of a combination
of the following criteria (Backlund & Bremer, 1998; Razafimandimbison & Bremer, 2002): (1) if they are not nested within
other well-defined genera; and (2) if they have at least one
Table 1. Characteristics of the markers/datasets used, including statistics of alignments, analyses, as well as parameter estimates and evolutionary
models suggested by MrModeltest 2.2 (Nylander, 2004).
ndhF
rbcL
rps16
trnTF
Combined
Coding
Noncoding
Number of taxa
40
53
65
66
66
56
66
Included characters
2159
1403
1073
2441
7076
3562
3514
Variable characters
677
291
382
886
2236
968
1268
Parsimony-informative characters 353
158
227
465
1203
511
692
% informative characters
16.35
11.26
21.16
19.05
17.00
14.35
19.69
Consistency index (CI)
0.70
0.54
0.68
0.75
0.68
0.64
0.72
Retention index (RI)
0.73
0.64
0.82
0.82
0.77
0.69
0.82
945
Razafimandimbison & al. • A basal grade in the Vanguerieae alliance
TAXON 60 (4) • August 2011: 941–952
Luculia gratissima - LUC
Morinda citrifolia - MOR
1.00
100
1.00
92
1.00
94
1.00
100 0.90
66
1.00
94
1.00
100
0.80
65
0.98
87
Subfamily Ixoroideae
Cinchona pubescens - CIN
Cubanola domigensis - CHI
Posoqueria latifolia - POS
Sipanea biflora - SIP
Sipanea hispida - SIP
1.00
100
1.00
Sipanea pratensis - SIP
100
Emmenopterys henryi - CON
Calycophyllum candidissimum - CON
Pentagonia macrophylla - CON
Rustia thibaudioides - CON
Mussaenda arcuata - MUS
1.00
Pseudomussaenda flava - MUS
100
Sabicea villosa - SAB
1.00
Tamridea capsulifera - SAB
100
Steenisia pleurocarpa
1.00
68
Retiniphyllum concolor - RET
Retiniphyllum maguirei - RET
Retiniphyllum pilosum - RET
0.99
91
Retiniphyllum schomburgki - RET
Airosperma vanuense
Boholia nematostylis
1.00
100
1.00
100
1.00
100
Augusta rivalis
Wendlandia tinctoria
Alberta magna - ALB
1.00
1.00
Nematostylis anthophylla - ALB
100
100
Razafimandimbisonia minor - ALB
1.00 1.00
1.00
Razafimandimbisonia sambiranensis - ALB
99 93
100
Bertiera guianensis - BER
0.98
Diplospora polysperma - COF
1.00
79
100
Coffea arabica - COF
1.00
87
Tricalysia cryptocalyx - COF
0.87
52
1.00
Cremaspora triflora subsp. confluens - CRE
100
1.00
1.00
Hypobathrum racemosum - OCT
100
100
Aulacocalyx jasminiflora - GAR
0.99
83
Tocoyena pittieri - GAR
1.00
Gardenia hansemanii - GAR
0.89 75
Pavetta abyssinca - PAV
0.69
Coffeeae alliance
1.00
Tennantia sennii - PAV
100
Crossopteryx febrifuga 1 - CRO
1.00
Crossopteryx febrifuga 2 - CRO
100
Jackiopsis ornata 1 - JAC
Jackiopsis ornata 2 - JAC
1.00
1.00
100
90
Jackiopsis ornata 3 - JAC
Scyphiphora hydrophylacea 1
1.00
1.00
Scyphiphora hydrophylacea 2
100
93
Trailliaedoxa gracilis 1
1.00
Trailliaedoxa gracilis 2
100
1.00
67
Glionnetia sericea 1
Glionnetia sericea 2
1.00
100
Glionnetia sericea 3
0.98
59
Vanguerieae alliance
Canthium tetraphyllum - VAN
1.00
Vangueria madagascariensis - VAN
100
1.00
Keetia guenzii - VAN
0.55
100
Cyclophyllum deplanchei - VAN
1.00
100
Peponidium comorense - VAN
0.99
75
Pyrostria hystrix - VAN
0.98
65
0.53
Greenea sp. 1 - GRE
Greenea oblonga - GRE
1.00
100
Greenea corymbosa - GRE
1.00
86
Greenea sp. 2 - GRE
0.86
70
1.00
Aleisanthia rupestris - ALE
100
1.00
Aleisanthiopsis distantiflora - ALE
99
Ixora coccinea - IXO
1.00
Ixora margaretae - IXO
98
1.00
1.00
90
Ixora moorensis - IXO
99
1.00
Ixora trilocularis - IXO
100
Ixora brachypoda - IXO
0.93
67
Ixora guianensis - IXO
1.00
991.00
Ixora hookeri - IXO
1.00
-
0.01
outgroup taxa
1.00
100
93
Fig. 3. Bayesian majority-rule consensus tree of the subfamily Ixoroideae from the combined ndhF/rbcL/rps16/trnLF data. Below branches are
posterior probabilities and bootstrap support percentages (bold). Bootstrap support < 50% is indicated by a dash. The outgroup taxa are delimited by a vertical line. ALB, Alberteae; ALE, Aleisanthieae; CHI, Chiococceae; CIN, Cinchoneae; COF, Coffeeae; CON, Condamineeae; CRE,
Cremasporeae; CRO, Crossopterygeae; GAR, Gardenieae; GRE, Greeneeae; IXO, Ixoreae; JAC, Jackieae; LUC, Luculieae; MUS, Mussaendeae;
OCT, Octotropideae; PAV, Pavetteae; POS, Posoquerieae; RET, Retiniphylleae; SAB, Sabiceeae; SIP, Sipaneeae; VAN, Vanguerieae. The positions of the subfamily Ixoroideae and the Coffeeae and Vanguerieae alliances are indicated. The sampled specimens of Glionnetia, Jackiopsis,
and Trailliaedoxa are in boldface.
946
TAXON 60 (4) • August 2011: 941–952
Razafimandimbison & al. • A basal grade in the Vanguerieae alliance
autapomorphic character or a combination of plesiomorphic
characters, allowing them to be recognized easily.
Glionnetia, Jackiopsis or Trailliaedoxa are not nested
within the five currently recognized tribes (Aleisanthieae,
Crossopterygeae, Greeneeae, Ixoreae, Vanguerieae) of the
Vanguerieae alliance. Like the monogeneric tribe Crossopterygeae, each of these three genera can also be placed in their
own tribes, as they have distinct morphological features that
warrant tribal recognition.
The large, persistent, and sheathed stipules with 8–15 filiform lobes and the large (Fig. 1D), paniculate inflorescences
with scorpioid lateral branches are unique for Jackiopsis in the
Vanguerieae alliance and may represent potential apomorphies
for the genus. A combination of valvate aestivation and dry,
indehiscent fruits with pterophylls (Fig. 1E) can additionally be
used to characterize Jackiopsis. Within the Vanguerieae alliance the members of Vanguerieae also have valvate aestivation
but their fruits are drupes (Table 2). Dry fruits with pterophylls
are also found in some other rubiaceous genera (e.g., Steenisia
Bahk. f., Bremer, 1984; Cosmocalyx Standl., Delprete, 1998;
Alberta E. Mey, Kainulainen & al., 2009). Furthermore, the
Ixoroideae-Four-Locus analyses (Fig. 3) support the monogeneric tribe Jackieae as circumscribed by Ridsdale (1979). Consequently, an older view of Jackieae (Korthals, 1851), as containing Diplospora, Hypobathrum, Jackiopsis, Scyphiphora, and
Tricalysia, is highly polyphyletic. The phylogenetic positions
of Diplospora and Tricalysia in Coffeeae and Hypobathrum
in Octotropideae have been shown by many independent molecular phylogenetic studies (e.g., Andreasen & Bremer, 2000;
Robbrecht & Manen, 2006). The fourth genus Scyphiphora has
been shown to be closely related to Aleisanthieae, Greeneeae,
Ixoreae, and Vanguerieae of the Vanguerieae alliance (e.g.,
Robbrecht & Manen, 2006; Bremer & Eriksson, 2009; Cortés-B. & al., 2009; Mouly & al., 2009). A close relationship
of Jackiopsis with the former Hedyotideae (now Knoxieae in
subfamily Rubioideae) as put forward by Baillon (1878) and
Schumann (1891) is not supported by this study (Fig. 2).
The Ixoroideae-Four-Locus analyses (Fig. 3) strongly support the position of Glionnetia in the Vanguerieae alliance,
although its relationship to other taxa within the alliance is
poorly resolved. This finding is inconsistent with Tirvengadum
(1984), who tentatively placed the genus in Rondeletieae of the
subfamily Cinchonoideae. Within Rondeletieae, Tirvengadum
(1984) postulated a close relationship to the genus Lindenia
Benth. (now Augusta Pohl), a genus that has recently been
demonstrated to have a close affinity with the genus Wend
landia Bartl. ex DC. (Rova & al., 2002) of the Coffeeae alliance of Ixoroideae (Fig. 3). The long, intrapetiolar, and convolute stipules are unique for Glionnetia within the Vanguerieae
alliance, and may represent a potential apomorphy for the
Table 2. Morphological characteristics and other important information of the major lineages of the Vanguerieae alliance.
Crossopterygeae Jackieae
Scyphi
phora
Traillaiae
doxa
Vanguerieae
Aleisanthieae
Greeneeae
Ixoreae
Distribution
Tropical
Africa
SE Asia
SE Asia
and Madagascar
Yunnan,
Sichuan,
China
Seychelles
Paleotropics
SE Asia
SE Asia
Pantropical
Habit
Shrubs
to small
trees
Tall to
emergent
trees
Shrubs
Subshrubs
(up to
60 cm tall)
Small
trees
Small trees, Shrubs
shrubs or
herbs
Shrubs
or small
trees
Shrubs
Inflorescence position
Terminal
Axillary
(rarely
axillary/
terminal)
Axillary
Terminal/
axillary
Terminal
Axillary
Terminal/
axillary
Terminal
Terminal/
cauliflorous
Inflorescence type
Paniculate
Paniculate with
scorpioid
lateral
branches
Cymose
Cymose to
umbelliform or
fasciculate
Paniculate
Cymose
Scorpioid
Scorpioid
Cymose/
paniculate
Corolla aestivation
Leftcontorted
Valvate
Leftcontorted
Leftcontorted
Leftcontorted
Valvate
Leftcontorted
Leftcontorted
Leftcontorted
Ovules per carpel
Few
2–5
2
1
Many
1
Many
Many
1
Fruit type
Capsular
Samaralike
Non-fleshy, Schizodrupaceous carpous
Capsular
Drupaceous
Capsular
Capsular
Drupaceous
Dispersal mode
Anemochorous
Anemochorous
Sea
currents
Anemochorous
Anemochorous
Zoochorous
Anemochorous
Anemochorous
Zoochorous
Pollen type
Colporate
Colporate
Colporate
Colporate
Colporate
Porate
Pororate/
colporate
Colporate
Colporate
Character
Glionnetia
947
Razafimandimbison & al. • A basal grade in the Vanguerieae alliance
genus. The genus can be confused with some members of
Ixoreae because of its arborescent growth habit, terminal
and paniculate inflorescences, and large, 5-merous flowers
with left-contorted aestivation. However, Glionnetia bears
capsular fruits with many-seeded carpels, while the members
of Ixoreae have drupaceous fruits with one-seeded carpels
(Table 2). Futhermore, Glionnetia and Crossopteryx have arborescent growth habit, terminal, paniculate inflorescences,
left-contorted aestivation, and capsular fruits. However, these
genera have very distinct seeds: the former with very small
(2–3 mm long), unwinged seeds (Tirvengadum, 1984) and
the latter with large, flattened seeds with deeply fimbriate
wings (Stoffelen & al., 1996). Additionally, Crossopteryx is
restricted to tropical Africa, while Glionnetia is endemic to
the Seychelles. For now, we leave Glionnetia unclassified at
tribal level pending further analyses.
Trailliaedoxa was considered to be a genus with uncertain
phylogenetic position within the family Rubiaceae (Smith, 1917;
Robbrecht, 1988). Smith (1917) thought that the floral structure
of the genus is similar to that of Alberteae sensu Hooker (1873),
which is characterized by contorted aestivation and solitary
pendulous ovules. On the other hand, its ericoid habit has been
compared to that of Spermadictyon of the tribe Paederieae in
the subfamily Rubioideae (Smith, 1917). Our Ixoroideae-FourLocus analyses (Fig. 3) place Trailliaedoxa in the Vanguerieae
alliance. This position is consistent with the frequent occurrence of contorted aestivation in Ixoroideae, particularly in
the Coffeeae and Vanguerieae alliances. Trailliaedoxa is very
distinct from other genera in the alliance because of its ericoid
habit, densely pubescent styles, and schizocarpous fruits.
Based on the results of the analyses presented (see also
Table 2), we maintain the generic status of Glionnetia, Jacki
opsis, and Trailliaedoxa and the tribal status of Jackieae as
delimited by Ridsdale (1979). We suggest that Trailliaedoxa and
Scyphiphora be recognized at tribal level. However, the formal
recognition of the two respective new tribes will be published
in another paper focusing on the tribal assessment and relationships in the subfamily Ixoroideae (Kainulainen & al., subm.).
A basal grade of monotypic genera in the species-rich
Vanguerieae alliance and its conservation implications. —
The Ixoroideae-Four-Locus analyses (Fig. 3) reveal a basal
grade of morphologically distinct, monotypic genera (Crossop
teryx, Jackiopsis, Scyphiphora, Trailliaedoxa, and Glionnetia,
respectively) in the otherwise species-rich Vanguerieae alliance. In other words, these monotypic genera form a paraphyletic assemblage at the base of the alliance. These results here
presented are interesting from both phylogenetic and conservation standpoints, as these genera may be sole representatives
of their respective lineages and therefore may carry unique
genetic information. Their extinction would mean loss of their
entire lineages (see also Rydin & al., 2008; Rana & Ranade,
2009). These monotypic genera could be potential candidates
for conservation priorities due to their genetic isolation, however this latter should not automatically be reason for conservation concern. Below we present conservation assessments of
these five genera, applying the criteria set in World Conservation Union (IUCN) Red List Categories (IUCN, 2001).
948
TAXON 60 (4) • August 2011: 941–952
■ Crossopteryx febrifuga is a shrub or small tree species
restricted to the savanna woodlands of tropical Africa. The species is common and widespread throughout tropical Africa and
is fire resistant due to its thick bark (Gignoux & al., 1997); it is
widely used as a medicinal plant across much of tropical Africa
but is not considered endangered. At present, it may represent
less of a conservation priority, and therefore, we consider it to
be Least Concern (IUCN, 2001).
■ Jackiopsis ornata is restricted to Southeast Asia and
distributed in the Malay Peninsula, Sumatra, Borneo, and the
Riau Archipelago (Ridsdale, 1979). According to Sosef & al.
(1998), the species is “reported to be locally frequent but never
common in lowland swamp forests and riverine habitats”; the
wood of J. ornata is “rarely and only locally used”. It was considered by UNEP-WCMC (2008) to be a timber tree species,
which is not in the international trade or of conservation concern. However, the occurrence of this species appears patchy
and is not registered in most peat swamp forest inventories (e.g.,
Kishokumar, 2008). In Southeast Asia, there has been much
large-scale conversion of peatlands into commercial agriculture, such as for oil palms (Aiken & Leigh, 1992; Jomo & al.,
2004; Kathirithamby-Wells, 2005). In addition, the frequent
fires degrading peat swamp forests on Borneo (Sosef & al.,
1998) and Sumatra (Anderson & Bowen, 2000) already had a
tremendous impact on the natural habitats of J. ornata. Based
on the information presented above, we consider J. ornata
Endangered (IUCN, 2001). Therefore, an ex situ conservation
plan for this unique taxon is strongly encouraged. The gregarious flowering and stately habit of mature J. ornata trees, with
spectacular displays of dense, brightly colored inflorescences,
should provide an added incentive for future conservation and
planting.
■ Scyphiphora hydrophylacea is a mangrove plant. It is
distributed from East India throughout the Indo-Malesian region to the West Pacific and northern Australia, Sri Lanka, and
Madagascar (Puff & al., 2007). The wide coastal distribution
range can be attributed to the trans-oceanic dispersal of its
buoyant fruits. Mangrove stands are highly threatened ecosystems and exploited for fuelwood and timber, local constructions, development of salt beds, and conversion to aquaculture
ponds (e.g., Tomlinson, 1986; Primavera, 2000). For example,
mangrove areas in the Philippines decreased from 428,382 ha
(Villaluz, 1953) to 200,500 ha (DENR, 1996) between 1951 and
1995. About 50% of the Philippine mangroves that disappeared
from 1950 to 1988 had been converted into culture ponds, making aquaculture the main cause of the mangrove loss in the
Philippines (Primavera, 2000). Scyphiphora hydrophylacea
is reported to be rare and highly threatened in Sri Lanka and
Peninsular India, where seedlings and young plants are scarce.
This situation has been attributed to a very low percentage of
fertile fruits in S. hydrophylacea and its inability to produce
healthy seedlings, which is possibly due to inbreeding depression in small, isolated populations (Hettiarachchi & Jayaratne,
2006). According to Puff & al. (2007), S. hydrophylacea is
usually not present in large populations in Thailand. Within
its center of distribution in Southeast Asia, there is much
alteration and destruction of its habitat. Largely ignored by
TAXON 60 (4) • August 2011: 941–952
forestry inventories or conservation projects, the occurrence
of S. hydrophylacea is rare or patchy along the more frequently
inundated mangrove fringes and adjacent shores. Occurrence is
largely insignificant to absent within the main formation that
is dominated by taller stands of Rhizophoraceae and other tree
species. Moreover, conversion to other land use or subsequent
degradation due to adjacent coastal development can drastically reduce mangrove extents (Chan & al., 1993; Sasekumar
& Then, 2005). Based on the evidence for concern presented
above, we consider S. hydrophylacea Near Threatened (IUCN,
2001) despite its extensive range.
■ Trailliaedoxa gracilis appears to have a narrow distribution range. Endemic to southern China, it grows in rocky
habitats and thickets on the mountain slopes of Sichuan and
Yunnan at an altitude of 1540 to 3000 m. The conservation
status of the genus is currently unknown, as it is only known
from a few specimens. Trailliaedoxa gracilis may be a potential
candidate for a high conservation priority, however it is poorly
known (= Data Deficient; IUCN, 2001).
■ Finally, Glionnetia sericea is confined to a very restricted area less than 1000 ha on Mahé and Silhouette Islands
in the Seychelles Archipelago. It is one of two genera of Rubiaceae endemic to the Seychelles and has been considered
Vulnerable D2 (IUCN, 2010). However, a recent assessment
concluded that the species is Endangered B1ab(iii)+2ab((iii)
(Huber, pers. comm.). Glionnetia sericea thrives mainly on
high ridges in the mountains (Tirvengadum, 1984); it does not
seem to grow well at lower altitudes (K. Beaver, pers. comm.).
Conservation in situ is strongly encouraged.
ACKNOWLEDGEMENTS
The authors thank Anbar Khodanbadeh for help with sequencing;
the three anonymous reviewers and Elmar Robbrecht for their constructive criticisms on an earlier version of the paper; the Seychellois
authority for approving our research proposal to collect Glionnetia
for this study; and the following herbaria for allowing access to their
collections: BR, K, L, NY, P, S, SING, TAN, TEF, and UPS. This work
is supported by the Swedish Research Council and the Knut and Alice
Wallenberg Foundation to BB.
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Appendix. Species sampled for the study.
Species, accession nos. [ndhF, rbcL, rps16, trnTF; an n-dash (–) denotes missing data; superscripts 1–27 refer to literature or GenBank sources, superscripts
28–37 refer to voucher specimens and herbarium acronyms, both given at the end of the Appendix].
Acranthera frutescens Valeton, –, AM1171989, –, –; Acranthera grandiflora Bedd., –, AM1171999, –, –; Alstonia scholaris (L.) R. Br., –, X9176028, –, –; Am
phidasya ambigua Standl.) Standl., –, Y1184420, –, –; Arcytophyllum aristatum Standl., –, AJ28859529, –, –; Anthocleista Afzel. ex R. Br., –, L1438930, –, –;
Anthospermum herbaceum L. f., –, X8362310, –, –; Airosperma vanuense S.P. Darwin, AM9498451,–, FM2047001, FM2071081; Alberta magna E. Mey., AJ2362823
EU8174117 FM2047011 AJ6201184; Aleisanthia rupestris (Ridl.) Ridl., –, –, AF2429026, AF1526605; Aleisanthiopsis distantiflora (Merr.) Tange, HM16435028,
EU8174117, EU8174347, EU8174537; Aidia micrantha (K. Schum.) Bullock ex F. White, –, Z6884415, –, –; Argostemma hookeri King, –, Z6878831, –, –; Augusta
rivalis (Benth.) J.H. Kirkbr., AM9498461, AM9498421, –, FM2071181; Aulacocalyx jasminiflora Hook.f., –, EU8174137, EF205639 8, EU8174557; Bertiera
guianensis Aubl.; AM9498471, AJ2248452, FM2047101, FM2071191 & AF1526705; Boholia nematostylis Merr., AM9498481, FM2047111, AM1173509; Caly
cophyllum candidissimum (Vahl) DC., AJ2362853, X8362710, FM2047121, AJ84739811; Canthium tetraphyllum (Schweinf. ex Hiern) Robyns, AM9498491,
X8364910, FM2047131, FM2071201; Carphalea glaucescens (Hiern) Verdc., –, Z6878931, –, –; Catesbaea spinosa L., –, X8362810, –, –; Chioccoca alba (L.)
Hitch., –, L1439430, –, –; Cephalanthus occidentalis L., –, X8362910, –, –; Cinchona pubescens Vahl., AJ23584312, X8363010, FM2047141, AJ34696313; Coc
cocypselum hirsutum Bartl. ex DC., –, X8714510, –, –; Coffea arabica L., EF04421314, EF04421314, EF04421314, EF04421314; Colletoecema dewevrei (De Wild.)
E.M.A. Petit, –, EU14545723, –, –; Condaminea corymbosa (Ruiz & Pav.) DC., –, Y187133, –, –; Coptosapelta diffusa Steenis, –, EU14545223, –, –; Coptosapelta
flavescens Korth., –, Y187143, –, –; Coptosapelta montana Korth. ex Valeton, –, EU14545123, –, –; Coussarea macrophylla (Mart.) Müll. Arg., –, Y118473, –,
–; Cremaspora triflora ssp. confluens (K. Schum.) Verdc., AM9498501, Z6885615, FM2047151, FM2071211; Cremocarpon lantzii Bremek., –, AM1172229, –,
–; Crossopteryx febrifuga (Afzel. ex G. Don) Benth. 1, –, AJ34700913, FM2047161, FM2071221; Crossopteryx febrifuga (Afzel. ex G. Don) Benth. 2, AM9498511,
AM1172239, FM2047171, FM2071231; Cruckshancksia hymenodon Hook. & Arn., –, AJ28859929, –, –; Cubanola domingensis (Britton) Aiello, AM1173459,
X8363210, FM2047181, FM2071241; Cyclophyllum deplanchei Hook.f., –, EU8174167, EF2056408, EF2056318; Damnacanthus indicus C.F. Gaertn., –, Z6879331,
–, –; Danais xanthorrhoea (K. Schum.) Bremek., –, Z6879431, –, –; Declieuxia cordigera Mart. & Zucc. ex Scult. & Schult.f., –, AM1172249, –, –; Dibrachiono
stylus kaessneri (S. Moore) Bremek., –, AJ61621132, –, –; Diplospora polysperma Valeton, –, AJ28670317, AM1173019, EU14553823; Dunnia sinensis Tutcher 1,
–, EU14546723, –, –; Dydimaea alsinoides (Cham. & Schtdl.) Standl., –, Z6879531, –, –; Emmenopterys henryi Oliv., AJ2362943, Y187153, FM2047191, FM2071251;
Ernodea littoralis Sw., –, AJ28860129, –, –; Faramea multiflora A. Rich., –, Z6879631, –, –; Ferdinandusa speciosa Pohl., –, AM1172269, –, –; Feretia aerugi
nescens Stapf, –, Z6885731, –, –; Fernelia buxifolia Lam., –, AJ28670417, –, –; Galium album Mill., –, X8109010, –, –; Gardenia hansemannii K. Schum.,
AM9498521, AJ31844616, FM2047201, FM2071261; Gelsemium Juss., –, L1439730, –, –; Gentiana L., –, L1439830, –, –; Geophila obvallata Didr., –, AM1172289,
–, –; Glionnetia sericea (Baker) Tirveng. 1, HM53621629, HM53622229, HM53622829, HM53623429; Glionnetia sericea (Baker) Tirveng. 2, HM53621730,
HM53622330, HM53622930, HM53623530; Glionnetia sericea (Baker) Tirveng. 3, HM53621831, HM53622431, HM53623031, HM53623631; Greenea corymbosa
(Jack) Volgt, –, –, AF2429616, AF1526575; Greenea oblonga Craib, HM16437132, –, EU8174597; EU8174397; Greenea sp. 1, –, –, EU8174387, EU8174587; Greenea
sp. 2, –, EU8174187, EU8174407, EU8174607; Guettarda uruguensis Cham. & Schltdl., –, X8363810, –, –; Gynochthodes coriacea Blume, –, AJ28860329, –, –;
Hedyotis fruticosa L., –, Z6879931, –, –; Hillia triflora (Oerst.) C.M. Taylor; –, X8364210;, –, –,; Houstonia caerutea L., –, AJ28860429, –, –; Hydnophytum
formicarum Jack, –, X8364510, –, –; Hypobathrum racemosum (Roxb.) Kurz, AM9498531, AJ28670517, AM1173189, FM2071271; Ixora brachypoda DC., –,
EU8174217, EU8174427, EU8174637; Ixora coccinea L., AJ2362993, X8364610, EF2056418, EU8174647; Ixora guineensis Benth., –, EU8174247, EU8174437,
EU8174677; Ixora hookeri (Oudem.) Bremek.; –, EU8174257, EU8174437, EU8174677; Ixora margaretae N. Hallé, –, EU8174257, EU8174447, EU8174687; Ixora
moorensis (Nadeaud) Fosberg, –, EU8174207, EU8174417, EU8174627; Ixora trilocularis (Balf.f.) Mouly & B. Bremer, –, EU8174177, EU8174377, EU8174577;
Jackiopis ornata Ridsdale 1, HM5362133, HM53621933, HM53622533, HM53623133; Jackiopis ornata Ridsdale 2, HM53621434, HM53622034, HM53622634,
HM53623234; Jackiopis ornata Ridsdale 3, HM53621535, HM53622135, HM53622735, HM53623335; Keetia gueinzii (Sond.) Bridson, –, –, AM1173239, AJ6201439;
Kohautia caespitosa Schnizl., –, Z6880031, –, –; Kraussia floribunda Harv., –, Z6885831, –, –; Lasianthus pedunculatus (Griseb.) Urb., –, Z6880231, –, –; Lerchea
bracteata Valeton, AJ28861029; Luculia grandifolia Ghose, –, X8364810, –, –; Luculia gratissima (Wall.) Sweet, AJ01198718, AM1172439, AJ43103619, AJ43091119;
Luculia pinceana Hook., –, EU14544723, –, –; Manostachya ternifolia E.S. Martins, AJ61621320; Margaritopsis acutifolia C. Wright, –, AM1172479, –, –;
Maschalocorymbus corymbus (Blume) Bremek., –, AJ28861129, –, –; Mitchella repens L., –, Z6880531, –, –; Mitrasacmopsis quadravalvis Jovet, –, AJ61621420,
–, –; Morinda citrifolia L., AJ2363003, X8365110, AJ32007816, FM2075891 & AF1526165; Mostuea Didr., –, L144042, –, –; Mussaenda arcuata Poir., AJ2363013,
Y1185420, FM2047211, FM2071281; Mussaenda erythrophylla Schumach. & Thonn., –, X836521; Mycetia malayana (G. Don) Craib, –, Z6880631, –, –; Nauclea
orientalis (L.) L., –, X8365310, –, –; Nematostylis anthophylla (A. Rich. ex DC.) Baill., FM2076501, FM2076481, FM2047231, FM2071301; Nertera granadensis
(Mutis ex L.f.) Druce, –, X8365410, –, –; Neurocalyx zeylanicus Hook., –, Z688073, –, –; Normandia neocaledonica Hook.f., –, AM1172509, –, –; Oldenlandia
corymbosa L., –, X8365510, –, –; Ophiorrhiza mungos L., –, X8365610, –, –; Oreopolus glacialis (poepp.) Ricardi, –, AJ28861229, –, –; Paederia foetida L., –,
AF33237333, –, –; Palicourea crocea (Sw.) Schult, –, AM1172539, –, –; Parapentas silvatica (K. Schum.) Bremek., –, X8365710, –, –; Pauridiantha paucinervis
(Hiern) Bremek., –, Z6881131, –, –; Pavetta abyssinica Fresen., AM9498541, Z6886315, FM2047261, FM2071331; Pentagonia macrophylla Benth., AJ2363033,
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TAXON 60 (4) • August 2011: 941–952
Appendix. Continued.
X8365810, FM2047271, FM2071341; Pentas lanceolata (Forssk.) Deflers., –, Z8365931, –, –; Pentodon pentandrus (Schumach. & Thonn.) Vatke. Oesterr., –,
X8366010, –, –; Peponidium comorense Arènes, –, –, EF2056468 EF2056328 ; Posoqueria latifolia (Rudge) Roem. & Schult., AM9498551, Z6885015, FM2047281,
FM2071351; Pouchetia gilletii De Wild., –, Z6885915 , –, –; Praravinia suberosa (Merr.) Bremek., –, AJ28861629, –, –; Pseudomussaenda flava Verdc.,
AM9498561, Y1185520, FM2047291, FM2071361; Psychotria kirkii Hiern, –, X8366310, –, –; Psychotria poeppigiana Müll.Arg., –, Z6881831, –, –; Pyrostria
hystrix (Bremk.) Bridson, EU14541823, AM1172629, AM1173389, AJ6201684; Razafimandimbisonia minor (Baill.) Kainul. & B. Bremer, AM9498441, EU8174107,
EF2056378, EU8174527; Razafimandimbisonia sambiranensis (Homolle ex Cavaco) Kainul. & B. Bremer, –, EU8174317, EF2056458, EU8174747; Retiniphyllum
concolor (Spruce ex Benth.) Müll.Arg., –, –, EU82162924 EU82164124; Retiniphyllum maguirei Standl., –, –, EU82163224 EU82164624; Retiniphyllum pilosum
(Spruce ex Benth.) Müll.Arg., –, AF33165421, FM2047301, FM2071371; Retiniphyllum schomburgki (Benth.) Müll.Arg., –, –, EU82163124, EU82164524 ; Rhachi
callis americana (Jacq.) Hitchc., –, X8366410, –, –; Rondeletia odorata Jacq., –, Y1185720, –, –; Rubia tinctorum L., –, X8366610, –, –; Rustia thibaudioides (H.
Karst.) Delprete, AJ2363103, Y187163, FM2047311, FM2071381; Sabicea aspera Aubl., –, AY53850822, –, –; Sabicea diversifolia Pers., –, EU14545923, –, –;
Sabicea villosa Roem. & Schult., AM9498571, Y1185820, FM2047321, FM2071391; Saldinia sp. 1, –, AM1172699, –, –; Schradera K. Krausse sp., –, Y118593,
–, –; Schismatoclada sp., –, AM1172719, –, –; Schizocolea linderi (Hutch. & Dalziel) Bremek., –, AM1172729, –, –; Scyphiphora hydrophylacea C.F. Gaertn.
1, AJ2363113, Y187173, FM2047331, FM2071401; Scyphiphora hydrophylacea C.F. Gaertn. 2, –, –, EU82163424 EU82164824; Sherardia arvensis L., –, X8110610,
–, –; Spermacoce laevis Lam., –, Z6882331–, –; Spigelia L., –, Y1186320, –, –; Sipanea biflora (L. f.) Cham. & Schltdl., EU14541323, AY53850922, FM2047341,
FM2071411; Sipanea hispida Benth. ex Wernham, EU14541423, EU14545823, EU14549223, AY55510727; Sipanea pratensis Aubl., –, –, AF2430226, AF1526775;
Spiradiclis bifida Kutz, –, EU145465, –, –; Steenisia pleurocarpa (Airy Shaw) Bakh.f., –, AM1172799, FM2047351, FM2071421; Strychnos L., –, L1441028, –,
–; Tamridaea capsulifera (Balf.f.) Thulin & B. Bremer, –, Y1186020, FM2047361, FM2071431; Tennantia sennii (Chiov.) Verdc. & Bridson, AM9498581,
AM9498431, FM2047371, FM2071441; Thecorchus wauensis (Schweinf. ex Hiern) Bremek., –, AM1172829, –, –; Theligonum cynocrambe L., –, X8366810, –,
–; Tocoyena pittieri (Standl.) Standl., AM9498591, –, FM2047381, FM2071451; Trailliaedoxa gracilis W.W. Sm. & Forrest 1, HM16439936, HM16418236,
HM16422636, HM16433836; Trailliaedoxa gracilis W.W. Sm. & Forrest 2, HM16440037, HM16418337, HM16422737, HM16433937; Tricalysia cryptocalyx Baker,
–, Z6885415, AF00408826, AM99948725; Trichostachys aurea Hiern, –, EU14546223, –, –; Trichostachys sp., –, AJ28862629, –, –; Urophyllum ellipticum (Wight)
Thwaites, –, X8367010, –, –; Vangueria madagascariensis J.F. Gmel., AJ1308403, X8367010, EU82163624, FM2071461; Virectaria major (K. Schum.) Verdc., –,
Y1186120, –, –; Xanthophytum borneense (Valeton) Axelius, –, EU14546623, –, –; Wendlandia tinctoria (Roxb.) DC., AM9498601, FM2076491, FM2047391,
FM2071471.
Published sequences: 1, Kainulainen & al. (2009); 2, Andreasen & al. (1999); 3, Bremer & al. (1999); 4, Lantz & Bremer (2004); 5, Rova & al. (2002); 6, Rova,
J.H.E. (Genbank unpub.); 7, Mouly & al. (2009); 8, Mouly & al. (2007); 9, Bremer & Eriksson (2009); 10, Bremer & al. (1995); 11, Alejandro & al. (2005); 12,
Backlund & al. (2000); 13, Razafimandimbison & Bremer (2002); 14, Samson & al. (2007); 15, Andreasen & Bremer (1996); 16, Novotny & al. (2002); 17, Andreasen & Bremer (2000); 18, Oxelman & al. (1999); 19, Bremer & al. (2002); 20, Bremer & Thulin (1998); 21, Andersson, L. (Genbank unpub.); 22, Andersson
& Antonelli (2005); 23, Rydin & al. (2008); 24, Cortes-B. & al. (2009); 25, Tosh & al. (2009); 26, Andersson & Rova (1999); 27, Delprete & Cortes-B. (2004) .
Voucher information: 28, Tange 46977 (AAU); 29, Beaver 3 (S); 30, Beaver 17 (S); 31, Beaver 27 (S); 32, Larsen K. & Larsen S.S. 33451 (P); 33, Tan s.n. (Malaysia), cA047; 34, Tan s.n. (Malaysia), cA048; 35, Tan s.n. (Malaysia), cA049; 36, Yü 1348 (HUH); 37, Boufford & al. 35041 (MO) .
952