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De Block & al. • Molecular phylogenetics of Pavetteae (Rubiaceae)
Molecular phylogenetics and generic assessment in the tribe Pavetteae
(Rubiaceae)
Petra De Block,1 Sylvain G. Razafimandimbison,2 Steven Janssens,1 Helga Ochoterena,3 Elmar Robbrecht1
& Birgitta Bremer2
1 Botanic Garden Meise, Nieuwelaan 38, 1860 Meise, Belgium
2 Bergius Foundation, Royal Swedish Academy of Sciences and Botany Department, Stockholm University, 10691 Stockholm, Sweden
3 Instituto de Biología, Universidad Nacional Autónoma de México, Apdo. Postal 70-367, CP 04510, Mexico City, Mexico
Author for correspondence: Petra De Block, Petra.DeBlock@BR.fgov.be
ORCID (http://orcid.org/): PDB, 0000-0001-7210-7868; SGR, 0000-0002-4545-3893; HO, 0000-0002-3830-4603
DOI http://dx.doi.org/10.12705/641.19
Abstract This is the first phylogenetic study focused on the Pavetteae, one of the most species-rich and morphologically
diverse tribes within the coffee family (Rubiaceae). Fifteen of the 17 currently recognized genera, represented by 85 taxa, were
sequenced for rps16, trnT-F and ITS and analysed using Bayesian inference and maximum likelihood methods. The monophyly
of the Pavetteae is confirmed. Four major lineages are identified, but their phylogenetic relationships are not fully resolved.
The continental African genera Rutidea, Nichallea and Tennantia, the Madagascan genera Homollea and Robbrechtia, and the
paleotropical genus Pavetta are monophyletic. Other genera are paraphyletic in their current circumscriptions and the following
changes are made: Homolliella is placed in synonymy with Paracephaelis, and Coleactina and Dictyandra with Leptactina,
resulting in four new combinations. The large paleotropical genus Tarenna is shown not to be monophyletic. In the future, the
name Tarenna should not be used for continental African species. Most of these could be transferred to the hitherto monospecific genus Cladoceras, but other species might constitute altogether new genera. The relationship between the monophyletic
Asian-Pacific and Madagascan Tarenna species remains unclear. The phylogeny of the Madagascan genera of the Pavetteae
is largely unresolved and the largest Madagascar-centred genus Coptosperma was not recovered as monophyletic. The low
resolution for the Madagascan taxa can be considered as an indication of rapid radiation. Further molecular and morphological studies are necessary to clarify the phylogeny of the Pavetteae, especially regarding the African Tarenna species and the
Madagascan genera of the tribe.
Keywords Coleactina; Dictyandra; Homolliella; Madagascar; Tarenna
Supplementary Material Electronic Supplement (Figs. S1–S2) and alignment are available in the Supplementary Data section
of the online version of this article at http://www.ingentaconnect.com/iapt/tax
INTRODUCTION
With 17 genera and ca. 650 species (Table 1; Fig. 1), the
Pavetteae is one of the largest tribes in the subfamily Ixoroideae
of the Rubiaceae (coffee family). The two genera with the highest species numbers, Pavetta L. (ca. 360 spp.) and Tarenna
Gaertn. (ca. 200 spp.), have a Paleotropical distribution. Pachystylus K.Schum. (2 spp.) is endemic to Melanesia, and Triflorensia S.T.Reynolds (3 spp.) to Australia. All other genera occur
in Africa and/or Madagascar, with Madagascar as an important
center of diversity for the tribe. Pavetteae show high morphological variation, especially regarding reproductive characters
such as the number of seeds per fruit, seed and placentation
type, etc. Representatives of the tribe occur throughout the
Paleotropics in both humid and dry vegetation types.
The taxonomic history of the tribe is long and complicated,
with the name Pavetteae first used in 1829 (Dumortier, 1829;
Richard, 1829) but quickly abandoned. The genera included
in it, such as Ixora L. and Pavetta, were placed in the tribes
Ixoreae or Coffeeae (Richard, 1830). More then a century later,
Bremekamp (1934) suggested that within Ixoreae/Coffeeae the
genera with terminal inflorescences formed a natural group.
Robbrecht (1981, 1984) concurred with him, and elevated this
group to tribal rank, resurrecting the name Pavetteae A.Rich.
ex Dumort. In this tribe, Robbrecht not only included genera of
the Ixoreae/Coffeeae, but also several genera of the Gardenieae
(e.g., Tarenna, Leptactina Hook.f.). The Pavetteae are characterized by the following characters: terminal inflorescences;
3- or 4-colporate pollen grains with reticulate or perforate tectum; relatively small, bilocular drupes; one to many seeds per
locule, freely surrounding the placenta; seeds with an adaxial
hilar excavation, the exotesta often forming a thickened ring
around this cavity; exotesta cells with or without thickenings,
when present, then thickenings only occurring along the outer
Received: 16 Jun 2014 | returned for (first) revision: 4 Aug 2014 | (last) revision received: 16 Dec 2014 | accepted: 16 Dec 2014 || publication date(s):
online fast track, n/a; in print and online issues, 2 Mar 2015 || © International Association for Plant Taxonomy (IAPT) 2015
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TAXON 64 (1) • February 2015: 79–95
tangential wall and containing narrow channels. Shortly after
the reinstatement of the tribe, as a result of a detailed morphological study, Bridson & Robbrecht (1985) redelimited the
Pavetteae and distinguished two informal groups, one including
the genera allied to Tarenna, and the other including the genera
allied to Ixora. Molecular studies demonstrated the paraphyletic nature of Pavetteae sensu Bridson & Robbrecht (1985),
with Ixora consistently placed separately from the rest of the
tribe (e.g., Andreasen & Bremer, 1996, 2000; Andreasen, 1997).
Bridson & Robbrecht’s (1985) informal groups were therefore
elevated to tribal rank, which resulted in the reinstatement of a
much-narrowed tribe Ixoreae A.Gray and the transfer of Ixora,
Captaincookia N.Hallé, Doricera Verdc., Myonima Comm. ex
A.Juss. and Versteegia Valeton to this newly resurrected tribe.
The currently accepted circumscription of Pavetteae follows De Block (2003b). It includes the genera cited as representatives of the tribe by Bridson & Robbrecht (1985) and
Robbrecht (1988, 1994) with the exceptions of Duperrea Pierre
ex Pit. and Ixora and allied genera (Table 1). The only recent
change was the description of two new genera: Robbrechtia
De Block, endemic to Madagascar (De Block, 2003b) and Triflorensia, endemic to Australia (Reynolds & Forster, 2005).
Molecular studies have shown the tribe Pavetteae in this delimitation to be a strongly supported group (Andreasen & Bremer,
Table 1. Overview of the Pavetteae according to recent literature.
Genera
Geographical distribution
No. of
species
Protologue
Inclusion in
tribe based on:
Genera of Pavetteae in
De Block & al., this paper
Cladoceras Bremek.
East Africa
1
Bremekamp, 1940
2;3;4;5;6;8;9
Cladoceras (including a number
of continental African Tarenna)
Coleactina N.Hallé
West central Africa
1
Hallé, 1970
2;3;4;5;6;8;9
Coptosperma ª Hook.f.
= Enterospermum Hiern
East and South Africa, Comores,
Mascarenes, Madagascar
19
Hooker, 1873
1;2;3;4;6;8;9
Dictyandra Welw. ex
Hook.f.
Continental tropical Africa
2
Hooker, 1873
1;2;3;4;5;6;8;9
Homollea Arènes
Madagascar
3
Arènes, 1960
2;3;6;4;8
Homolliella Arènes
Madagascar
1
Arènes, 1960
2;3;4;6;8
Leptactina Hook.f.
Continental tropical Africa
ca. 20
Hooker, 1871
1;2;3;4;5;6;8;9
Leptactina (including
Coleactina and Dictyandra)
Nichallea Bridson
West and west central Africa
1
Bridson, 1978b
1;2;3;4;6;8
Nichallea
Pachystylus K.Schum.
New Guinea
2
Schumann, 1889
1;2;3;4;6;8
Pachystylus
Paracephaelis Baill.
East Africa, Madagascar
4
Baillon, 1879
2;3;4;6;8;9
Paracephaelis (including
Homolliella)
Pavetta L.
Paleotropics (not in Madagascar)
ca. 360
Linnaeus, 1753
1;2;3;4;5;6;8;9
Pavetta
Robbrechtia De Block
Madagascar
2
De Block, 2003b
6;8;9
Robbrechtia
Rutidea DC.
Continental tropical Africa
22
Candolle, 1807
1;2;3;4;5;6;8;9
Rutidea
Schizenterospermum
Homolle ex Arènes
Madagascar
4
Arènes, 1960
2;3;4;6;8
Schizenterospermum
TarennaB Gaertn.
Paleotropics
ca. 200
Gaertner, 1788
1;2;3;4;5;6;8;9
Tarenna (excluding all
continental African species)
Tennantia Verdc.
East Africa
1
Verdcourt, 1981
2;3;4;5;6;8;9
Tennantia
Triflorensia
S.T.Reynolds
Australia
3
Reynolds & Forster,
2005
7
Triflorensia
Coptosperma
Homollea
Note: this table does not take into account genera that in the past were considered to belong to the Pavetteae but whose new position outside the
tribe is generally accepted (such as Ixora and allies, Duperrea).
1, Robbrecht (1984); 2, Bridson & Robbrecht (1985); 3, Robbrecht (1988); 4, Robbrecht (1994); 5, Andreasen & Bremer (2000); 6, De Block
(2003b); 7, Reynolds & Forster (2005); 8, Robbrecht & Manen (2006); 9, Bremer & Eriksson (2009).
a, sensu De Block & al., 2001 (all species with a single, usually ruminate seed per fruit occurring in Africa, Madagascar, the Seychelles, Mascarenes and Comores, i.e., including Zygoon and Enterospermum).
b, sensu De Block & al., 2001 (all species of Tarenna except those with a single, usually ruminate, seed per fruit).
80
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De Block & al. • Molecular phylogenetics of Pavetteae (Rubiaceae)
Fig. 1. Representative taxa of the tribe Pavetteae. A, Homollea longiflora, young fruits; B, Homolliella sericea, flowers; C, Paracephaelis cinerea,
flowers; D, Paracephaelis tiliacea, young fruits; E, Rutidea sp., flowers; F, Pavetta schumanniana, flowers; G, Pavetta schumanniana, leaf with
bacterial galls; H, Coptosperma sp., leaves and stipules; I, Schizenterospermum rotundifolium, leaves and stipules; J, Coptosperma nigrescens,
fruits and flowers; K, Robbrechtia grandifolia, flowers; L, Tarenna grevei, flowers; M, Tarenna thouarsiana, flowers; N, Dictyandra arborescens, flowers; O, Leptactina sp., flowers; P, Leptactina benguelensis, fruit. — Photographs by Petra De Block (A–B, H–I, K, M–N), Steven
Dessein (C–E, P) and Frank Van Caekenberghe (F–G, J, L, O).
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TAXON 64 (1) • February 2015: 79–95
2000; Robbrecht & Manen, 2006; Bremer & Eriksson, 2009).
However, in previous studies only a limited number of genera
were sequenced (Andreasen & Bremer, 2000: 6 of 17 genera;
Robbrecht & Manen, 2006: 6/17; Bremer & Eriksson, 2009:
9/17). Furthermore, relationships within the Pavetteae remain
unclear and generic circumscription uncertain, especially for
Tarenna (De Block & al., 2001) and the Madagascan representatives of the tribe.
This is the first molecular phylogenetic study focusing on
the Pavetteae, carried out within the framework of ongoing
classical taxonomic studies on the tribes Pavetteae and Ixoreae
(e.g., De Block, 1998, 2003a, 2005). Fifteen of the 17 genera currently ascribed to the tribe are represented. The main objectives
of this study are: (1) to test the monophyly of the tribe Pavetteae,
(2) to assess the monophyly of its currently recognized genera,
and (3) to assess the phylogenetic relationships among its genera. The results of this study will be used to evaluate, and, if
necessary, to improve existing tribal and generic delimitations.
species from different tribes belonging to subfamily Ixoroideae
(Alberteae, Mussaendeae, Vanguerieae, Ixoreae, Coffeeae,
Gardenieae) in accordance with earlier analyses (Robbrecht
& Manen, 2006, Bremer & Eriksson, 2009). Five Coptosperma
Hook.f. accessions from Madagascar and one Pavetta accession
from continental Africa represent undescribed new species. In
addition, we were unable to identify two Asian Pavetta species, here referred to as P. sp. B and P. sp. C (despite consulting the relevant taxonomic literature: Bremekamp, 1934,
1939a, b). Accession data of ingroup and outgroup taxa is given
in Appendix 1.
DNA isolation, amplification and sequencing. — Total
genomic DNA was extracted from silica-dried leaf material
using either a modified version of the hot CTAB protocol
(Saghai-Maroof & al., 1984, Doyle & Doyle, 1987) or the commercial E.Z.N.A.TM High Performance Plant DNA Mini Kit
(OMEGA bio-tek, Norcross, Georgia, U.S.A.).
Primers for chloroplast rps16, trnT-F and nuclear ribosomal ITS are listed in Table 2. Amplification of rps16 and
trnT-F followed protocols of Oxelman & al. (1997) and Razafimandimbison & Bremer (2002), respectively. For ITS, an
optimized touchdown PCR program was used for species of
Pavetteae in order to provide sufficient DNA. This temperature
profile consisted of 3 min initial denaturation at 95°C; 10 cycles
of 30 s denaturation at 95°C, 30 s primer annealing at 60°C,
and 1 min extension at 72°C; 30 cycles of 30 s denaturation
at 95°C, 30 s primer annealing at starting temperature 60°C
lowering 0.3°C/cycle, and 1 min extension at 72°C; and a final
extension of 7 min at 72°C. Amplification reactions were carried out on a Perkin Elmer GeneAMP 9700 thermocycler or
Eppendorf Mastercycler. The PCR mixes for rps16 and trnT-F
contained 1 µl genomic DNA, 1 µl of each primer (100 ng/µl),
2.5 µl of 10 mM dNTPs, 2.5 µl Taq Buffer, 0.2 µl KAPA Taq
DNA polymerase adjusted with MilliQ water to 25 µl. The PCR
mix for ITS was similar to that of rps16 and trnT-F except for
the addition of 1 µl DMSO (v/v) for a total of 25 µl. Sequencing reactions were performed using the Big Dye Terminator
3.1 Cycle Sequencing kit (Applied Biosystems, Foster City,
California, U.S.A.) on an Applied Biosystems 310 Genetic
Analyzer or were sent to Macrogen Inc. (Seoul, Republic of
Korea) for sequencing.
MATERIALS AND METHODS
Taxon sampling. — Fifteen of the 17 genera of the tribe
Pavetteae were sampled. Pachystylus and Triflorensia, New
Guinean and Australian endemics, respectively, were not
included due to lack of material. Apart from the monospecific
Cladoceras Bremek, Coleactina N.Hallé, Homolliella Arènes,
Nichallea Bridson and Tennantia Verdc., and Dictyandra
Welw. ex Hook.f. (comprising two species), all genera were
represented by at least two species. For genera with infrageneric classifications, we sampled species from all subgenera
(Pavetta) or sections (Rutidea DC.). In total, we included 85
Pavetteae taxa, covering the entire distribution range of the
tribe. Our sampling is representative for continental Africa and
Madagascar. However, certain regions are underrepresented,
such as the western Indian Ocean islands, Malesia/Indochina,
Papua New Guinea, Australia and the Pacific islands (with the
exception of New Caledonia).
Five genera were sequenced here for the first time: Coleactina, Homollea Arènes, Homolliella, Nichallea and Schizenterospermum Homolle ex Arènes. As outgroup, we chose eight
Table 2. Amplification primers used.
Region
rps16
trnT-trnL
trnL-trnF
ITS
82
Primer
Primer sequence (5′–3′)
rps16-F
GTGGTAGAAAGCAACGTGCGACTT
rps16-2R
TCGGGATCGAACATCAATTGCAAC
trnL-C
CGAAATCGGTAGACGCTACG
trnL-F
ATTTGAACTGGTGACACGAG
trnL-A1
ACAAATGCGATGCTCTAACC
trnL-I
CCAACTCCATTTGTTAGAAC
ITS-P17F
CTACCGATTGAATGGTCCGGTGAA
ITS-26S-82R
TCCCGGTTCGCTCGCCGTTACTA
ITS-P16F
TCACTGAACCTTATCATTTAGAGGA
ITS-P25R
GGGTAGTCCCGCCTGACCTG
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Reference
Oxelman & al., 1997
Taberlet & al., 1991
Razafimandimbison & Bremer, 2002
Lidén & al., 1995
Popp & Oxelman, 2001
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De Block & al. • Molecular phylogenetics of Pavetteae (Rubiaceae)
Sequence alignment and phylogenetic analyses. —
Sequences were automatically aligned with MAFFT v.7.017
(Katoh & al., 2002) using the E-INS-I Algorithm with a scoring matrix of 100PAM/k=2 and a Gap open penalty of 1. The
automatically aligned data matrix was subsequently finetuned
by hand in the Geneious v.5.6.1 software package. Potentially
informative indels were coded as separate characters, following
the “simple indel coding” method (Simmons & Ochoterena,
2000). Newly generated sequences have been submitted to
GenBank (Appendix 1).
The methodology of Wang & al. (2014) was used to infer
topological conflicts between different datasets. A threshold
with a BS value ≥ 70% and a PP value ≥ 0.95 was applied as an
indication of strongly supported incongruence between different datasets.
The best-fit nucleotide substitution model for each plastid
and nuclear dataset was determined using jModelTest v.2.1.4
(Posada, 2008) under the Akaike information criterion (AIC).
For ITS, the GTR + I + G model was found as best fit, whereas
the GTR + G model was shown to be the best substitution
model for rps16 and trnT-F. Bayesian analyses were conducted
with MrBayes v.3.1 (Huelsenbeck & Ronquist, 2001) on three
individual data partitions and a combined data matrix. Each
analysis was run two times for 5 million generations with trees
sampled every 1000 generations. Convergence of the chains
was examined with TRACER v.1.4 (Rambaut & Drummond,
2007). Maximum likelihood analyses were computed on the
CIPRES web portal using RAxML v.7.2.8 (Stamatakis & al.,
2008) under the GTRGAMMA model. Non-parametric bootstrapping was carried out with 1000 bootstrap replicates.
RESULTS
For this study, we generated 261 new sequences, which
were complemented with 7 sequences from GenBank in order
to obtain a dataset of 268 sequences, representing 93 taxa.
Due to difficulties in amplification and/or sequencing of ITS,
Coptosperma madagascariense (Baill.) De Block and Paracephaelis saxatilis (Scott-Elliot) De Block were represented
by two different accessions, which were thoroughly examined
to make sure they belonged to the same species. For 14 further
taxa (both ingroup and outgroup) we were unable to generate
ITS sequences.
Table 3. Characteristics of individual and combined datasets.
rps16
trnT-F ITS
Total
Number of sequences
94
93
79
94
Characters
918
2217
895
4030
Constant characters
738
1777
614
3129
Variable characters
180
440
281
901
Parsimony-informative characters
117
293
115
525
% Parsimony-informative characters 12.7
13.2
12.8
13.0
Indel-coding characters
51
30
89
6
In general, sequence variability of individual markers was
rather low (Table 3). The percentage of potentially parsimonyinformative (PI) characters was ± equal in all gene markers
used in this study (trnT-F: 13.2%; ITS: 12.8%; rps16: 12.7%). For
the combined nuclear ribosomal ITS and chloroplast trnT-F/
rps16 matrix, 89 indel characters were added (Table 3).
The majority-rule consensus topologies from the separate Bayesian inference (BI) and maximum likelihood (ML)
bootstrap analyses of rps16, trnT-F, and ITS revealed similar
topologies, yet they were largely unresolved. Nevertheless,
several clades at generic level were always recovered, e.g.,
Rutidea/Nichallea, Leptactina/Coleactina/Dictyandra, etc. No
supported incongruence (Bayesian posterior probabilities, BPP
> 0.95; maximum likelihood bootstrap support, ML-BS > 70)
was observed between the different datasets. Hence, they were
concatenated for subsequent analyses. The combined chloroplast phylogeny and the ITS phylogeny are given in the Electr.
Suppl.: Figs. S1–S2, respectively.
BI and ML analyses of the combined dataset provided similar topologies with a similar level of support for most clades
(Fig. 2). The monophyly of the tribe Pavetteae was strongly supported in both the BI and ML analyses (ML-BS = 100, BPP =
1.00). Within the tribe there was support for four clades (Fig. 2),
but the relationships among these clades were unresolved.
Clade I (ML-BS = 100, BPP = 1.0) comprised the continental African genera Nichallea and Rutidea, which were resolved
as sister taxa. The monophyly of Rutidea was well supported
(ML-BS = 100, BPP = 1.00). Rutidea sect. Rutidea (R. orientalis
Bridson to R. decorticata Hiern) was recovered as monophyletic, but R. sect. Tetramera Bridson (R. membranacea Hiern
and R. fuscescens Hiern) was not.
Clade II (ML-BS = 100, BPP = 1.0) comprised the continental African genera Leptactina, Dictyandra and Coleactina.
Leptactina was shown not to be monophyletic in its current
delimitation since Coleactina was nested within it. Coleactina
papalis N.Hallé was sister to Leptactina benguelensis (Welw.
ex Benth. & Hook.f.) R.D.Good (ML-BS = 70, BPP = 1.0).
Dictyandra arborescens Welw. ex Hook.f. formed a weakly
supported clade (ML-BS = 66, BPP = 0.93) with the sister
species L. pynaertii De Wild. and L. mannii Hook.f. (ML-BS
= 62, PP: 0.99), the type of Leptactina.
Clade III (ML-BS = 100, BPP = 1.0) consisted of the paleotropical Pavetta, the monospecific East African Cladoceras and
the continental African species of Tarenna. Within this lineage,
Tarenna jolinonii N.Hallé was sister to the weakly supported
clade comprising the rest of the sampled taxa (ML-BS = 65,
BPP = 0.66). This clade was resolved into two well-supported
monophyletic subclades, but the relationships between the two
subclades and T. jolinonii remained unclear due to poor support. The first subclade comprised Cladoceras subcapitatum
(K.Schum. & K.Krause) Bremek. from East Africa and seven
of the ten sampled continental African Tarenna species (MLBS = 93, BPP = 1.0). The second subclade (ML-BS = 92, BPP =
1.0) contained the paleotropical Pavetta with Tarenna bipindensis (K.Schum.) Bremek. and T. precidantenna N.Hallé, which
together were sister (ML-BS = 92, BPP = 1.0) to Pavetta (MLBS = 100, BPP = 1.0). Pavetta was recovered as monophyletic
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De Block & al. • Molecular phylogenetics of Pavetteae (Rubiaceae)
Razafimandimbisonia humblotii
100/1.0
100/1.0
Mussaenda flava
Vangueria madagascariensis
Ixora sp.
Tricalysia semidecidua
Oxyanthus troupinii
Gardenia rutenbergiana
Euclinia longiflora
Nichallea soyauxii
100/1.0
Rutidea membranacea
92/1.0
100/1.0
Clade I
Rutidea fuscescens
Rutidea orientalis
71/0.79
Rutidea parviflora
100/0.94
57/0.54
Rutidea seretii
94/1.0 Rutidea olenotricha
91/1.0
Rutidea dupuisii
Rutidea ferruginea
72/1.0
98/1.0
Rutidea decorticata
Leptactina leopoldisecundi
Leptactina involucrata
100/1.0 66/0.93 Dictyandra arborescens
Leptactina mannii
Clade II
62/0.99
Leptactina pynaertii
Pavetteae
100/1.0
Leptactina delagoensis
*/0.51
Leptactina papyrophloea
Leptactina epinyctios
74/1.0
Leptactina benguelensis Continental
76/0.95
Africa
70/1.0
Coleactina papalis
Tarenna jolinonii
Tarenna fuscoflava
57/0.95
Tarenna lasiorachis
89/1.0
Tarenna nitidula
100/1.0 93/1.0
95/1.0
Tarenna pallidula
Clade III
Tarenna vignei
Tarenna roseicosta
70/1.0
Cladoceras subcapitatum
81/1.0
Tarenna pembensis
65/0.66
98/1.0
76/1.0
Tarenna precidantenna
Tarenna bipindensis
51/0.50
82/1.0
Pavetta tetramera
92/1.0
Pavetta suffruticosa
85/0.98
Pavetta ternifolia
100/1.0
Pavetta hymenophylla
Pavetta sp. A (FTEA)
100/1.0
100/1.0 100/1.0 Pavetta tarennoides
Pavetta sansibarica
Pavetta schumanniana
Pavetta stenosepala
67/0.78
55/0.91
Pavetta batesiana
Pavetta vaga
74/1.0
Australia
Pavetta agrostiphylla
65/0.53
Pavetta indica
Asia
80/0.96
Pavetta sp. B
71/0.99
Pavetta sp. C
Continental
Tennantia sennii
Africa
Tarenna alpestris
54/0.95 * /0.98
100/1.0
Tarenna asiatica
Tarenna flava
Tarenna leioloba
88/1.0
75/0.97
Tarenna rhypalostigma
Asia/Pacific
Tarenna microcarpa
94/1.0
* /0.96
Tarenna sambucina
97/1.0
Tarenna gracilipes
* /0.90
Tarenna attenuata
Clade IV
* /0.59
Tarenna depauperata
60/0.73
Coptosperma graveolens
Continental
Coptosperma peteri
Africa
100/1.0 Homollea perrieri
Homollea longiflora
* /0.78 * /0.84
Paracephaelis tiliacea
Homolliella sericea
96/1.0
Paracephaelis cinerea
58/0.66
* /0.55
Paracephaelis saxatilis
90/0.93
100/1.0
Robbrechtia grandifolia
Madagascar
Robbrechtia milleri
* / 98/1.0
Tarenna spiranthera
Tarenna grevei
* /0.86 0.77
92/1.0
Tarenna capuroniana
93/1.0
Tarenna alleizettei
Tarenna uniflora
51/0.81
Tarenna thouarsiana
97/1.0
Coptosperma supra-axillare
Fig. 2. BI phylogram of Pavetteae and outContinental Africa
Coptosperma nigrescens
+ Madagascar
group dataset using rps16, trnT-F and ITS
90/0.71
Coptosperma nigrescens
100/1.0
Coptosperma sp. D
sequences. Bayesian posterior probabili95/1.0
Coptosperma sp. E
97/1.0
Madagascar
ties and maximum likelihood bootstrap
Coptosperma madagascariense
* /0.97 69/0.99
Coptosperma sp. A
support are indicated. An asterisk (*)
Coptosperma littorale
Continental Africa
52/0.56
indicates nomenclatural types; names in
Coptosperma sp. B
82/0.99
Coptosperma
sp.
C
bold indicate type species of synonymized
52/0.64
Madagascar
* /0.85
Schizenterospermum rotundifolium
76/1.0
genera. Abbreviations: FTEA, Flora of
91/1.0
Schizenterospermum grevei
Mascarenes
tropical East Africa.
Coptosperma borbonica
* /0.65
*
*
**
*
*
*
*
*
**
*
*
**
*
84
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and so was P. subg. Dizygoon Bremek. (P. tetramera (Hiern)
Bremek., P. suffruticosa K.Schum.: ML-BS = 82, BPP = 1.0).
Pavetta subg. Baconia Bremek. (P. hymenophylla Bremek.,
P. ternifolia Hiern: ML-BS = 85, BPP = 0.98) and subg.
Pavetta were also recovered as monophyletic in this study, but
only few representatives of these subgenera were included so
their monophyly is not certain. The Asian species of Pavetta
(P. agrostiphylla Bremek., P. indica L., P. sp. B, P. sp. C)
formed a monophyletic group (ML-BS = 80, BPP = 0.96). The
Australian P. vaga S.T.Reynolds formed a weakly supported
clade with P. batesiana Bremek. from continental Africa
(ML-BS = 55, BPP = 0.91).
Clade IV (ML-BS = 97, BPP = 1.0) comprised the East
African monospecific Tennantia, the Paleotropical Tarenna,
the Madagascan endemics Homollea, Homolliella, Robbrechtia
and Schizenterospermum and the Madagascar-centered Paracephaelis Baill. and Coptosperma (also present in East Africa
and the islands of the western Indian Ocean). Mostly, the
nodes in this clade were poorly supported and the relationships between subclades remained unclear. In the first subclade, Tennantia was weakly supported as sister to the rest of
the subclade (ML-BS = 54, BPP = 0.95), comprising the Asian
and Pacific Tarenna species. The second subclade consisted of
Madagascan and Madagascar-centred genera (ML-BS < 50,
BPP = 0.78). Homollea (ML-BS = 100, BPP = 1.0) and Robbrechtia (ML-BS = 100, BPP = 1.0) were each supported as
monophyletic. Homolliella and Paracephaelis formed a wellsupported clade (ML-BS = 96, BPP = 1.0), with Homolliella
sericea Arènes nested within Paracephaelis. The Madagascan
Tarenna species were a well-supported monophyletic group
(ML-BS = 93, BPP = 1.0), comprising three main lineages:
T. spiranthera (Drake) Homolle, T. capuroniana De Block and
T. grevei (Drake) Homolle (ML-BS = 98, BPP = 1.0); T. uniflora
(Drake) Homolle and T. thouarsiana (Drake) Homolle (ML-BS
= 97, BPP = 1.0); and, T. alleizettei (Dubard & Dop) De Block,
weakly supported as sister to the latter two species (ML-BS
= 51, BPP = 0.81). The Afro-Madagascan Coptosperma was
not recovered as monophyletic. The BI analysis showed that
the type of the genus name, C. nigrescens Hook.f., formed
a monophyletic group with all sampled Madagascan Coptosperma species, C. littorale (Hiern) Degreef from East Africa
and C. borbonicum (Hend. & Andr.Hend.) De Block from the
Comores (BPP = 0.97). In the ML analysis, the same group was
recovered, with the exceptions of C. supra-axillare (Hemsl.)
Degreef and C. borbonicum (ML-BS = 69, BPP = 0.99). In both
analyses the Madagascan endemic Schizenterospermum was
nested within the Coptosperma group comprising C. nigrescens. The continental African C. graveolens (S.Moore) Degreef
and C. peteri (Bridson) Degreef were unresolved.
Our results clearly showed the polyphyly of the large genus
Tarenna. The type, T. asiatica (L.) Kuntze ex K.Schum., was
situated in the Asian-Pacific subclade of clade IV. The Madagascan representatives of Tarenna were more closely related
to Coptosperma, Paracephaelis and other Madagascan genera
in the second subclade of clade IV than to the Asian-Pacific
Tarenna. The continental African Tarenna were more closely
related to Cladoceras and Pavetta in clade III.
DISCUSSION
Monophyly and main lineages of the Pavetteae. — Our
study, the first to include all but two of the currently recognized
genera of the Pavetteae (see Table 1 for a complete list), supports
a monophyletic tribe Pavetteae in agreement with earlier studies (Andreasen & Bremer, 2000 ; Robbrecht & Manen, 2006;
Bremer & Eriksson, 2009). It also supports the current circumscription of the Pavetteae, notably sensu De Block (2003b)
(Table 1). While the circumscription of the tribe as a whole is
supported, several genera are not monophyletic as currently
delimited.
We retrieved four main clades, all strongly supported in
both BI and ML analyses. However, phylogenetic relationships
among these lineages remained largely unresolved. Clades I
and II were restricted to continental Africa and respectively
comprised the genera Rutidea/Nichallea and Coleactina/Dictyandra/Leptactina. Clade III comprised the continental African
Cladoceras and Tarenna species and the paleotropical Pavetta.
Clade IV was the most heterogeneous with respect to geographic distribution; it comprised eastern and southern African (Tennantia, Paracephaelis, Coptosperma), Asian-Pacific
(Tarenna), Madagascan (Coptosperma, Homollea, Homolliella,
Paracephaelis, Robbrechtia, Schizenterospermum, Tarenna)
and western Indian Ocean island elements (Tarenna, Paracephaelis, Coptosperma).
Finding morphological synapomorphies for these four
clades was not simple. Clade I comprised species with an
incompletely bilocular ovary with two basally attached ovules
and a unilocular fruit with a single, partially or completely
ruminate seed. While fruits with a single ruminate seed also
occur in some Afro-Madagascan taxa such as Coptosperma,
the placentation in the latter is always different. Taxa in clade
II were chacterized by large stipules, large and accrescent
calyx lobes, well-developed flowers with pubescent corollas, massive placentas with numerous ovules, numerous small
angular seeds with entire endosperm and (3–)4-colporate pollen grains. Within the Pavetteae, 4-colporate pollen grains are
only present in one other species, Cladoceras subcapitatum.
Clades III and IV were more difficult to characterize. Species
of clade III were characterized by two to several seeds per
fruit, seeds with a large adaxial hilar cavity, entire endosperm
and exotestal cells with thickenings along the outer tangential
wall. This combination of characters is by no means exclusive
for clade III, but also present in Tennantia and in the Asian/
Pacific and Madagascan species of Tarenna in clade IV. Clade
IV encompassed most of the morphological variation of the
tribe, with seed number per fruit ranging from one to numerous, seed shape varying from angular to spherical or laterally
flattened, exotesta cells parenchymatic or with thickenings,
etc. No morphological synapomorphies can be identified at
this point.
It is premature to propose a subtribal classification for
the Pavetteae, since the relationships between the four main
clades retrieved in our analysis cannot yet be ascertained and
the clades not unambiguously characterized by morphological features.
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Relationships and circumscriptions of the genera of the
Pavetteae. — Of the 15 genera studied, 6 were supported as
Coleactina, Dictyandra and Leptactina (clade II). — This
study included 8 of approximately 20 species attributed to
Leptactina, 1 of the 2 Dictyandra species, as well as Coleactina papalis. Coleactina, Dictyandra and Leptactina formed
a strongly supported monophyletic group. This corroborates
earlier morphological observations that considered Coleactina, Dictyandra and Leptactina as closely related (Robbrecht,
1984; De Block & Robbrecht, 1997, 1998). In our study, Coleactina was nested within Leptactina. It can therefore not be
retained as a separate genus, but must be considered a synonym
of Leptactina. As for Dictyandra, while the type D. arborescens grouped with the type of Leptactina, the support was
not very high (ML-BS = 66, BPP = 0.93). Therefore, its exact
position within Leptactina could not be ascertained. Based
on morphological characters, however, Dictyandra is here
placed in synonymy with Leptactina.
Originally, Dictyandra was distinguished from Leptactina
based on a number of flower characters such as, e.g., multilocellate anthers (Hooker, 1871, 1873). With the inclusion of more
species in Leptactina and Dictyandra, it became evident that
the flower characters used to distinguish the two genera were
not clear-cut. As a pragmatic solution, Robbrecht (1984) retained
Dictyandra as a small satellite genus of Leptactina based on
differences in corolla tube length (much longer than the lobes
in Leptactina, shorter than or equal to the lobes in Dictyandra).
Coleactina was described as a separate genus because
of its axillary, opposite, uniflorous inflorescences, 6–7-merous flowers, well-developed calyx tube (ca. 2 cm long), large
stipules (≥ 4 cm long) forming an involucre together with the
inflorescence-supporting leaves, and the presence of a second—small—involucre surrounding the ovary (Hallé, 1970).
In our study, C. papalis, a monocaul dwarf up to 1.5 m tall
of the humid lowland forests of west central Africa, grouped
together with L. benguelensis and L. epinyctios Bullock ex
Verdc., which are geofrutices up to 75 cm tall from the dry
savanna woodland (miombo) in eastern Africa.
The inclusion of Coleactina and Dictyandra in Leptactina
is supported by stipule, placentation (De Block & Robbrecht,
1997), seed, seed-coat and pollen characters (Hallé, 1970;
Robbrecht, 1984; De Block & Robbrecht, 1998). Furthermore,
several characters used to differentiate between the genera are no
longer considered valid. For Dictyandra, this is the case for the
length difference between corolla tube and lobes and the multilocellate anthers (Neuba, 2006). For Coleactina, the axillary,
uniflorous inflorescences are also present in, e.g., L. deblockiae
Neuba & Sonké (Neuba & al., 2006). Other characters, such as
the well-developed calyx tube and the involucre surrounding the
ovary, can be considered apomorphies for C. papalis.
Leptactina as newly delimited here can easily be recognized by large stipules, large pubescent corollas, welldeveloped calyces, massive placentas with numerous ovules,
large bilocular fruits (up to 3 cm long) with many small angular
seeds and (3–)4-colporate pollen grains.
monophyletic and their generic delimitation was corroborated. Of these, only Rutidea and Nichallea (clade I) belonged
to a well-resolved clade. Pavetta (clade III), Homollea, Robbrechtia and Tennantia (clade IV) belonged to less-resolved
clades. Nevertheless, support for these genera was high and
they are well characterized morphologically. Leptactina and
Paracephaelis were shown to be paraphyletic unless smaller
genera are included: Coleactina in Leptactina, Homolliella in
Paracephaelis. Tarenna was shown to be polyphyletic and the
delimitation of the Afro-Madagascan Coptosperma remained
unclear with the genus not recovered as monophyletic.
Rutidea and Nichallea (clade I). — This study investigated
10 of 22 species of the tropical African Rutidea as well as the
widespread West and west central African Nichallea soyauxii
(Hiern) Bridson, the only representative of Nichallea. Rutidea
was supported as monophyletic and as sister to Nichallea. This
corroborates the close relationship between the two genera as
already proposed by Bridson & Robbrecht (1985) and De Block
(1995) using morphological characters.
Nichallea and Rutidea share a unique type of placentation
within Pavetteae (De Block, 1995). The ovary is bicarpellate
but incompletely bilocular due to an incomplete septum. Each
locule has a single, basally attached, semi-campylotropous
ovule. Because of the abortion of one ovule/locule, the drupaceous fruits have a single ovoid, ruminate seed. The exotesta
cells are parenchymatic. This fruit and seed type is common
in the Madagascan representatives of Pavetteae (clade IV), and
occurs, e.g., in Coptosperma, which is also present in continental Africa.
While closely related, there are enough morphological
differences to keep Nichallea and Rutidea separate, notably
lianescent (Rutidea) versus shrubby (Nichallea) habit, pubescent (Rutidea) versus glabrous (Nichallea) leaves and inflorescences, compact (Rutidea) versus lax (Nichallea) inflorescences, small (Rutidea) versus larger (Nichallea) flowers,
completely ruminate (Rutidea) versus incompletely ruminate
seeds (Nichallea: rumination restricted to the area around the
hilar cavity; Bridson, 1978a, b) and a somewhat different pollen
type (sexine rugulate to microreticulate in both genera except
in R. dupuisii De Wild., the sexine of which is reticulate, but
muri grooved longitudinally and columellae equal in height in
Rutidea versus muri not grooved longitudinally but undulating
as a result of height difference in the columellae in Nichallea:
De Block & Robbrecht, 1998).
Two sections, Rutidea sect. Tetramera (R. fuscescens,
R. membranacea) and sect. Rutidea (all other species included
in this study), are recognized within Rutidea. They are distinguished based on, e.g., flower merosity (4-merous in sect.
Tetramera versus 5-merous in sect. Rutidea) and stigma type
(ovate to globose in sect. Tetramera versus fusiform to clavate
in sect. Rutidea; Bridson, 1978a). Our analysis showed sect.
Rutidea to be monophyletic but this was not the case for sect.
Tetramera. A more in-depth study of Rutidea comprising the
third species of sect. Tetramera is necessary to clarify the status
of this section.
86
Tarenna, Pachystylus, Triflorensia (clades III and IV). —
Tarenna, as traditionally circumscribed (e.g., Bridson, 1979;
Smith & Darwin, 1988), consists of approximately 200 species, occurring in continental Africa, Madagascar, the western
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De Block & al. • Molecular phylogenetics of Pavetteae (Rubiaceae)
Indian Ocean islands, Asia and the Pacific region. Recently,
the circumscription of Tarenna was emended by the transfer to
Coptosperma of all African, Madagascan and western Indian
Ocean island species possessing fruits with a single, usually
ruminate seed (Degreef & al., 2001; De Block & al., 2001). Even
in this narrower sense, Tarenna remains variable in certain
morphological characters, such as flower, fruit, seed and pollen types (De Block & Robbrecht, 1998; De Block & al., 2001),
which has raised questions as to its delimitation (e.g., Bridson,
1979; Smith & Darwin, 1988; De Block & al., 2001).
In the present study, we included 26 Tarenna representatives, 10 from continental Africa, 6 from Madagascar, and 10
from Asia and the Pacific. Our phylogeny showed that Tarenna
was not monophyletic as currently delimited, since representatives occurred in both clades III and IV. They formed three
geographically separate groups. The Madagascan and AsianPacific representatives each formed a monophyletic group,
with the latter group containing the type of the genus name,
T. asiatica. The continental African representatives, however,
were paraphyletic with respect to Pavetta and Cladoceras. The
relationship between the Asian/Pacific and the Madagascan
Tarenna species remained unresolved, but it was clear that the
continental African species must be excluded from Tarenna.
The polyphyly of Tarenna was previously suggested by
Bridson (1979) and Smith & Darwin (1988), based on morphological characters. Over the years, Tarenna seems to have
become the “dustbin genus” of Pavetteae, comprising species
with different flower, fruit, seed, seed coat, placentation and
pollen types. Because of the wide distribution and the large size
of the genus, studies have been restricted to limited geographic
regions (e.g., Jérémie, 1974; Bridson, 1988, 2003a; Reynolds
& Forster, 2005; Degreef, 2006), with no one evaluating the
variation in the entire genus. Our analysis clearly showed that
in the future the name Tarenna should not be used for species
from continental Africa. At least one morphological character
supports this redelimitation of Tarenna: exotesta cell shape.
The Asian/Pacific and Madagascan species have exotestal cells
with straight walls, whereas (most) continental African species
have exotestal cells shaped like puzzle pieces with the cell walls
wavy near the surface and straight near the endosperm (Robbrecht & Bridson, 1984; De Block & al., 2001).
More than 140 species of Tarenna occur in Asia and the
Pacific region. Therefore, our sampling of 10 species was
too limited to infer the delimitation of and the relationships
between taxa (generic and infrageneric). Also, two small genera
closely related to Tarenna, Pachystylus and Triflorensia, were
not included in this study because of lack of sequence data.
The New Guinean Pachystylus is unusual in having unisexual
flowers but has been considered closely allied to (Bremekamp,
1934) or part of Tarenna (Valeton, 1926). The Australian Triflorensia comprises three species that were only recently transferred from Tarenna (Ali & Robbrecht, 1991) based on, amongst
other characters, the two ovules/seeds per locule (versus 3 to
many), the 4- or 5-merous flowers (versus 5-merous) and the
inflorescence branches terminated by 3-flowered dichasial
cymes (versus not terminated by 3-flowered dichasial cymes;
Reynolds & Forster, 2005). According to Reynolds & Forster
(2005) the genus may also be represented in New Caledonia
and they suggest Tarenna microcarpa (Guillaumin) Jérémie
(included in our study) as a possible species to be transferred
to Triflorensia.
Recently, in a study of the tribe Gardenieae, Mouly & al.
(2014) found that Pelagodendron vitiense Seem. from Fiji was
closely related to Tarenna. They suggested inclusion of Pelagodendron Seem. in the tribe Pavetteae. Previously, the genus
was considered a synonym of Aidia Lour. and placed in the
Gardenieae. Pelagodendron vitiense posesses pseudo-axillary
inflorescences, a calyx that completely encloses the corolla in
bud and eventually ruptures into two or three broad lobes, and
seeds that are embedded in placental pulp, all characters absent
or unusual in the Pavetteae. Since Mouly & al. (2014) only
sampled one of the three species of Pelagodendron, and since
we have not been able to examine material of the genus, we only
mention Mouly & al.’s (2014) finding without commenting on it.
The Madagascan Tarenna species in clade IV formed a
monophyletic group (ML-BS = 93, BPP = 1.00) within the
unresolved, predominantly Madagascan clade. Two subclades
were well supported as monophyletic groups, each characterized by different morphological characters: T. thouarsiana and
T. uniflora (ML-BS = 97, BPP = 1.00) have partially exserted
stigmas and anthers and microreticulate or reticulate pollen
without supratectal elements but with undulating sexine as a
result of different columellae heights (De Block & al., 2001)
whereas T. capuroniana, T. spiranthera and T. grevei (ML-BS
= 98, BPP = 1.00) possess flowers with long-exserted stigmas
and anthers. The pollen is microreticulate without supratectal
elements in T. capuroniana and T. spiranthera and perforate
with supratectal elements in T. grevei (De Block & al., 2001).
This last species is also characterized by 4-merous flowers
and a single ovule/seed per locule, characters which, within
Tarenna, are only found in the closely related T. sechellensis (Baker) Summerh. from the Seychelles and the Comoros.
Tarenna alleizettei differs from all other Madagascan species
by its short flowers and microreticulate pollen without supratectal elements.
The group of 10 continental African Tarenna species (of
42 species in total; clade III) was paraphyletic with respect to
Cladoceras and Pavetta. Most species grouped with Cladoceras subcapitatum (ML-BS = 93, BPP = 1.00), the only species
of the East African Cladoceras (Bremekamp, 1940; Verdcourt,
1988b). Cladoceras subcapitatum was considered closely
related to Tarenna (Bridson, 1979; Robbrecht & Bridson, 1984)
but was placed in a genus of its own because of the presence
of spines and the absence of secondary pollen presentation
(Bremekamp, 1940). However, the species is similar in habit to
the East African Tarenna junodii (Schinz.) Bremek., wich has
secondary pollen presentation but no spines. Furthermore, fruit
and placentation characters of Cladoceras are identical to those
of the continental African Tarenna species. Also, C. subcapitatum possesses the same puzzle-shaped exotestal cells as present
in the continental African Tarenna species it grouped with.
This seed-coat type is further only present in Leptactina and
Pavetta (De Block & al., 2001). The identical fruit, placentation
and exotestal cell characters certainly support the merging of
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continental African Tarenna with Cladoceras. The absence
of secondary pollen presentation in Cladoceras subcapitatum
should not contradict such merger. As Verdcourt (1988b) stated,
“reduced forms of the secondary pollination mechanism could
be evolved easily”. In fact, another Pavetteae genus, Leptactina, also comprises species with and without secondary pollen
presentation (Puff & al., 1996). The only remaining difference
is in the pollen, which is (3–)4-colporate in C. subcapitatum
versus 3-colporate in the continental African Tarenna. We do
not see this as an obstacle to transfer certain continental African Tarenna species to Cladoceras.
However, other Tarenna species seem to represent separate
lineages. This is the case for Tarenna jolinonii (Hallé, 1970),
which fell separate from the other continental African Tarenna
species and was weakly supported as sister to the rest of clade
III (ML-BS = 65, BPP = 0.66). While most of its characters
fit well within Tarenna (e.g., 5-merous flowers, large axillary
placentas with 12–15 embedded ovules, angular seeds with
a deep hilar cavity), T. jolinonii differs from all other continental African Tarenna species by having large foliaceous
stipules (up to 3.5 cm long). These stipules are different from
the smaller stipules of the other species that have triangular or
ovate, truncate or aristate sheaths, which are often blackened
in the central area when dry (Hallé, 1970; Bridson, 1988, 2003a;
Degreef, 2006). Furthermore, the exotesta of T. jolinonii has
straight-walled cells rather than the puzzle-shaped cells present
in Cladoceras subcapitatum and the species grouping with it
(De Block, pers. obs.).
The last two Tarenna species included in this study are
the sister species T. bipindensis and T. precidantenna, which,
together, formed the sister group of Pavetta. This relationship
was well supported (ML-BS = 92, BPP = 1.00) but puzzling,
because the two species certainly do not resemble Pavetta in
their characters (e.g., 5-merous versus 4-merous flowers in
Pavetta, up to six seeds versus two seeds per fruit in Pavetta).
Tarenna bipindensis and T. precidantenna possess exotestal
cells with wavy cell walls as is the case for the other continental African Tarenna species (excepting T. jolinoni) and
for the Pavetta species. At present, the position of these two
continental African Tarenna species as sister to Pavetta cannot
be explained. It should be noted, though, that three different
samples of T. precidantenna were analysed in order to exclude
sequencing errors.
Based on the present results, the continental African species must be excluded from Tarenna. At least two options are
possible. The first option would require the amalgamation of
continental African Tarenna and Cladoceras with Pavetta.
Similarities in certain characters would support this inclusion, e.g., both groups have seeds with an adaxial excavation
surrounded by a thickened annulus and exotestal cells with
mostly continuous thickenings along the outer tangential wall
but containing channels to the cell lumina (Robbrecht, 1984).
However, there are important differences between Pavetta
and continental African Tarenna and Cladoceras: e.g., presence versus absence of bacterial leaf galls, 4-merous versus
5-merous flowers, one versus several ovules per locule (but
exceptions do occur: e.g., Tarenna burttii Bridson possesses a
single ovule per locule and species of Pavetta subg. Dizygoon
possess two ovules per locule. However, together these two
groups represent less than 10 species of a total of ca. 560 in
Tarenna and Pavetta). The inclusion of continental African
Tarenna and Cladoceras would make the genus Pavetta heterogeneous and is therefore not desirable. We prefer a second
option in which most of the continental African Tarenna species are transferred to the hitherto monospecific Cladoceras.
However, two additional continental African Tarenna lineages
(T. jolinonii and T. bipinensis/T. precidantenna) were retrieved
in our analysis. We therefore plan a more extensive molecular
and morphological study of the continental African Tarenna
species in order to clarify relationships within this group before
making nomenclatural changes. Further study is also needed
to clarify relationships between the Madagascan and AsianPacific species of the genus and the relationships within the
Asian-Pacific clade.
Pavetta (clade III). — Pavetta, as traditionally delimited,
includes ca. 360 species. It is the largest genus of the Pavetteae
and has a paleotropical distribution, although it is absent from
Madagascar. Pavetta species are easily recognised by their
4-merous flowers, stigmatic lobes fused over most of their
length, single ovule per locule and hemispherical seeds with a
large adaxial hilar cavity. Typical is the presence of bacterial
leaf galls (in ca. 85% of the species; Miller, 1990; Lemaire
& al., 2012).
Pavetta was extensively studied by Bremekamp (e.g.,
1934, 1939a, b), who recognized three subgenera. As presently
circumscribed, subg. Pavetta, subg. Baconia and subg. Dizygoon are well defined morphologically, notably by flower,
fruit (Bremekamp, 1934, 1939a, b) and pollen type (De Block
& Robbrecht, 1998). Most distinct are the west central African species of subg. Dizygoon, which differ from all other
Pavetta species by having short anthers (versus long anthers),
two collateral ovules per locule (versus one ovule per locule),
red fruits (versus black) and pollen with reticulate sexine and
no supratectal elements (versus pollen with microreticulate to
perforate sexine, with supratectal elements in Pavetta, without
supratectal elements in Baconia; De Block & Robbrecht, 1998).
Subgenus Baconia is restricted to continental Africa, subg.
Pavetta is paleotropical (but absent in Madagascar).
In our study we included 15 species of Pavetta: 10 from
Africa, 1 from Australia (P. vaga) and 4 from Asia (P. agrostiphylla to P. sp. C; Fig. 2). Subgenus Pavetta was represented
by 10 species of a total of approximately 300, subg. Baconia
by 2 species of approximately 60 and subg. Dizygoon by 2 of
4 species. Pavetta was recovered as monophyletic in its current circumscription and so was subg. Dizygoon (P. tetramera,
P. suffruticosa). Subgenus Baconia (P. ternifolia, P. hymenophylla) and subg. Pavetta (P. tarennoides to P. sp. C.) were
recovered as monophyletic only if P. sp. A of Flora of Tropical
East Africa (Bridson, 1988) is considered part of subg. Pavetta.
However, the taxonomic placement of P. sp. A is difficult since
no flowering material is available, which makes it impossible
to score important distinguishing characters (corolla length,
style length, throat bearded or not). Bridson (1988, 2001)
listed P. sp. A as new and poorly known but closely related
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(morphologically) to P. roseostellata Bridson, a species which
resembles those of subg. Baconia by the short corolla tube, the
bearded throat and the short style (table 2 in Bridson, 2001).
Therefore, Bridson placed the two species “very provisionally”
(2001: 573) in subg. Baconia, while at the same time stressing
that they differ from members of Baconia in inflorescence position: terminal on very short lateral branches versus terminal
on normal-length lateral branches. Bridson further suggested
the two species may eventually need to be accommodated in a
new genus. Because of the incomplete knowledge of P. sp. A
and because the subgenera Pavetta and Baconia were represented by only a few species in our study, it was impossible to
confirm their monophyly.
Within the paleotropical subg. Pavetta, the Asian taxa
(P. agrostiphylla, P. indica, P. sp. B, P. sp. C) formed a monophyletic group. The Australian P. vaga was not included in
the Asian clade but formed a weakly supported clade with the
African P. batesiana. The monophyly of Pavetta has previously been questioned by Bremekamp (1934: 20) who stated
that subg. Dizygoon comprises “a group of species which are
so markedly different from all others [Pavetta] that it is questionable whether they would not be more at home in a genus of
their own”. Our results showed that Dizygoon is the sister lineage to the rest of Pavetta and therefore support the distinction
between subg. Dizygoon and the rest of the genus. A further
study including more Pavetta representatives and more genetic
markers, and taking into account morphology, is necessary to
ascertain the monophyly of subgenera Baconia and Pavetta,
the taxonomic status of P. sp. A and P. roseostellata and the
taxonomic rank of Dizygoon.
Tennantia (clade IV). — In our study, this East African
monospecific genus was well-supported as a member of the
predominantly Madagascan/Asian/Pacific clade IV and weakly
supported as sister to the Asian-Pacific Tarenna species. In
the past, Tennantia sennii (Chiov.) Verdc. & Bridson was considered closely related to Tarenna, but placed in a separate
genus because of its distinctive characters, such as its clavate,
winged stigma, corolla tube half as long as the corolla lobes
and seeds shaped like segments of an orange, with a groove on
each side of the hilar cavity (Verdcourt, 1981, 1988a). Bridson
& Robbrecht (1985) also considered Tennantia to be closely
related to Tarenna, mainly because of the similar seed-coat
structure and exotestal thickenings.
Our results do not support a close relationship between
Tennantia and the continental African Tarenna species (clade
III), but rather between Tennantia and the Asian-Pacific
Tarenna species. This grouping is corroborated by the fact that
both Tennantia (Verdcourt, 1981; Bridson & Robbrecht, 1985)
and the Asian-Pacific Tarenna species (De Block & al., 2001)
have exotesta cells with straight walls. Furthermore, Tennantia
seeds show intrusions of the seedcoat in the endosperm on the
lateral surfaces, which is a form of superficial rumination.
Superficially ruminate seeds are characteristic for one group
of Asian-Pacific Tarenna species, including T. asiatica, the
type of the genus name. Further morphological and molecular
studies are needed to unravel the precise relationship between
Tennantia and the Asian-Pacific Tarenna species.
Homollea, Homolliella and Paracephaelis (clade IV). — In
this study we included two species of Homollea, the monospecific Homolliella and three Paracephaelis species. These
three genera form a morphologically distinct group within
the Pavetteae. They can readily be distinguished by laterally
flattened seeds with a shallow linear hilum and entire endosperm, two to seven ovules arranged on the periphery of the
placenta (Capuron, 1973; De Block, unpub. data) and by pollen
with supratectal microgemmae. The occurrence of supratectal
elements is rare within Pavetteae and otherwise only seen in
Pavetta subg. Pavetta (absent from Madagascar), in the AfroMadagascan Coptosperma nigrescens and in a few Madagascan Tarenna species (De Block & Robbrecht, 1998; De Block
& al., 2001). The placentation and seed types in the three genera
are not found in any other Pavetteae.
Bridson & Robbrecht (1985) tentatively included Homollea,
Homolliella and Paracephaelis in the Pavetteae, a position which
is corroborated by our study. Because of their distinctive morphological characters, the three genera were considered closely
related (Bridson & Robbrecht, 1985; De Block, 1997). In our
study, this close relationship was confirmed for Homolliella and
Paracephaelis, which formed a monophyletic group. Homollea
was also retrieved as a monophyletic lineage but its relationship
with the Paracephaelis-Homolliella clade remained unresolved
(a sister relationship is weakly supported in the BI analysis:
BPP = 0.84). Our results suggest the inclusion of Homolliella
in Paracephaelis, a finding that was already proposed (but
not published) by Capuron (1973). However, Capuron considered Homollea, Homolliella and Paracephaelis synonymous
with Tarenna in Madagascar because of the seeds with entire
endosperm. Within Tarenna, he recognized five sections, with
Homollea and Paracephaelis (including Homolliella) among
them. Our study does not support the congenerity of Homollea
and Paracephaelis (including Homolliella) with the Madagascan
Tarenna species. We therefore keep them at generic rank.
Next to a similar placentation and seed type, Homolliella
and Paracephaelis share the following characters: vegetative
parts pubescent; flowers densely pubescent, inflorescences
terminal on lateral branches, sessile. The only differences are
quantitative: a well-developed calyx with the calyx tube much
longer than the lobes and large flowers and fruits in H. sericea
versus a less-developed calyx with the lobes longer than or
equal in length to the tube and small flowers and fruits in Paracephaelis. Based on morphological characters, Homolliella can
easily be accommodated within Paracephaelis.
Homollea differs from the Paracephaelis-Homolliella
clade by the absence of pubescence in the vegetative and generative parts (except in H. perrieri Arènes), the pseudoaxillary
position of the pedunculate inflorescences and the corolla tube,
which is much longer than the corolla lobes. All three Homollea species have long, narrow calyx lobes but this character is
also encountered in some, as yet undescribed, Paracephaelis
species (De Block, pers. obs.).
Coptosperma and Schizenterospermum (clade IV). —
Coptosperma was recently reinstated (De Block & al., 2001;
Degreef & al., 2001) to accomodate African, Madagascan
and western Indian Ocean island species previously placed in
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Tarenna (Bridson, 1988), and characterized by a single, usually
ruminate seed per fruit, Hitherto, Coptosperma was a monospecific genus, only comprising C. nigrescens. Upon reinstatement, however, it was emended to include Zygoon Hiern and
Enterospermum Hiern, the species of which also possess fruits
with a single, usually ruminate seed. In the present paper, the
name Coptosperma is always used in this emended sense.
Coptosperma comprises approximately 40 species endemic
to Madagascar (mostly undescribed: De Block, unpub. data),
9 species endemic to eastern and southern Africa and 2 species
endemic to the Mascarenes. A further 2 species, C. nigrescens,
the type, and C. supra-axillare, occur in Madagascar, continental Africa and the western Indian Ocean islands (Bridson,
1979, 1988; De Block & al., 2001; Degreef & al., 2001). Schizenterospermum is a genus of 4 species, restricted to the dry forest
and scrub vegetation of western and northwestern Madagascar
(Arènes, 1960). Species of Coptosperma and Schizenterospermum typically have multiflorous, often compact inflorescences
with small (4–)5-merous white flowers and unilocular fruits
with a single ruminate seed. Morphological characters that
show variation within this group of species are, e.g., stipule
shape (triangular with apiculate tip, ovate with rounded tip, …),
placentation (ovules immersed in or pendulous from placenta),
and degree of rumination of the seed (endosperm completely
or partly ruminate or entire).
We included 12 species of Coptosperma and 2 of Schizenterospermum, all of which fell in the predominantly Madagascan clade IV. In the past, Coptosperma was often considered
a synonym of Tarenna, notably by botanists focusing on continental African Pavetteae, where ruminate endosperm is rare
(Hiern, 1877; Bremekamp, 1934; Bridson, 1979, 1988). However,
more than 60% of the Madagascan species of the Pavetteae
have seeds with ruminate endosperm. Botanists studying Madagascan Pavetteae therefore attributed great importance to this
character, placing species with two or more seeds and entire
endosperm in Tarenna and those with a single seed and ruminate endosperm in Coptosperma (as Enterospermum; Homolle,
1938; Capuron, 1973). Our study favours this last view and corroborates the decision to separate Coptosperma and Tarenna at
genus level (De Block & al., 2001; Degreef & al., 2001).
However, we did not recover Coptosperma as a monophyletic group and the relationships between certain of its species
remained unclear, especially between the Madagascan and the
continental African species. In the BI analysis, 10 of the 12
Coptosperma and the 2 Schizenterospermum species formed a
predominantly Madagascan, monophyletic group (BPP = 0.97),
which included the type C. nigrescens (henceforth: main Coptosperma clade). In the ML analysis, the same group (ML-BS
= 70) was recovered with the exclusion of C. supra-axillare
(continental Africa, Indian Ocean islands and Madagascar) and
C. borbonicum (Mascarenes), which were unresolved. In both
analyses, two exclusively continental African species, C. graveolens and C. peteri, were also unresolved in clade IV, but a third,
C. littorale, was nested within the main Coptosperma clade.
The continental African species of Coptosperma are rather
variable in their characters, e.g., inflorescences compact (e.g.,
C. neurophylla (S.Moore) Degreef) or lax (e.g., C. nigrescens),
endosperm ruminate (e.g., C. nigrescens), partly ruminate (e.g.,
C. neurophylla) or entire (e.g., C. graveolens), inflorescences
few-flowered (e.g., C. kibuwae (Bridson) Degreef) or multiflowered (e.g., C. graveolens), etc. Bridson (1979, 1988, 2003b)
therefore recognized three informal infrageneric groups, more
or less coinciding with the historically recognized genera
Zygoon (Bridson’s group I), Enterospermum (Bridson’s group
II) and Coptosperma s.str. (Bridson’s group III). Species of
Bridson’s group I are characterized by chartaceous leaves, often
immature at the time of flowering, small and compact inflorescences born on short leafless spurs and small placentas with 3–7
pendulous ovules (Bridson, 2003b). This group includes, e.g.,
C. zygoon (Zygoon graveolens Hiern) and C. peteri. Because of
lack of material, we only included C. peteri, which was unresolved in our analysis. Bridson’s group II comprises species
characterized by the following characters: leaves coriaceous
or subcoriaceous, mature at the time of flowering; terminal
or axillary inflorescences on leafy branches, usually compact
with short pedicels; small placentas with 2–7 pendulous ovules
or large placentas with 2–3(–6) impressed ovules; and ruminate, partly ruminate or entire seeds (Bridson, 2003b). Three
species of Bridson’s group II were included in our analysis but
C. graveolens, C. supra-axillare and C. littorale did not form
a monophyletic group. Coptosperma graveolens fell alone at
the base of the entire Madagascan–western Indian Ocean–
continental African clade in clade IV. Coptosperma supraaxillare fell at the base of the main Coptosperma clade, and,
C. littorale, type of Enterospermum (Hiern, 1877), within the
main Coptosperma clade. Bridson’s group III comprises only
C. nigrescens. This species is characterized by coriaceous,
very shiny leaves, mature at the time of flowering, lax inflorescences, positioned terminally on leafy branches, long pedicels,
large placentas with three impressed ovules and seeds with
fully ruminate endosperm (Bridson, 2003b). In our analysis,
C. nigrescens grouped with C. madagascariense, which fits
well the characters of Bridson’s group III. However, these two
species also grouped with C. sp. D and C. sp. E, which possess flowers with short pedicels and small placentas with three
pendulous ovules (fitting in Bridson’s group II). Our analysis
indicated that neither Bridson’s group II nor her group III are
monophyletic. We cannot comment on Bridson’s group I since
we only included a single species in our analysis. It is clear
that further study of the continental African Coptosperma species is necessary to ascertain their taxonomic position and the
relationships between them.
Within the Madagascan representatives, C. madagascariense, type of the name of the historical genus Santalina
Baill. fell within the main Coptosperma clade. This corroborates that Santalina is congeneric with Coptosperma as
was already suggested based on morphological characters
(Homolle, 1938; Capuron, 1973; Bridson & Robbrecht, 1985;
De Block & al., 2001; Bridson, 2003; De Block, 2007).
Schizenterospermum was tentatively included in the tribe
Pavetteae by Bridson & Robbrecht (1985) and this taxonomic
decision is consistent with the results of the present study. The
two Schizenterospermum species formed a well-supported
monophyletic group nested within the main Coptosperma
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De Block & al. • Molecular phylogenetics of Pavetteae (Rubiaceae)
clade. Capuron previously suggested merging Schizenterospermum with Coptosperma (as Enterospermum) in his unpublished
treatment of the Madagascan Rubiaceae (Capuron, 1973). Morphological data also support this transfer since the main characters of the two genera, such as fruit and seed morphology, stipule morphology, placentation type, etc., are identical. The main
differences between the two genera are found in leaf shape
and texture, but seem mostly related to ecological factors, e.g.,
smaller, glabrous, persistent, coriaceous leaves in Coptosperma
versus larger, orbicular, pubescent, caducous, papyraceous/
subcoriaceous leaves in Schizenterospermum. However, with
overall support within clade IV mostly weak and Coptosperma
not retrieved as monophyletic, we prefer to postpone a decision
on the synonymisation of Schizenterospermum until more resolution and better support have been achieved. Further study is
necessary to reach conclusive insights into the delimitation of
Coptosperma, and the relationships between its Madagascan
and continental African species.
Robbrechtia (clade IV). — Robbrechtia comprises two species, both of which were included in our analysis. They were
strongly supported as a monophyletic group. However, the
relationship between Robbrechtia and the other Madagascan
genera of the Pavetteae remained obscure because of weak resolution and support. Robbrechtia is characterized by a striking
character combination, unique in the Pavetteae: sheathing stipules with intrapetiolar lobes, young shoots and inflorescence
parts covered with copious colleter exudate, long-tubed flowers with a well-developed calyx, a bilobed stigma, unilocular,
one-seeded fruits, and seeds with deeply ruminate endosperm
(De Block, 2003b). In Madagascar, fruits with a single ruminate seed also occur in Coptosperma and Schizenterospermum.
Robbrechtia differs from these genera by the stipule type, the
bilobed stigma and the much larger corollas, ovaries, calyces
and fruits. In fact, the characters of Robbrechtia are reminiscent of those of Homolliella sericea, with which it shares its
habitat but from which it differs by the unilocular fruits with
a single ruminate seed, the bilobed stigma and the sheathing
intrapetiolar stipules.
Stipules interpetiolar, large, triangular or ovate, erect or bent
back, sometimes with short needle-like awn. Inflorescences
terminal or axillary, trichotomously branched, uniflorous to
multiflorous, congested or lax, bracteose or more rarely frondose, sometimes with bracts and bracteoles fused into involucres, often all inflorescence parts including the corolla densely
pubescent. Flowers hermaphroditic, actinomorphic, 4–7-merous, pedicellate or sessile. Secondary pollen presentation present or rarely absent. Calyx well developed; tube much shorter or
rarely longer than lobes; lobes elliptic or foliaceous, up to 6 cm
long, or, rarely narrowly triangular, up to 7 mm long. Corolla
white or pale green; tube narrowly cylindrical, 1–17 cm long;
lobes contorted to the left in bud, spreading at anthesis, 1–11 cm
long. Stamens sessile or with short filaments, inserted somewhat below or at the level of the throat, entirely or for most of
their length included in the corolla tube, or rarely exserted and
spreading at anthesis; anthers linear, sometimes multilocellate.
Ovary bilocular, with numerous ovules per locule; placentation
axillary; ovules born on massive, peltate placentas attached to
the upper half of the septum. Style slender; stigma bilobed,
exserted at anthesis or included at the level of the throat or deep
in the corolla tube. Disc annular, fleshy, glabrous. Fruits drupaceous, well developed, globose, ellipsoid or oblong, bilocular
with numerous small seeds per locule; calyx persistent. Seeds
small, angular; hilar cavity round, deep, surrounded by thickened annulus; endosperm entire; exotesta cells thickened along
the outer tangential wall, thickenings containing narrow channels. Pollen grains (3–)4-colporate, supratectal elements absent.
Distribution: tropical continental Africa.
Leptactina arborescens (Welw. ex Benth. & Hook.f.) De
Block, comb. nov. ≡ Dictyandra arborescens Welw. ex
Benth. & Hook.f., Gen. Pl. 2: 85. 1873 – Holotype: Angola,
Golungo Alto, Welwitsch 2561 (BM!; isotypes: K!, P!).
Leptactina congolana (Robbr.) De Block, comb. nov. ≡ Dictyandra congolana Robbr. in Pl. Syst. Evol. 145: 114. 1984 –
Holoype: Congo, Nsah Plateau, Ngo, Makany 1768 (BR!;
isotypes: BR!, P!).
Based on the results presented in this study we formally
propose four new combinations and amend generic descriptions for two genera. Three genera are placed into synonymy.
Leptactina papalis (N.Hallé) De Block, comb. nov. ≡ Coleactina papalis N.Hallé in Aubréville & Leroy, Fl. Gabon 17:
83. 1970 – Holotype: Gabon, Moughimba, SW de Koulamotou, approximativement à mi-distance de Mbigou, Le
Testu 8356 (P!).
Leptactina Hook.f., Hooker’s Icon. Pl. 11: 73, t. 1092. 1871 –
Type (designated by Robbrecht in Pl. Syst. Evol. 145: 106.
1984): Leptactina mannii Hook.f.
= Dictyandra Welw. ex Benth. & Hook.f., Gen. Pl. 2: 85. 1873,
syn. nov. – Type: Dictyandra arborescens Welw. ex Benth.
& Hook.f.
= Coleactina N.Hallé in Aubréville & Leroy, Fl. Gabon 17: 83.
1970, syn. nov. – Type: Coleactina papalis N.Hallé.
Small trees, erect or scandent shrubs, monocaul dwarfs,
prostrate or erect geofrutices. Leaves petiolate or subsessile;
blades papyraceous to thinly coriaceous, domatia often present.
Paracephaelis Baill. in Adansonia 12: 316. 1879 – Type: Paracephaelis tiliacea Baill.
= Homolliella Arènes in Notul. Syst. (Paris) 16: 16. 1960, syn.
nov. – Type: Homolliella sericea Arènes.
Shrubs or trees, sometimes deciduous. Leaves petiolate;
blades coriaceous or rarely papyraceous, both surfaces pubescent to densely pubescent; domatia often present as hairy tufts
at the axils of secondary veins. Stipules interpetiolar, triangular
or ovate, acute to acuminate at the tip. Inflorescences terminal, sessile, trichotomously branched, multi- or pauciflorous,
congested or lax, bracteose; all inflorescence parts including
NOMENCLATURAL CHANGES
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the corolla pubescent. Flowers hermaphroditic, actinomorphic,
5-merous, pedicellate or sessile. Secondary pollen presentation
present. Calyx well developed or not; tube short and lobes as
long as or longer than the tube, or tube much longer than lobes;
lobes triangular or ovate. Corolla white; tube cylindrical or
infundibuliform, ≤ 2 cm long; lobes contorted to the left in bud,
spreading at anthesis. Stamens with short filaments inserted at
the throat, exserted at anthesis; anthers linear. Ovary bilocular, with 4–8 ovules per locule; placentation axillary; ovules
arranged along the margins of a peltate placenta attached to the
upper half of the septum. Style slender; stigma lobes fused over
most of their length, exserted at anthesis. Disc annular, fleshy,
glabrous. Fruits drupaceous, globose or ellipsoid, bilocular
with (1–)2–8 seeds per locule; calyx persistent. Seeds laterally flattened; hilar cavity linear, shallow; endosperm entire;
exotesta cells thickened along the outer tangential wall, thickenings containing 2 narrow channels. Pollen grains 3-colporate,
supratectal microgemmae present.
Distribution: Madagascar.
Scientific Research-Flanders (postdoctoral travel grant to first author
and research project G.0250.05) and the Percy Sladen Memorial Fund.
The Royal Swedish Academy of Sciences and the Swedish Research
Council supported a major part of the molecular work (grant 621-20041059 to last author).
Paracephaelis sericea (Arènes) De Block, comb. nov. ≡
Homolliella sericea Arènes in Notul. Syst. (Paris) 16: 17,
fig. 4 (19–25). 1960 – Holotype: Madagascar, Province
Toamasina, forêt d’Analamazaotra, Thouvenot in Perrier
de la Bâthie 122 (P!; isotypes: BR!, P!).
ACKNOWLEDGEMENTS
We thank the herbarium curators of the G, K, MO, P, S, TAN,
TEF, UPS and WAG herbaria for loans of specimens and for help
extended during study visits; the K, MO, TAN, UPS and WAG herbaria for supplying silica gel material or allowing the use of specimen fragments for DNA study; Aaron Davis (K), Quentin Luke
(Fairchild Tropical Botanic Garden and East African Plant Redlist
Authority), Steven Dessein (BR), Geoffrey Mwachala (EA), Frank
Van Caekenberghe (BR), Inge Groeninckx (KUL), Dominique Champluvier (BR), Ferdinand Niyongabo (BR), Jean Pierre Vande Weghe
(Wildlife Conservation Society, Gabon), Salvator Ntore (BR), Olivier
Lachenaud (BR), James Tosh (KUL), Arnaud Mouly (University of
Franche-Comté), Jan Wieringa (WAG) and Katarina Andreasen (UPS)
for collecting leaf material in silica gel; Anbar Khodanbadeh (Bergius
Foundation) and Wim Baert (BR) for help with the lab work and the
sequencing; Anja Vandeperre (KUL), Koen Geuten (KUL) and Erik
Smets (KUL) for the first author’s initiation in molecular techniques;
Steven Dessein and Frank Van Caekenberghe (BR) for the use of photographs; Liliane Tytens (BR) for making the photographic plate; Pete
Lowry (MBG) for allowing field work in Madagascar to take place
within the framework of the Madagascar Research and Conservation
Program of Missouri Botanical Garden; the MBG office staff in Antananarivo for logistic support; Madagascar National Parks, Ministère
des Eaux et Forêts and Parc Botanique et Zoologique de Tsimbazaza
(PBZT) for permission to collect in protected areas in Madagascar;
Lalao Andriamahefarivo (MBG) and Franck Rakotonasolo (TAN)
for arranging collecting and export permits; Franck Rakotonasolo
(TAN), Solo Rapanarivo (TAN) and Tiana Randriamboavonjy (K)
for help during field work. This study was supported by the Fund for
92
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Appendix 1. List of taxa used in the phylogenetic analyses with voucher information (geographic origin, collection, herbarium), EMBL accession numbers
and literature citations for previously published sequences for the two plastid markers, rps16 and trnT-trnF, and the nuclear marker ITS. FTEA: Flora of
tropical East Africa; (1) = Cortes-B. & al., 2009; (2) = Rydin & al., 2008; (3) = Bremer & Eriksson, 2009; (4) = Kainulainen & al., 2013. New sequences are
marked with *.
Tribe Alberteae Hook.f.: Razafimandimbisonia Kainul. & B.Bremer: R. humblotii (Drake) Kainul. & B.Bremer, Madagascar, Tosh & al. 263 (BR), KM592238*,
KM592145*, KM592324*. Tribe Coffeeae DC.: Tricalysia A.Rich. ex DC.: T. semidecidua Bridson, Zambia, Dessein & al. 1093 (BR), KM592279*, KM592185*,
–. Tribe Ixoreae A.Gray: Ixora L.: I. sp., Thailand, Sudde 1487 (K), KM592208*, KM592115*, –. Tribe Gardenieae DC.: Euclinia Salisb.: E. longiflora
Salisb., Africa (country unknown), Van Caekenberghe 348 (BR), KM592203*, KM592110*, –. Gardenia J.Ellis: G. rutenbergiana (Baill. ex Vatke) J.-F.Leroy,
Madagascar, Groeninckx & al. 24 (BR), KM592204*, KM592111*, KM592295*. Oxyanthus DC.: O. troupinii Bridson, Burundi, Niyongabo 115 (BR),
KM592219*, KM592126*, –. Tribe Mussaendeae Hook.f.: Mussaenda Wernham: M. flava Verdc., Africa (country unknown), Van Caekenberghe 60 (BR),
KM592217*, KM592124*, KM592306*. Tribe Pavetteae A.Rich. ex Dumort.: Cladoceras Bremek.: C. subcapitatum (K.Schum. & K.Krause) Bremek.,
Tanzania, Luke & al. 8351 (UPS), AM117290(3), KM592094*, KM592281*. Coleactina N.Hallé: C. papalis N.Hallé, Gabon, Dessein & al. 2355 (BR), KM592188*,
KM592095*, KM592282*. Coptosperma Hook.f.: C. borbonicum (Hend. & Andr.Hend.) De Block, Comores, De Block 1389 (BR), KM592189*, KM592096*,
KM592283*; C. graveolens (S.Moore) Degreef, Kenya, Mwachala 3711 (BR), KM592200*, KM592107*, KM592293*; C. littorale (Hiern) Degreef, Mozambique, Luke & al. 9954 (UPS), KM592190*, KM592097*, KM592284*; C. madagascariense (Baill.) De Block, Madagascar, Razafimandimbison & al. 577
(UPS), KM592191*, KM592098*, –; C. madagascariense (Baill.) De Block, Madagascar, De Block & al. 2238 (BR), –, –, KM592285*; C. nigrescens Hook.f.,
Madagascar, De Block & al. 535 (BR), KM592192*, KM592099*, KM592286*; C. nigrescens Hook.f., Kenya, Luke & Luke 9030 (UPS), KM592193*,
KM592100*, KM592287*; C. peteri (Bridson) Degreef, Tanzania, Lovett & Congdon 2991 (BR), KM592201*, KM592108*, KM592294*; C. supra-axillare
(Hemsl.) Degreef, Madagascar, De Block & al. 1321 (BR), KM592194*, KM592101*, KM592288*; C. sp. nov. A, Madagascar, De Block & al. 720 (BR),
KM592199*, KM592106*, KM592292*; C. sp. nov. B, Madagascar, De Block & al. 796 (BR), KM592195*, KM592102*, KM592289*; C. sp. nov. C, Madagascar, De Block & al. 1355 (BR), KM592196*, KM592103*, KM592290*; C. sp. nov. D, Madagascar, De Block & al. 704 (BR), KM592197*, KM592104*,
KM592291*; C. sp. nov. E, Madagascar, De Block & al. 733 (BR), KM592198*, KM592105*, –. Dictyandra Welw. ex Hook.f.: D. arborescens Welw. ex Hook.f.,
Ghana, Schmidt & al. 1683 (MO), KM592202*, KM592109*, –. Homollea Arènes: H. longiflora Arènes, Madagascar, De Block & al. 767 (BR), KM592205*,
KM592112*, KM592296*; H. perrieri Arènes, Madagascar, Morat 4700 (TAN), KM592206*, KM592113*, KM592297*. Homolliella Arènes: H. sericea
Arènes, Madagascar, De Block & al. 849 (BR), KM592207*, KM592114*, KM592298*. Leptactina Hook.f.: L. benguelensis (Welw. ex Benth. & Hook.f.)
R.D.Good, Zambia, Dessein & al. 1142 (BR), KM592209*, KM592116*, KM592299*; L. delagoensis K.Schum., Tanzania, Luke & Kibure 9744 (UPS),
KM592210*, KM592117*, KM592300*; L. epinyctios Bullock ex Verdc., Zambia, Dessein & al. 1348 (BR), KM592211*, KM592118*, KM592301*; L. involucrata Hook.f., Cameroon, Davis 3028 (K), KM592212*, KM592119*, KM592302*; L. leopoldi-secundi Büttner, Republic of Congo, Champluvier 5248 (BR),
KM592213*, KM592120*, –; L. mannii Hook.f., Gabon, Dessein & al. 2518 (BR), KM592214*, KM592121*, KM592302*; L. papyrophloea Verdc., Tanzania,
Luke & Kibure 9838 (UPS), KM592215*, KM592122*, KM592304*; L. pynaertii De Wild., Republic of the Congo, Champluvier s.n. (BR), KM592216*,
KM592123*, KM592305*. Nichallea Bridson: N. soyauxii (Hiern) Bridson, Cameroon, Dessein & al. 1402 (BR), KM592218*, KM592125*, KM592307*.
Paracephaelis Baill.: P. cinerea (A.Rich. ex DC.) De Block, Madagascar, De Block & al. 2193 (BR), KM592220*, KM592127*, KM592308*; P. saxatilis
(Scott-Elliot) De Block, Madagascar, Davis & al. 2731 (K), KM592221*, KM592128*, –; P. saxatilis (Scott-Elliot) De Block, Madagascar, De Block & al. 2401
(BR), –, –, KM592309*; P. tiliacea Baill., Madagascar, Groeninckx & al. 113 (BR), KM592222*, KM592129*, KM592310*. Pavetta L.: subg. Baconia Bremek.:
P. hymenophylla Bremek., Tanzania, Luke & al. 9101 (UPS), KM592225*, KM592132*, –; P. ternifolia Hiern, Burundi, Ntore 19 (BR), KM592235*, KM592142*,
KM592321*; subg. Dizygoon Bremek.: P. tetramera (Hiern) Bremek, Gabon, Van de Weghe 163 (BR), KM592236*, KM592143*, KM592322*; P. suffruticosa
K.Schum., Cameroon, Lachenaud & al. 838 (BR), KM592231*, KM592138*, –; subg. Pavetta: P. agrostiphylla Bremek., Sri Lanka, Bremer B. & K. 936 (UPS),
KM592223*, KM592130*, KM592311*; P. batesiana Bremek., Gabon, Dessein & al. 2071 (BR), KM592224*, KM592131*, KM592312*; P. indica L., Sri
Lanka, Andreasen 202 (UPS), HM164217(4), HM164331(4), KM592313*; P. sansibarica K.Schum., Kenya, Luke & al. 8326 (UPS), KM592227*, KM592134*,
KM592314*; P. schumanniana F.Hoffm. ex K.Schum., Zambia, Dessein & al. 911 (BR), KM592228*, KM592135*, KM592315*; P. stenosepala K.Schum.,
Kenya, Luke & al. 8318 (UPS), KM592233*, KM592140*, KM592319*; P. tarennoides S.Moore, Kenya, Luke & al. 8325 (UPS), KM592234*, KM592141*,
KM592320*; P. sp. A of FTEA Bridson, Tanzania, Luke & al. 9134 (UPS), KM592232*, KM592139*, KM592318*; P. sp. B, Vietnam, Davis & al. 4082 (K),
KM592229*, KM592136*, KM592316*; P. sp. C, Asia (country unknown), Van Caekenberghe 199 (BR), KM592230*, KM592137*, KM592317*; P. vaga
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Appendix 1. Continued.
S.T.Reynolds, Australia, Harwood 1290 (DNA), KM592237*, KM592144*, KM592323*. Robbrechtia De Block: R. grandifolia De Block, Madagascar, Kårehed
311 (UPS), AM117339(3), AM117383(3), KM592325*; R. milleri De Block, Madagascar, Bremer & al. 5295 (S), KM592240*, KM592147*, KM592326*. Rutidea
DC.: sect. Rutidea: R. decorticata Hiern, Cameroon, Maurin 14 (K), KM592241*, KM592148*, –; R. dupuisii De Wild., Gabon, Dessein & al. 1802 (BR),
KM592242*, KM592149*, –; R. ferruginea Hiern, Cameroon, Dessein & al. 1674 (BR), KM592242*, KM592150*, KM592327*; R. olenotricha Hiern, Ghana,
Schmidt & al. 1731 (MO), KM592246*, KM592153*, KM592329*; R. orientalis Bridson, Tanzania, Borhidi & al. 84008 (UPS), KM592247*, –, KM592330*;
R. parviflora DC., Liberia, Adam 20156 (UPS), KM592248*, KM592154*, KM592331*; R. seretii De Wild., Cameroon, Gereau 5588 (UPS), KM592249*,
KM592155*, KM592332*; sect. Tetramera Bridson: R. fuscenscens Hiern, Tanzania, Luke & al. 9124 (UPS), KM592244*, KM592151*, KM592328*; R. membranacea Hiern, Liberia, Adam 21433 (UPS), KM592245*, KM592152*, –. Schizenterospermum Homolle ex Arènes: S. grevei Homolle ex Arènes, Madagascar, De Block & al. 2167 (BR), KM592250*, KM592156*, KM592333*; S. rotundifolia Homolle ex Arènes, Madagascar, De Block & al. 771 (BR), KM592251*,
KM592157*, KM592334*. Tarenna Gaertn.: T. alleizettei (Dubard & Dop) De Block, Madagascar, De Block & al. 1883 (BR), KM592272*, KM592178*,
KM592353*; T. alpestris (Wight) N.P.Balakr., India, De Block 1474 (BR), KM592252*, KM592158*, KM592335*; T. asiatica (L.) Kuntze ex K.Schum., India,
Auroville 998 (SBT), KM592253*, KM592159*, KM592336*; T. attenuata (Hook.f.) Hutch., Asia, country unknown, BR Living Collection 20031135-53 (BR),
KM592254*, KM592160*, KM592337*; T. bipindensis (K.Schum.) Bremek., Liberia, Jongkind 8495 (BR), KM592255*, KM592161*, KM592338*; T. capuroniana De Block, Madagascar, De Block & al. 937 (BR), KM592273*, KM592179*, KM592354*; T. depauperata Hutch., China, Chow & Wan 79063 (UPS),
KM592256*, KM592162*, KM592339*; T. flava Alston, Sri Lanka, Klackenberg 440 (S), KM592257*, KM592163*, KM592340*; T. fuscoflava (K.Schum.)
S.Moore, Ghana, Schmidt & al. 2099 (MO), KM592258*, KM592164*, KM592341*; T. gracilipes (Hayata) Ohwi, Japan, Van Caekenberghe 149 (BR),
KM592259*, KM592165*, –; T. grevei (Drake) Homolle, Madagascar, De Block & al. 959 (BR), KM592274*, KM592180*, KM592355*; T. jolinonii N.Hallé,
Gabon, Champluvier 6098 (BR), KM592260*, KM592166*, KM592342*; T. lasiorachis (K.Schum. & K.Krause) Bremek., Gabon, Wieringa 4432 (WAG),
KM592261*, KM592167*, –; T. leioloba (Guillaumin) S.Moore, New Caledonia, Mouly 174 (P), KM592262*, KM592168*, KM592343*; T. microcarpa
(Guillaumin) Jérémie, New Caledonia, Mouly 297 (P), KM592263*, KM592169*, KM592344*; T. nitidula (Benth.) Hiern, Liberia, Jongkind 8000 (BR),
KM592264*, KM592170*, KM592345*; T. pallidula Hiern, Gabon, Dessein & al. 2215 (BR), KM592265*, KM592171*, KM592346*; T. pembensis J.E.Burrows,
Mozambique, Luke & al. 10136 (UPS), KM592266*, KM592172*, KM592347*; T. precidantenna N.Hallé, Gabon, Dessein & al. 2360 (BR), KM592267*,
KM592173*, KM592348*; T. rhypalostigma (Schltr.) Bremek., New Caledonia, Mouly 182 (P), KM592268*, KM592174*, KM592349*; T. roseicosta Bridson,
Tanzania, Luke & al. 9170 (UPS), KM592269*, KM592175*, KM592350*; T. sambucina (G.Forst.) T.Durand ex Drake, New Caledonia, Mouly & al. 364 (P),
KM592270*, KM592176*, KM592351*; T. spiranthera (Drake) Homolle, Madagascar, De Block & al. 946 (BR), KM592275*, KM592181*, KM592356*;
T. thouarsiana (Drake) Homolle, Madagascar, De Block & al. 655 (BR), KM592276*, KM592182*, KM592357*; T. uniflora (Drake) Homolle, Madagascar,
Bremer & al. 5230 (S), KM592277*, KM592183*, KM592358*; T. vignei Hutch. & Dalziel, Republic of Guinea, Jongkind 8126 (BR), KM592271*, KM592177*,
KM592352*. Tennantia Verdc.: T. sennii (Chiov.) Verdc. & Bridson, Kenya, Luke & al. 8357 (UPS), KM592278*, KM592184*, KM592359*. Tribe Vanguerieae
Dumort.: Vangueria Juss.: V. madagascariensis J.F.Gmel., Africa (country unknown), Bremer 3077 (UPS), –, AJ620184(2), –; V. madagascariensis J.F.Gmel.,
Africa (country unknown), Delprete 7383 (NY), EU821636(1), –, –.
Version of Record
95