American Journal of Botany 96(5): 989–1010. 2009.
A PRELIMINARY PHYLOGENY OF THE ‘DIDYMOCARPOID
GESNERIACEAE’ BASED ON THREE MOLECULAR DATA SETS:
INCONGRUENCE WITH AVAILABLE TRIBAL CLASSIFICATIONS1
Michael Möller,2,5 Martin Pfosser,3,6 Chang-Gee Jang,3,7 Veronika Mayer,3
Alexandra Clark,2 Michelle L. Hollingsworth,2 Michael H. J. Barfuss,3
Yin-Zheng Wang,4 Michael Kiehn,3 and Anton Weber3
2Royal
Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh EH3 5LR, Scotland, UK; 3Faculty Centre of Biodiversity,
University of Vienna, Rennweg 14, A-1030 Vienna, Austria and 4Institute of Botany, Chinese Academy of Sciences,
Beijing, China
The ‘didymocarpoid Gesneriaceae’ (traditional subfam. Cyrtandroideae excluding Epithemateae) are the largest group of Old
World Gesneriaceae, comprising 85 genera and 1800 species. We attempt to resolve their hitherto poorly understood generic relationships using three molecular markers on 145 species, of which 128 belong to didymocarpoid Gesneriaceae. Our analyses
demonstrate that consistent topological relationships can be retrieved from data sets with missing data using subsamples and different combinations of gene sequences. We show that all available classifications in Old World Gesneriaceae are artificial and do
not reflect natural relationships. At the base of the didymocarpoids are grades of clades comprising isolated genera and small
groups from Asia and Europe. These are followed by a clade comprising the African and Madagascan genera. The remaining
clades represent the advanced Asiatic and Malesian genera. They include a major group with mostly twisted capsules. The much
larger group of remaining genera comprises exclusively genera with straight capsules and the huge genus Cyrtandra with indehiscent fruits. Several genera such as Briggsia, Henckelia, and Chirita are not monophyletic; Chirita is even distributed throughout
five clades. This degree of incongruence between molecular phylogenies, traditional classifications, and generic delimitations indicates the problems with classifications based on, sometimes a single, morphological characters.
Key words: atpB-rbcL spacer; Bayesian inference analysis; ITS; maximum parsimony; molecular phylogeny; Old World
Gesneriaceae; taxonomy; trnL-F intron-spacer.
Gesneriaceae is a medium-sized family, comprising between
150 and 160 genera, and over 3200 species (Weber, 2004; Weber and Skog, 2007). The distribution is mainly tropical and
subtropical, both in the Old and the New World, with minor
outliers to the north (e.g., Pyrenees, Balkan peninsula, central
and northern China) and to the south (southeastern Australia,
New Caledonia, New Zealand, southern Chile).
While the neotropical Gesneriaceae (subfam. Gesnerioideae,
including Coronanthereae, raised to subfamily rank by Wiehler,
1
1983) have received much attention by molecular systematists
and apparently approach consolidation regarding a phylogenetic and formal classification (Smith, 1996, 2000; Smith et al.,
1997a, b; Zimmer et al., 2002; Perret et al., 2003; Roalson et al.,
2005a, b), the paleotropical Gesneriaceae (subfam. Cyrtandroideae, now Didymocarpoideae) lag behind. The last attempt at a
formal (morphological) classification was by Burtt and Wiehler
(1995), who distinguished five tribes: (1) Cyrtandreae (with indehiscent, berry-like fruits); (2) Trichosporeae (with appendaged seeds); (3) Epithemateae (Klugieae and Loxonieae sensu
Burtt (1963), a group rather difficult to characterize, partly
with peculiar anatomical characters such as secretory canals
and meduallary vascular bundles); (4) Didymocarpeae (the
many remaining genera arranged alphabetically to express the
wide lack of phylogenetic understanding); and Titanotricheae
including the sole genus Titanotrichum. Additional tribes
(Saintpaulieae, Ramondeae, Rhynchotecheae) have been recognized by Ivanina (1965a, b, 1967) and Wang et al. (1990,
1992).
Detailed morphological investigations (Weber, 1975–1988,
as cited in Mayer et al., 2003) and, more recently, a molecular
analysis based on cpDNA sequences (Mayer et al., 2003)
showed that the Epithemateae form a distinct clade, sister to the
remaining Old World Gesneriaceae. Both the morphological investigations and the molecular analyses led to a fairly good understanding of the phylogenetic relationships for six of seven
genera of the ‘epithematoid Gesneriaceae’, as they are informally referred to in Weber (2004) and Weber and Skog (2007).
The present paper deals with the diverse non-epithematoid
Old World Gesneriaceae, the ‘didymocarpoid Gesneriaceae’. A
number of genera had already been included in the molecular
Manuscript received 26 August 2008; revision accepted 12 December 2008.
The authors thank the horticulturists at the Royal Botanic Garden
Edinburgh, in particular, S. Scott, S. Barber, and A. Ansell; and A. Sieder
at the Botanic Garden Vienna, for excellent work in maintaining and
accurately curating the living Gesneriaceae collections. They are also
grateful to staff at KIB for assistance with fieldwork, especially Dr. D. Z.
Li and Dr. L. M. Gao, and for the provision of samples by Profs. Z. J. Gu
and C. Q. Zhang (KIB). The work was carried out and is still continued
in the frame of a multidisciplinary cooperation project between the
University of Vienna (supported by the Austrian Science Fund (FWF)proj. no. P-13107-Bio) and the Royal Botanic Garden Edinburgh
(RBGE). RBGE is supported by the Scottish Government Rural and
Environment Research and Analysis Directorate (RERAD). Fieldwork
of M.M. was supported by the Percy Sladen Memorial Fund, Oleg
Polunin Memorial Fund, Davis Expedition Fund of the University of
Edinburgh, and FWF.
5 Author for correspondence (e-mail: m.moeller@rbge.ac.uk)
6 Present address: Biology Centre Linz, Oberösterreichisches Landesmuseum, Johann Wilhelm Klein Straße 73, A-4040 Linz, Austria
7 Present address: Department of Biology Education, College of Education, Kongju National University, Gongju, Korea
doi:10.3732/ajb.0800291
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analysis of Mayer et al. (2003), and preliminary results of the
current study formed the basis of the informal classification
presented by Weber (2004). In the meantime, the number of
samples included in the molecular analysis has considerably increased, and sufficient results are available to make some headway in our understanding of relationships in this group,
particularly with respect to previous subdivisions into tribes.
Nonetheless, we abstain from a new formal classification at this
point because a significant number of genera are not yet included in our analysis.
Effectively analyzing large data sets is challenging and complete analyses computationally intractable (e.g., Savolainen and
Chase, 2003). Furthermore, sample-rich analyses including
multiple data sets often suffer from missing data or issues of
incongruencies between data sets (Sanderson and Shaffer,
2002). Here we address the issue of missing data by analyzing
selected subsets of samples with complete data compared to a
complete sample set with missing data, and demonstrate that
“correct” topologies of phylogenetic trees can be recovered
from largely incomplete data matrices.
MATERIALS AND METHODS
Plant materials—Material for DNA extraction came in various forms and
from diverse sources, including fresh leaves from research collections (E,
HBV), silica-dried leaves of field collections, and herbarium specimens at various herbaria (Appendix 1).
Outgroup choice—To produce a reliable phylogeny of the family Gesneriaceae, we included members of major families of basal Lamiales (Oleaceae,
Tetrachondraceae, Scrophulariaceae, Plantaginaceae s.l., Calceolariaceae s.s.)
(Oxelman et al., 1999; Bremer et al., 2002; AGP II, 2003) in the analysis and
used them as outgroups. The trees were rooted on Oleaceae (Olmstead et al.,
2000; Tank et al., 2006). Details of outgroup taxa are given in Appendix 1.
Ingroup taxa—The samples of Gesneriaceae included 174 species in 78
genera. Their taxonomic classification followed Weber (2004). Twenty-three
species were from gesnerioid Gesneriaceae covering 20 (of 53) genera, and six
species belonged to coronantheroid Gesneriaceae (six of nine genera). A total
of 17 species were sampled from epithematoid Gesneriaceae (six of seven genera); only the monotypic genus Gyrogyne W.T.Wang is missing. Gyrogyne
subaequifolia W.T.Wang is only known from the type collection, and DNA
extraction from the isotype failed. Finally, 128 species (from 46 of 78 genera)
came from didymocarpoid Gesneriaceae. The sample selection covered all
tribes recognized by Burtt and Wiehler (1995, Epithemateae as ‘Klugieae’).
Speciose genera of didymocarpoid Gesneriaceae were represented by a
higher number of samples; Aeschynanthus Jack: five species of ca. 185, Chirita
Buch.-Ham.: 15 of 80–140, Cyrtandra Forst.: six of (perhaps) 450–600,
Didymocarpus Wall. s.s.: seven of ca. 70, Henckelia: five of ca. 180, Paraboea:
14 of 87, Streptocarpus: 10 of ca. 140.
In addition, Jerdonia Wight (monotypic with J. indica Wight) and Titanotrichum Solereder (monotypic with T. oldhamii Solereder) were included in the
analysis, the former described in Weber (2004) with uncertain familial affiliations and the latter as excluded from Gesneriaceae. Jerdonia was originally
described in Gesneriaceae (Wight, 1850), but referred to Scrophulariaceae by
Burtt (1977). Titanotrichum was originally described in Scrophulariaceae, but
recent molecular analyses suggest it to belong to Gesneriaceae, closely allied to
New World taxa (Wang et al., 2004).
DNA extraction, PCR, and direct sequencing—Genomic DNA was extracted using a modified CTAB procedure (Doyle and Doyle, 1987, 1990) and/
or the Qiagen DNeasy DNA Isolation Kit (Crawley, UK) following the manufacturer’s protocol.
PCR amplification of the trnL-F intron-spacer region (trnL-F) and atpBrbcL spacer (atpB-rbcL) followed Mayer et al. (2003). Some trnL-F and ITS
sequences were obtained as follows: PCR amplification was performed using
primers ‘c’ and ‘f’ (Taberlet et al., 1991) for trnL-F or primers 5P and 8P
(Möller and Cronk, 1997) for ITS on an MJ Research PTC-200 DNA Engine
[Vol. 96
thermal cycler. The 50 µL reactions contained 5 µL 10× NH4 reaction buffer
(Bioline, UK), 5 µL dNTPs (2 mM), 2.5 µL MgCl2 (50 mM), 1.5 µL of each
primer (10 µM), 32.25 µL dH2O, 1.25 U Biotaq polymerase (Bioline, UK) and
1.0 µL DNA template DNA. The PCR thermocycle profile for trnL-F was: initial denaturation for 4 min at 94°C; followed by 30 cycles of 45 s at 94°C, 45 s
at 55°C and 3 min at 72°C; with a final extension step for 10 min at 72°C. ITS
amplifications were carried out using the PCR profile described in White et al.
(1990) or Möller and Cronk (1997).
PCR products were run on 1% agarose gels to check for amplification success and quality. Amplified fragments were purified using QIAquick PCR
purification kits (Qiagen, Crawley, UK) following the manufacturer’s protocol, and sequenced using the dideoxy chain-termination method. Cycle sequencing was performed as in Mayer et al. (2003), or in 10 µL reactions
containing 4 µL DTCS Quickstart mix (Beckman Coulter, High Wycombe,
UK), 1 µL primer (10 µM), 3 µL dH2O and 2 µL purified PCR product, under
the following PCR conditions: 35 cycles of 96°C for 20 s, 50°C for 20 s and
60°C for 4 min. Sequencing primers were identical to those used for PCR
with the addition that primer ‘d’ (Taberlet et al., 1991) was also used to sequence the trnL intron region. Sequencing atpB-rbcL followed Mayer et al.
(2003). Sequencing PCR products were purified following the manufacturer’s instructions, then run and analyzed on a CEQ 8000 Genetic Analysis
System (Beckman Coulter, UK). Editing and assemblage of contigs was performed using the programs CEQuence Investigator (Beckman Coulter, High
Wycombe, UK) and Sequencher 4.5 (Gene Codes Corp, Ann Arbor, USA),
and for atpB-rbcL as in Mayer et al. (2003). The cpDNA alignment matrices
were assembled manually, based on those of Mayer et al. (2003). ITS sequences were initially aligned using the program CLUSTAL W (Larkin et al.
2007) and the alignment then adjusted manually, as described in Möller and
Cronk (1997).
Phylogenetic analysis—For this study, 123 trnL-F, 59 atpB-rbcL, and 65
ITS sequences were newly acquired and submitted to GenBank; the remaining
sequences were retrieved from GenBank (Appendix 1). Because a complete
overlap of sequences across the three gene regions used could not be achieved,
the data were analyzed in three sets:
(1) A combined trnL-F and atpB-rbcL matrix (cpDNA) that included 129
samples (59 trnL-F and 59 atpB-rbcL sequences were new, the rest from GenBank) (TreeBase: SN4215–20651). This complete plastid matrix included nine
outgroup taxa; 22 gesnerioid, five coronantheroid, and 18 epithematiod samples; and a backbone set of 73 samples for didymocarpoid taxa and Jerdonia
and Titanotrichum. The main purpose for this analysis was to resolve out-/ingroup relationships and the backbone topology for the Gesneriaceae family,
specifically for the basal Asiatic and European taxa. The addition of the two
samples of Tetraphyllum Griff ex C.B.Clarke, for which no atpB-rbcL data
were available, did not alter the tree topology in any analysis, and were thus
included in a final matrix of 131 samples.
(2) A complete, combined trnL-F and ITS data set with 88 didymocarpoid
samples (71 trnL-F and 65 ITS sequences were new, the rest from GenBank)
(TreeBase: SN4215–20652). This analysis focused on resolving relationships
among the advanced Asiatic and Malesian genera (Weber, 2004), with specific
focus on testing the monophyly of members of the tribe Trichosporeae. This
analysis was, based on results of analysis 1, rooted on African and Madagascan
samples. The ITS alignment at higher taxonomic level above these samples was
found to be too ambiguous and the sampling too incomplete to be analyzed.
(3) A combined trnL-F, atpB-rbcL, and ITS data matrix with 201 samples
across the family, including missing sequences (201 trnL-F, 129 atpB-rbcL, 88
ITS) (TreeBase: SN4215–20650). 123 trnL-F, 59 atpB-rbcL and 65 ITS sequences were new, the rest were from GenBank. The purpose for this analysis
was to obtain a topology for all samples included in our study. The topology of
major groups in this analysis was basically identical to those of the complete
analyses 1 and 2.
The matrices were analyzed by maximum parsimony (MP) implemented in
the program PAUP* version 4.0b10 (Swofford, 2002) and by Bayesian Markov
chain Monte Carlo (MCMC) inference (BI; Yang and Rannala, 1997) using the
program MrBayes version 3.1.2 (Huelsenbeck and Ronquist, 2001, 2007) on
unordered and equally weighted characters.
Combinability of data sets was determined using the incongruence length
difference (ILD) test of Farris et al. (1994, 1995), implemented in PAUP* as
the partition-homogeneity test, on 1000 replicates of repartitioning with treebisection-reconnection (TBR) on (Yuan et al., 2005).
In view of the high number of sequences included, MP starting trees were
found using the parsimony ratchet (Nixon, 1999) implemented in the programs
PAUPRat (Sikes and Lewis, 2001) and PAUP*. Only the shortest of the 201
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Möller et al.—Phylogeny of didymocarpoid Gesneriaceae
trees saved with PAUPRat were further optimized, with TBR and MulTrees
activated, in PAUP*. For analysis 3, the MaxTree option was set to 100 000
trees. Descriptive tree statistics (ensemble consistency index [CI; Kluge and
Farris, 1969], ensemble retention index [RI; Farris, 1989a], and ensemble rescaled consistency index [RC; Farris, 1989b]) were obtained using PAUP*. Statistical branch support analyses were performed twofold, as 10 000 replicates of
heuristic bootstrap replicates (BS; Felsenstein, 1985) with TBR swapping on
and MulTrees off (Spangler and Olmstead, 1999) in PAUP* and as decay indices (DI; Bremer, 1988), derived from the program AutoDecay version 4.0.2
(Eriksson, 1999) and PAUP* from 100 replicates of random addition.
Models and parameters priors for the BI analyses were obtained independently for each data set and gene sequence in each analysis using Modeltest
(Posada and Crandall, 1998). In the higher level analysis 1 (with 131 samples),
the model TVM+I+G was suggested by the Akaike information criterion (AIC;
Akaike, 1974) for the trnL-F data, and TVM+G for the atpB-rbcL data. In analysis 2, the GTR+G model was selected for trnL-F, and GTR+I+G for ITS under
the AIC. For analysis 3, the models GTR+I+G, TVM+G and GTR+I+G were
selected for the trnL-F, atpB-rbcL, and ITS sequences, respectively.
For analyses 1 and 2, two million generations were run with four MCMC
chains in two independent parallel analyses, with one tree sampled every 100
generations (10 000 trees). The first 130 000 generations or the first 1300 trees
for the cpDNA analysis 1 and the first 60 000 generations or 600 trees for analysis 2 were discarded as burn-in (generations prior to stationarity of likelihood
values). For analysis 3, the number of generations was four million, and the
burn-in 400 000 generations. A majority rule consensus tree was constructed in
PAUP* from the remaining trees, combined from the two parallel analyses.
Although not strictly comparable to bootstrap values (see also Fig. 4) the retrieved posterior probabilities (PP) indicate robustness of clades (Lewis, 2001;
Alfaro et al., 2003; but see Cummings et al., 2003; Erixon et al., 2003). Majority rule consensus trees of individual BI runs were identical (except for two
branches in analysis 3 with PP values of 0.5 and 0.53). A high correlation of the
PP support values was found between the two parallel runs of the Bayesian
analysis for all three data sets (Appendix S1, see Supplemental Data with online
version of this article).
RESULTS
Matrix characteristics—The combined cpDNA matrix (analysis 1) had 2525 aligned characters (trnL-F: 1278 characters,
atpB-rbcL: 1247 characters), with 366 ambiguous characters excluded, resulting in 2159 characters used for analysis, of which
585 were constant, 176 variable but parsimony uninformative
and 386 (33.6%) parsimony informative in the trnL-F, and 484,
211, and 317 (31.3%) respectively in the atpB-rbcL data.
The combined matrix for analysis 2 consisted of an alignment matrix of 2141 characters (trnL-F: 1278 characters; ITS:
863), with 276 ambiguous sites excluded, leaving 1865 characters in the analysis. Of these, 752 were constant, 209 variable
but parsimony uninformative, and 186 (16.2%) parsimony informative for trnL-F and 248, 127, and 343 (47.8%), respectively, for ITS.
The combination of all three genes (analysis 3) resulted in a
matrix of 3652 characters, of which 2877 unambiguously
aligned characters were included in the analysis. Of these, 1251
were constant, 528 variable but parsimony uninformative, and
1098 (38.1%) parsimony informative.
Analysis 1: Tree topology trnL-F and atpB-rbcL— The cpDNA strict consensus tree, based on 6912 most parsimonious
trees of 2636 steps, showed a highly resolved topology with
strong backbone support in most areas (Fig. 1). Bootstrap values ranged from 50% to 100% with 64 of 98 internal branches
possessing support values of 90% or higher, and decay indices
from 1 to 69. The Gesneriaceae were highly supported (BS =
100%; DI = 15) with Calceolariaceae its closest allied family
(BS = 90%; DI = 3). A monophyletic coronantherioid clade
(BS = 99%; DI =7) nested within the gesnerioid clade. This
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clade also included the Old World (OW) genus Titanotrichum
(BS = 82%; DI = 2). Sister to this group were the other OW
samples, which formed a well-supported clade (BS = 96%;
DI = 5). Within this clade, the epithematoid (BS = 100%; DI =
13) clade was sister to the remaining OW genera (BS = 98%; DI =
3). Among these, the hitherto unassigned genus Jerdonia split
off first, followed by several grades and one polytomy for the
basal Asiatic and European genera. The African and Madagascan
genera formed a monophyletic sister clade (BS = 100%; DI =
11) to the advanced Asiatic and Malesian genera (BS = 65%;
DI = 2). The resolution and support among those was not very
high, but clades for individual genera were mostly well supported (BS = 98–100%; DI = 2–11), with the exception of samples of Chirita, which clustered in five different clades that
were closely associated with other genera.
The two genera belonging to tribe Cyrtandreae sensu Burtt
(1963) and Burtt and Wiehler (1995), Cyrtandra and Rhynchotechum Blume, were resolved separately in distant positions,
among the basal Asiatic and European genera (Rhynchotechum)
and among the advanced Asiatic and Malesian genera (Cyrtandra).
Tribe Ramondeae sensu Wang et al. (1990, 1992) was also not
monophyletic, with Ramonda among the basal Asiatic and
European genera, and Conandron Siebold & Zucc. among the
advanced Asiatic and Malesian genera.
The topology of the majority rule consensus tree of the BI
analysis (Appendix S2, see online Supplemental Data) was very
similar to the MP strict consensus tree, with only minor differences in terminal clade relationships, which were not highly
supported in any analysis. The most obvious discrepancy was a
sister rather than grade relationship of the European and part of
basal Asiatic genera (including Leptoboea Benth., Platystemma
Wall., Rhynchotechum and Boeica C.B.Clarke) (Fig. 1,
arrow).
Analysis 2: Tree topology trnL-F and ITS— The MP analysis yielded 28 most parsimonious trees of 3230 steps. The resulting strict consensus tree was highly resolved with 44 of 78
internal branches with 90% or higher bootstrap branch support
and decay values between 1 and 36 (Fig. 2). The trees showed
a strongly supported monophyletic ingroup (BS = 100%; DI =
29) of African and Madagascan genera, followed by a clade of
mainly twisted-fruited advanced Asiatic and Malesian genera
(Boea group) (BS = 99%; DI = 8). Among the remaining advanced Asiatic and Malesian genera, the tree topology was resolved but with low backbone support. Several subclades
harboring several genera received high branch support (discussed later).
Of the four genera of tribe Trichosporeae sensu Burtt and
Wiehler (1995) included in our analysis (Aeschynanthus,
Agalmyla Blume, Loxostigma C.B.Clarke, and Lysionotus D.
Don), the first three fell together in a polytomy (with Loxostigma and Agalmyla as sister genera), while Lysionotus appeared distant to these genera and more closely related to
Hemiboea C.B.Clarke (Fig. 2).
The BI analysis majority rule consensus tree showed more
resolution among the twisted-fruited genera (online Appendix
S2), but less resolution for the backbone structure of the straightfruited genera, though the branches involved generally received
low branch support in the MP analysis for the latter.
Analysis 3: Three-gene tree topology— The MP analysis on
all three-sequence matrices resulted in 18 405 most parsimonious trees of 5655 steps (Fig. 3). The topology of the strict con-
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Möller et al.—Phylogeny of didymocarpoid Gesneriaceae
sensus tree was identical to that in the respective areas of the two
two-gene MP analyses 1 and 2. The southern hemisphere Coronantheroideae nested within the New World (NW) Gesnerioid
genera and also included the OW Titanotrichum (BS = 82%;
DI = 2). This clade was sister to the rest of the NW didymocarpoid genera (BS = 100%; DI = 15), with the Epithematoid (BS =
100%; DI = 13) sister to the rest (BS = 96%; DI = 5), followed
by grades of Jerdonia (BS = 98%; DI = 3), Corallodiscus Batalin (BS = 100%; DI = 13), Tetraphyllum (BS = 99%; DI = 4),
and a polytomy of the remaining basal Asiatic genera (BS =
92%; DI = 4) and the European genera (BS = 63%; DI = 1). Next
followed the African and Madagascan genera, forming a strongly
supported monophyletic clade (BS = 100%; DI = 14), with five
genera, the African Acanthonema Hook f., Saintpaulia Wendl,
and Schizoboea (K.Fritsch) B.L.Burtt, and the Madagascan Colpogyne B.L.Burtt and Hovanella A.Weber & B.L.Burtt nesting
within the genus Streptocarpus Lindl..
Among the remaining advanced Asiatic and Malesian genera, the straight-fruited genus Didissandra C.B.Clarke appeared
to split the clades of the African (BS = 100%; DI = 14) and
Asian genera of the Boea group (BS = 85%; DI = 2). The latter
including the genera Boea Comm. Ex Lam., Emarhendia Kiew,
A.Weber & B.L.Burtt, Kaisupeea B.L.Burtt, Ornithoboea Parish ex C.B.Clarke, Paraboea Ridl., Rhabdothamnopsis Hemsl.,
and Spelaeanthus Kiew, A.Weber & B.L.Burtt. Trisepalum
C.B.Clarke was found nested within a Paraboea clade (BS =
97%; DI = 5). One of the four Asiatic members of Streptocarpus, S. orientalis Craib included here, was also found in the
Boea group, as well as the straight-fruited Henckelia ericii
A.Weber (= Loxocarpus holttumii M.R.Hen.) and Chirita lacunosa (Hook f.) B.L.Burtt.
The remaining advanced Asiatic and Malesian genera with
straight fruits formed a weakly supported clade (BS = 62%;
DI = 2) with fairly well-resolved relationships, but with low or
no internal branch support. A highly supported clade (BS =
100%; DI = 16) of Chirita species of section Microchirita was
sister to the remaining samples, followed by a clade of two SE
Asian Henckelia Spreng. species (BS = 99%; DI = 6) and a
mixed clade of Chirita and Henckelia from China and Sri Lanka
(BS = 70%; DI = 2).
The remainder of the samples fell into two large clades, but
with little backbone support, one including the genera Anna
Pellegr., Briggsia Craib, Calcareoboea C.Y.Wu, Chirita, Chiritopsis W.T.Wang, Hemiboea, Lysionotus, Petrocodon Hance,
Petrocosmea Oliv., Primulina Hance, Raphiocarpus Chun and
Ridleyandra A.Weber & B.L.Burtt. In this clade, Primulina was
sister to Chirita longgangensis W.T.Wang (BS = 96%; DI = 5),
nested deep inside a Chirita section Gibbosaccus clade (BS =
73%; DI = 1). Chiritopsis also nested within this clade (BS =
97%; DI = 2).
The second large clade included Aeschynanthus, Agalmyla,
Ancylostemon Craib, Briggsia, Chirita asperifolia (Blume)
B.L.Burtt, Conandron, Cyrtandra, Didymocarpus, Loxostigma,
Opithandra B.L.Burtt, and Oreocharis Benth. Chirita asperifolia (the type species of Chirita section Liebigia, reestablished
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by Hilliard, 2004), was sister to Didymocarpus (BS = 92%;
DI = 10).
The four samples of Briggsia included here did not form a
monophyletic group and the two sister pairs fell into different
clades, one closely allied to Ancylostemon, Opithandra and
Oreocharis (BS = 96%; DI = 3), the other sister to a group of
genera including Raphiocarpus sp., Anna, Lysionotus, and
Hemiboea, but with little branch support.
The genus Chirita was highly polyphyletic, falling in four
places among the straight-fruited, advanced Asiatic and Malesian genera and once in the Boea group.
The BI analysis was largely congruent with the MP analysis
for strongly supported branches but differed in areas that received low or no BS support in the MP analysis (Fig. 3; online
Appendix S2).
DISCUSSION
Phylogenetic analysis— Our MP analyses on 190 Gesneriaceae samples resulted in well-resolved and stable topologies
across the complete two-gene analyses (analyses 1 and 2), and
gave a highly resolved strict consensus tree in the three-gene
analysis (analysis 3), irrespective of missing sequences for some
samples in the latter. This finding is in line with previous studies
that suggested that even highly incomplete matrices can yield
accurate phylogenetic topologies (Qiu et al., 1999; Murphy et
al., 2001; Kearney, 2002; Wiens, 2003, 2006), and the effects of
missing sequences can be minor (Wiens and Reeder, 1995). In
fact, in our three-gene analysis, the more conserved cpDNA
data supported the backbone of the trees, particularly at the
higher taxonomic level, while the faster evolving ITS sequences
resolved and supported relationships at lower taxonomic levels.
This complementarity has previously been observed in other
data sets (Qiu et al., 1999; Long et al., 2000; Sinclair et al.,
2002). Furthermore, undesired effects such as long-branch attraction (Felsenstein, 1978), suspected to be problematic in
combining incomplete data sets (Wiens, 2006) were not found
in our analyses, as seen by the high similarity of topologies between analyses using different gene combinations.
The ILD test for combinability of our matrices showed some
incongruence between the data sets, but the probability values
were above the P = 0.05 threshold. The applicability of the ILD
test as a determinator of combinability of different data sets has
been discussed controversially, with Cunningham (1997) being
a proponent, while others opposed its use (Barker and Lutzoni,
2002; Hipp et al., 2004). However, the consistencies of our tree
topologies across the three analyses suggest that the hierarchy
retrieved from the three combined genes reflects reasonably
well the relationships of the genera included here.
Controversy surrounds the interpretation of posterior probabilities (PP) and their comparison to other branch support values (Wilcox et al., 2002; Suzuki et al., 2002; Cummings et al.,
2003; Erixon et al., 2003). We investigated this issue by plotting the bootstrap against PPs (Fig. 4), and it becomes clear that
←
Fig. 1. Strict MP consensus tree of 6912 most parsimonious trees of 2636 steps based on combined trnL-F and atpB-rbcL sequences of 131 samples
(CI = 0.62, RI = 0.84, RC = 0.52). Bootstrap values and decay indices (bold and italics) are given above branches. Light gray boxes = Trichosporeae, dark
gray boxes = Cyrtandreae; systematics (right side) follows Weber 2004; black bars = outgroups, hatched bars = gesnerioid, lined bars = coronantheroid,
open bars = didymocarpoid, crosshatched = unassigned. Branches in bold are supported by posterior probabilities of 1.00 (black) or 0.99 (gray) in the
Bayesian analysis. Asterisks indicate generic types. Arrow indicates a relationship found in the Bayesian analysis.
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Möller et al.—Phylogeny of didymocarpoid Gesneriaceae
the PP values were over most parts significantly higher than
bootstrap values, with branches receiving BS values as little as
51% having PPs of 0.99 or 1.00. Thus, while Bayesian inference analysis here often results in more resolved trees with high
PP values, these high PP values do not necessarily reflect strong
robustness of the BI tree topologies, irrespective of missing
data (see Fig. 4E for data set 2 without missing data, and Fig. 4F
for data set 3 with missing data). Our interpretations consequently rely predominantly on the more conservative MP topology and its branch support values.
We observed only few differences between the MP and BI
analyses with some bearing on our main objectives relating to
the monophyly of current tribes; one concerns the relationships
between the European and part of the basal Asiatic genera, the
other involves a sister relationship (BI) of Aeschynanthus and
Agalmyla as opposed to such a relationship of the latter to Loxostigma (MP). In neither case is monophyly of the tribe Trichosporeae supported (discussed later), and thus these incongruencies
have no effects on the interpretation of our data and the conclusions drawn.
Highly supported relationships among the straight-fruited,
advanced Asiatic and Malesian genera remained elusive, but it
must be noted that over 30 didymocarpoid genera (most are
likely to belong to this group) have not been included in our
analysis yet. Their addition may well stabilize the tree topology
in this area. It is not lack of sequence variation but lack of topology congruencies and synapomorphies (shared evolved characters) that causes the problem as inferable from individual
phylograms (online Appendix S3).
It was interesting to see that the distribution of branch support was greatly partitioned across the tree. While intergeneric
branches received low or medium support, branches leading to
genera were highly supported (Table 1). The latter indicates
that the genera included (except nonmonophyletic genera) represented strongly defined genetic entities. Nonetheless, further
data are required to better resolve the relationships of the
didymocarpoid genera.
Tribal classification of Old World Gesneriaceae–– The traditional family classifications of Gesneriaceae are those of Bentham (1876) and Fritsch (1893–1894). The latter represents the
most detailed classification available (2 subfamilies, 18 tribes,
9 subtribes). Fritsch’s (1893–1894) classification was largely
based on formal morphological characters, and many insufficiencies became apparent on closer inspection. Burtt (1954)
even qualified Fritsch’s classification as “negative in quality”
and a retrogression. In the Old World Gesneriaceae subfam.
Cyrtandroideae, Burtt reduced the number of tribes to five:
Cyrtandreae, Trichosporeae, Klugieae, Loxonieae, and Didymocarpeae. Later, based on morphological data of Weber (1975–
1988, cited in Mayer et al., 2003), he united Klugieae and
Loxonieae into a single tribe (informally in Burtt, 1977, formally in Burtt and Wiehler, 1995), which is presently known as
Epithemateae (Burtt, 1997). Apart from Didymocarpeae, each
of the tribes contained only a small number of genera. The
strong asymmetry in species number was paralleled by the dif-
995
ficulties in recognizing generic relationships. Burtt and Wiehler
(1995) thus listed the genera of Didymocarpeae simply in alphabetical order.
The five-tribe classification of OW Gesneriaceae of Burtt
and Wiehler (1995) is reflected in our analyses only to a very
low degree. Though morphologically not easy to define, the
Epithemateae are a well-supported monophyletic group, which
is sister to the remaining Old World genera (Mayer et al., 2003;
Wang et al., 2004). The tribes Cyrtandreae and Trichosporeae
were supported in a morphological cladistic analysis of Smith
(1996), but not by molecular investigations (Smith et al., 1997a,
b). In principal agreement with the latter data, we found both
tribes nested within tribe Didymocarpeae sensu Burtt and
Wiehler (1995). Furthermore, genera from neither tribe Cyrtandreae or Trichosporeae formed monophyletic groups, suggesting that the morphological features considered characteristics at
tribal level (Cyrtandreae with indehiscent fruits and Trichosporeae with seed appendages) have repeatedly and independently evolved.
Tribe Cyrtandreae included three genera in Burtt and Wiehler
(1995): Cyrtandra, Sepikea Schltr., and Rhynchotechum.
Because the monospecific Sepikea is probably just an abnormally tetrandrous Cyrtandra (perhaps even based on a misobservation, Burtt, 1998), only Cyrtandra and Rhynchotechum
remain. According to our data, Rhynchotechum has its place
among other basal Asiatic didymocarpoids, while Cyrtandra
occupies a position within the advanced Asiatic and Malesian
didymocarpoids. Therefore, there is no basis for retaining the
tribe.
Tribe Trichosporeae was thought to contain six genera in
Burtt and Wiehler (1995). From these, two genera (Oxychlamys
Schltr., Van Royen, 1983; Micraeschynanthus Ridl., Middleton, 2007) have been sunk into synonymy, thus leaving the four
remaining genera Aeschynanthus, Agalmyla, Loxostigma, and
Lysionotus. All these were included in our analysis. Some (but
not all) of our trees suggest a closer, though unsupported, affinity between the genera Agalmyla, Loxostigma, and to some degree Aeschynanthus, but Lysionotus was always more closely
associated with Hemiboea than with any other genus of Trichosporeae. Both the position within the advanced Asiatic and
Malesian genera and the partial nonaffinity of the genera require disbandment of the Trichosporeae.
Other tribes used in recent classifications— Early definitions of most tribes are problematic, but some have been revived, redefined, or newly established in recent work. These are
discussed here in some detail.
Ramondeae (Fritsch, 1893–1894)— Originally, this tribe included the European genera (Ramonda Rich., Jancaea Boiss.,
Haberlea Pohl ex Barker), Corallodiscus, and Petrocosmea
from Asia, and Saintpaulia from Africa. The key character for
defining this group is straight fruits with septicidal dehiscence.
Wang et al. (1990) redefined this tribe to include all OW genera
with actinomorphic flowers (Ramonda, Thamnocharis W.T.Wang,
Tengia Chun, Bournea Oliv., and Conandron). Neither definition
←
Fig. 2. Strict MP consensus tree of 29 most parsimonious trees of 3275 steps based on combined ITS and trnL-F sequences of 89 sampled of advanced
Asiatic genera rooted on African genera (CI = 0.43, RI = 0.63, RC = 0.27). Bootstrap values and decay indices (bold and italics) are given above branches.
Light gray boxes = Trichosporeae, dark gray boxes = Cyrtandreae; systematics (right side) follows Weber 2004; open bars = didymocarpoid. Branches in
bold are supported by posterior probabilities of 1.00 (black) or 0.99 (gray) in the Bayesian analysis. Asterisks indicate generic types.
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American Journal of Botany
of the tribe is supported in our analyses (see also Möller
et al., 1999).
Saintpaulieae (Ivanina, 1965b)— This tribe included the
straight-fruited African genera Saintpaulia, Carolofritschia
Engl. (now Acanthonema: Burtt, 1982), Acanthonema, and Linnaeopsis Engl. (now Streptocarpus: Darbyshire, 2006). Our
data show that the genera included in our analysis do not form
a coherent group (Figs. 2, 3), but are scattered among Streptocarpus (see also Möller and Cronk, 1997, 2001a, b).
Streptocarpeae (Fritsch, 1893–1894)— This tribe (with Phylloboea Benth., Boea, Ornithoboea, and Streptocarpus) was reduced to subtribe Streptocarpinae of tribe Didymocarpeae by
Ivanina (1965b) and expanded to include also Paraboea, Rhabdothamnopsis, and Trisepalum. All, except most Streptocarpus
species, are distributed in Asia and indeed form a coherent alliance in our analyses: the Boea group. The majority of Streptocarpus species, as currently circumscribed, occur in Africa,
Madagascar, and the Comoro Islands (~140 species Hilliard and
Burtt, 1971), but four species have been described from Asia: S.
burmanicus Craib (Burma), S. orientalis (Thailand), S. sumatranus B.L.Burtt (Sumatra), and S. clarkeanus (Hemsl.) Hilliard
& B.L.Burtt (China) (cf. Hilliard and Burtt, 1971). At first sight,
the occurrence of Streptocarpus species in Asia seems to support the idea of a transcontinental distribution of a group comprising Streptocarpus and the Asiatic genera with twisted fruits.
However, Hilliard and Burtt (1971) have doubted that the Asiatic species of Streptocarpus are placed in the correct genus.
They placed these in the genus with considerable reservations
because of the lack of distinguishing morphological features.
Indeed, one of them, S. clarkeanus, has been recently transferred
to Boea by Wang et al. (1990). Another, S. orientalis, was examined molecularly in the current study and cytologically by M.
Kiehn (University of Vienna, unpublished data). Both the molecular and the cytological data (2n = 18) indicated that there is
no relationship between the Asian S. orientalis and the African
and Madagascan species. We believe that it is simply a question
of time before the remaining Asiatic species follow suit.
The African and Madagascan species of Streptocarpus plus
the straight-fruited compatriots formed a highly supported
monophyletic clade in our analyses. If retained in a future classification, tribe or subtribe Streptocarpeae (-inae) will most
probably form a group comprising exclusively African and
Madagascan genera and species.
Rhynchotecheae (Ivanina, 1965a)— This tribe included
Rhynchotechum and Isanthera Nees (included in Rhynchotechum by Burtt 1962a). Ivanina indeed was right to separate
Rhynchotechum from the Cyrtandreae, but she still thought
there would be a close relationship between the two tribes
(Ivanina, 1965b: fig. 14). As shown here, this is not the case.
Therefore, the indehiscent fruit characterizing Cyrtandra and
Rhynchotechum has no taxonomic bearing. It is simply a
convergence.
[Vol. 96
Indication of para/polyphyly of some genera— Our data indicate that a number of genera are artificial and polyphyletic:
Streptocarpus (see discussion above), Chirita, Henckelia,
Briggsia, and possibly Paraboea, Boea, and Raphiocarpus.
Chirita—Species of this large genus (see revisions of
Wood, 1974, and Wang, 1985a, b) appear distributed over at
least five clades in our analysis. Some conform to current sections (sects. Chirita, Microchirita, Gibbosaccus, Liebigia),
but others do not (C. lacunosa). Because of its straight fruits,
C. lacunosa (S Thailand, NW Peninsular Malaysia) seems
misplaced among the predominantly twisted-fruited Boea
group. But it must be remembered that some species of Paraboea also possess straight fruits (similar to non-Streptocarpus
taxa among the African and Madagascan taxa), suggesting
that loss of fruit twist can occur frequently. The polyphyly of
Chirita species over different parts of the didymocarpoid
Gesneriaceae, however, is not erratic, but strongly indicates
the artificial nature of the genus and requires a thorough (re)
examination and (re)definition of the entire genus and its future segregates.
Henckelia—This genus was reestablished when splitting the
large genus Didymocarpus into smaller and more natural entities (Weber and Burtt, 1998b). As to the present data, the split
of Didymocarpus proves more than justified. Neither ‘African’
nor ‘South Indian’ nor ‘Malesian Didymocarpus’ (as discussed
in Weber and Burtt, 1998b) are parts of, or closely allied to
‘Didymocarpus s.s.’, which has its center of distribution in the
Himalaya region, but a possible Malay Peninsula origin (Palee
et al., 2006). Because ‘South Indian’ and ‘Malesian’ Didymocarpus as well as Loxocarpus R.Br. appeared somewhat linked,
the genus Henckelia was revived and used in an inclusive sense
for their accommodation (Weber and Burtt, 1998b). The present data give a first indication, though, that Henckelia is not
monophyletic.
Briggsia—This genus has over 20 species, ranging from the
Himalayas to Vietnam. Species number, the wide distribution,
and the wide range of morphologies (including rosette and
caulescent habits, differences in indumentum and anther morphology) allow the prediction that this rather variable taxon is
not monophyletic. Therefore, it is not too surprising that our
molecular data confirm this prediction.
Paraboea—This genus appears to be paraphyletic, with
Trisepalum sharing the polytomy with Paraboea clades and
species in our analysis 3 (Fig. 3). The close relationship of
Paraboea and Trisepalum is undisputed because both have the
characteristic arachnoid indumentum.
Boea—The species analyzed formed two clades in analysis
3, with Spelaeanthus seemingly linked to the Australian / Papua
New Guinean Boea species in one strongly supported clade, the
other in a basal polytomy of the Boea group. However, more
←
Fig. 3. Strict MP consensus tree of 10977 most parsimonious trees of 5694 steps based on combined ITS, trnL-F and atpB-rbcL sequences of 202
samples (CI = 0.47, RI = 0.75, RC = 0.35). Bootstrap values and decay indices (bold and italics) are given above branches. Light gray boxes = Trichosporeae, dark gray boxes = Cyrtandreae; black bars = outgroups, hatched bars = gesnerioid, lined bars = coronantheroid, open bars = didymocarpoid; numbers in bars = number of anthers; p, posterior pair, rest with two anterior anthers. Branches in bold are supported by posterior probabilities of 1.00 (black)
or 0.99 (gray) in the Bayesian analysis. Asterisks indicate generic types. Arrows indicate relationship suggested in the Bayesian analysis.
May 2009]
Möller et al.—Phylogeny of didymocarpoid Gesneriaceae
999
Fig. 4. Plots of branch support values, (A–C) boostrap vs. decay index and (D–F) posterior probabilities of (A, D) the combined trnL-F and ITS; (B,
E) the trnL-F and atpB-rbcL, and (C, F) the trnL-F, atpB-rbcL, and ITS data sets (bootstrap values >50% included only). Only decay values >5 receive
constantly >90% bootstrap values (vertical dotted red lines, top). In the bottom graphs, the diagonal line indicates the hypothetical 1 : 1 relationship between
bootstrap and posterior probabilities. However, in the trnL-F and ITS analysis, branches with boostrap values as low as 51% receive PP values of 1.0 (arrow), for the trnL-F and atpB-rbcL dataset boostrap values as low as 65%, and for the three-gene analysis branches with boostrap values as low as 51%
receive PP values of 0.99 (arrows), illustrating the overoptimism of PP values.
species need to be included and missing data completed in a
future analysis to elucidate the exact relationships in the Boea
group as a whole.
Raphiocarpus— This genus, revived by Weber and Burtt
(1998a) for the accommodation of a number of Sino-Vietnamese species of Didissandra, was noted as potentially artificial
even at its inception. Moreover, the identity of the Raphiocarpus sp. samples included in our analysis cannot be ascertained
at present; these may well be misidentified. Thus, a more detailed analysis is needed for clarification here.
require a detailed morphological discussion of many groups
which cannot be presented here.
Informally, the didymocarpoid Gesneriaceae can be divided
into three groups: (1) the ‘basal Asiatic and European group’;
(2) the ‘African and Madagascan group’; (3) the ‘advanced Asiatic and Malesian group’.
Our phylogenetic results support that the phytogeography
and distribution patterns form an essential component in the understanding of the evolutionary diversification of the didymocarpoid Gesneriaceae. Now we have to discuss whether these
groupings make sense in morphological respects.
Toward a new classification— As discussed, none of the
available classifications and definition of tribes agree with the
data presented here. Obviously, a revised classification needs to
be established. In view of the many isolated genera and cascades of clades (= grades), a formal classification will prove
difficult at this point. In the present paper, we do not attempt to
establish such a formal classification, particularly because the
position of a considerable number of genera (over 30) is still
unknown or uncertain. Such a revised classification would also
‘Basal Asiatic and European group’—This group comprises
a number of mono- or oligogeneric clades that form grades or
polytomies at the base of the didymocarpoid Gesneriaceae
clade. It is not a single taxonomic entity.
Their morphology is varied, some are flat-rosette plants (Jerdonia, Corallodiscus, Ramonda, Haberlea, Jancaea), some are
tall, shrubby (lignescent) plants with decussate (rarely alternate)
leaves (Tetraphyllum, Leptoboea, Boeica, Rhynchotechum),
and one (Platystemma) is a unifoliate herb. Floral form includes
American Journal of Botany
1000
Table 1.
Comparison of different branch support values for branches
between genera (intergeneric), branches supporting genera (generic,
except nonmonophyletic genera) and within genera (intrageneric)
for the three-gene analysis of combined trnL-F, atpb-rbcL, and ITS
data.
Branch support values
Index
Intergeneric
Generic
Intrageneric
Decay index
SE
N
3.57
0.40
82
10.12
2.16
33
3.84
0.45
38
Bootstrap
SE
Branches <50% support
N
82.78
2.04
18
64
94.85
1.91
0
33
88.28
2.19
2
36
Posterior probability
SE
Branches <0.5 support
N
0.96
0.01
13
69
0.99
0.01
1
32
0.97
0.01
1
37
Notes: SE = standard error, N = number of branches.
a full range from strongly zygomorphic with a distinct tube
(Corallodiscus) through slightly zygomorphic with a short,
broad tube (‘campanulate’ = e.g., Jancaea, Rhynchotechum) to
(sub)actinomorphic and flat-faced with very short tube (‘saintpaulioid’ = Ramonda, Platystemma). Thus, morphologically, there
is little evidence that the basal Asiatic and European Gesneriaceae belong together or that they are particularly primitive.
However, there are morphological features that are characteristic for the group and (at least partly) can be qualified as plesiomorphic: (1) Presence of four fertile stamens (tetrandry).
Tetrandy is characteristic of the coronantheroid, gesnerioid, and
epithematoid (except for Epithema Blume and Asian Rhynchoglossum Blume, which possess two fertile anthers in posterior
positions, unlike all other diandrous didymocarpoid taxa where
the anthers are in anterior position. This character state difference for taxa with two stamens was also overlooked by Smith,
1996) and is clearly ancestral within the family (Fig. 3). The
presence of four stamens is also characteristic for the European
group (except Ramonda with five). The African and Madagascan group (except for Acanthonema) and the twisted-fruited advanced Asiatic and Malesian group stamen number is always
two, the derived state, while in the straight-fruited advanced
Asiatic and Malesian group both tetrandrous and diandrous genera/groups occur. (2) Straight capsules with septicidal dehiscence (sometimes combined with loculicidal dehiscence). This
type of fruit opening has already been regarded as primitive by
Fritsch (1893–1894). This assumption was merely for morphological reasons (dehiscence along the lines of carpel fusion), but
can be supported by the fact that it also occurs in presumed
basal members of the New World coronantheroid Gesneriaceae
(Coronanthera Vieill. ex C.B.Clarke, Depanthus S.Moore;
combined with loculicidal dehiscence in Negria F.Muell. and
Rhabdothamnus A. Cunn.) and in the basal gesnerioid tribe
Beslerieae (Anetanthus Hiern ex Benth. & Hook f. and probably
others). (3) Seed cell ornamentation. As can be concluded from
the work of Beaufort-Murphy (1983) and personal observations
of the last author (A.W.), the genera of the basal Asiatic and
European group have seeds without testa cell ornamentation.
Reticulate and striate seeds, without ornamentation on the cell
surfaces, are also characteristic of the coronantheroid, gesnerioid, and epithematoid Gesneriaceae and are thus considered
[Vol. 96
plesiomorphic. These groups also share a twisted testa cell arrangement. Ornamented seeds are found frequently in the African and Madagascan group as well as in the advanced Asiatic
and Malesian group and are therefore derived. Thus, the basal
Asiatic and European genera with plesiomorphic unornamented
seeds and straight testa cell arrangement form a perfect transition to the higher groups of didymocarpoid Gesneriaceae.
‘African and Madagascan group’—While in earlier classifications the African and Madagascan genera appeared scattered
over several tribes, Burtt suggested on many occasions (e.g., in
Hilliard and Burtt, 1971) that they are closely related. In all our
phylogenetic trees, they indeed formed a well-supported clade
and can be considered a coherent taxonomic group. Despite the
huge variation in vegetative and floral characters (even in the
single genus Streptocarpus in the restricted sense), they are tied
together by at least three synapomorphies: (1) Diandry. (2)
Twisted fruits, with loculicidal dehiscence; the most parsimonious interpretation of the straight capsules found in Acanthonema,
Colpogyne, Hovanella, Saintpaulia, and Schizoboea suggests
that they are independent reversals to the ancestral state in the
family. (3) Ornamented seeds with verruculose surface pattern
(but with a reversal to the ancestral, reticulate state in most derived taxa in Streptocarpus subg. Streptocarpus). Before taxonomic changes can be made concerning this group, the status of
the Asian Streptocarpus species needs to be addressed (i.e., their
unrelatedness to African Streptocarpus species demonstrated).
Advanced Asiatic and Malesian group—This group is the
largest of the three groups. It needs detailed discussion, which
is postponed to a future, more complete analysis. This group
comprises, inter alias, the well-known and species-rich genera
Didymocarpus, Aeschynanthus, and Cyrtandra. These genera,
the leading genera of different tribes in former classifications,
thus prove surprisingly closely related. Their characteristic features, including the appendaged seeds of Aeschynanthus and
the indehiscent fruits of Cyrtandra, are obviously convergences, characterizing small groups or single genera, but have no
major classificatory significance. Like the basal Asiatic and European group, it consists of a number of larger clades, starting
with Didissandra (sensu Weber and Burtt, 1998a). This genus
has tetrandrous flowers, capsules of a very special type (tardily
loculicidally dehiscent, with the valves finally disintegrating
along the sclerified vascular bundles (see Weber and Burtt,
1998a), and seeds with mostly knobby ornaments along the
testa cell margins (see Sontag and Weber, 1998).
A well-supported major clade includes the genera with predominantly twisted capsules, the Boea group (Boea, Emarhendia, Kaisupeea, Ornithoboea, Paraboea p.p., Rhabdothamnopsis,
Trisepalum; only Senyumia Kiew, A.Weber & B.L.Burtt has not
been included in the analysis, but probably has also its place
here), but scattered within this group are also species with straight
fruits (Paraboea p.p., Chirita lacunosa, Henckelia ericii). This
group will be discussed in more detail in a forthcoming paper.
The remainder of clades in the advanced Asiatic and Malesian
group are not strongly supported, though many monophyletic
genera are (Fig. 3), and the intergeneric relationships of this group
will be addressed comprehensively in another publication.
Phytogeography— It is still enigmatic in which part of the
world Gesneriaceae originated. Burtt (1998) proposed the hypothesis that the family is of southern hemisphere (Gondwana)
origin, with the coronantheroid Gesneriaceae representing a sur-
May 2009]
Möller et al.—Phylogeny of didymocarpoid Gesneriaceae
vivors of the oldest group. This gave rise both to the gesnerioid
Gesneriaceae (invading South America via the Antarctic and
southern South America) and the didymocarpoid Gesneriaceae
(by migrating northwards, ‘dropping’ representatives in Africa
and Madagascar and finally reaching the Eurasiatic continent
and spreading from there to the Sunda Islands and the Pacific).
This hypothesis faces difficulties both from the geological
time scale and the molecular data. The age of the family has
been variously estimated, from 65 million years (Raven and
Axelrod (1974) to 71 million years (Bremer et al., 2004, though
Peltanthera was used erroneously as a member of Gesneriaceae
here, thus the family maybe younger), but nowhere near a
Gondwana origin (Gondwana break-up began 150 Ma, Storey
et al. 1995). As far as the didymocarpoid Gesneriaceae are concerned, the most basal members are found on the Eurasian continent, especially on the Indian subcontinent: Jerdonia
(mountains of SW India), Corallodiscus (Himalayas and
China), Tetraphyllum, Leptoboea, Boeica (Himalayas and adjacent areas). Only Rhynchotechum, with around 15 species being the largest genus of the group, has a wider distribution. It
spreads from the Himalayas to the Malay archipelago and one
species even reaches New Guinea. This island spreading would
have been aided by the possession of fleshy fruits of the genus,
as in Cyrtandra, that are putatively bird dispersed (Cronk et al.,
2005). The basal Asiatic genera thus can be marked as an essentially ‘Indian group’ with most genera represented in the
Sino-Himalayan area. This point is where the molecular and
phytogeographical data and parts of Burtt’s hypothesis meet.
These genera may well be relicts of a group that had its origin
on the Indian plate. Transgression to the west (Europe) was apparently very early, followed by a transgression to the south
(perhaps first Madagascar and then Africa; the highest morphological diversity occurs in Madagascar, and a subset may have
entered the African mainland 25–35 Ma; Möller and Cronk,
2001b) and—under explosive radiation and diversification—to
the east and southeast (Indochina, Malesia, Pacific). The case of
the widespread Rhynchotechum of the basal Asiatic and European group suggests that a migration from the Himalayas to the
east may have involved several lineages in parallel.
Conclusions— The present work represents a major step forward in our understanding of the largest group of Old World
Gesneriaceae, the ‘didymocarpoid Gesneriaceae’. The molecular data strongly suggest that none of the available current classifications properly reflect phylogeny. Neither the classification
into tribes nor the delimitation of the tribes established so far is
reflected in the molecular phylogenies. All characters that have
been considered to be of major taxonomic value, such as actinomorphic flowers, diandry, indehiscent fruits, appendaged seeds,
were found to be homoplastic, i.e., having evolved several times
independently. Thus, apart from perhaps fruit twist, most other
morphological characters and states are not helpful in shaping a
new classification for the family.
The informal classification proposed by Weber (2004), which
was partly based on unpublished molecular data, is essentially
confirmed here on a much larger data set. No formal taxonomy is
presented at this point, but a new classification and an understanding of the evolutionary pathways is emerging, and it is the biogeography that is best reflected in the resulting phylogenies so far.
This study will provoke a reappraisal of the approach for a
classification of the OW Gesneriaceae if it is to reflect our results obtained here. Even though the epithematoid, basal
Asiatic and European, and African and Madagascan groups are
1001
well defined and supported, relationships among the advanced
Asiatic and Malesian taxa are far from resolved. It is now paramount to obtain a stable phylogeny for this group of Gesneriaceae by adding more taxa and more data.
At present, molecular data for a considerable number of genera of didymocarpoids are still lacking. The bulk will be relevant for the advanced Asiatic and Malesian Gesneriaceae. We
are confident that their inclusion will result in a better resolution of this group and stabilize relationships. Their addition will
also contribute to a better definition of particular genera and
solve problems of generic delimitation. Even now it is clear that
some genera are not monophyletic, that some genera have to be
reduced to synonymy and that new genera have to be established. Much work is waiting.
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1004
American Journal of Botany
[Vol. 96
Appendix 1. List of taxa included in the phylogenetic analysis of Gesneriaceae, including voucher number, deposition of voucher, origin and GenBank sequence
information.(An asterisk [*] denotes generic types; [C] = Chirita section Chirita; [G] = Chirita section Gibbosaccus; [M] = Chirita section Microchirita; [L] =
Chirita section Liebigia.)
Taxon
Voucher number
Deposited in
A.Dahl 703 (trnL-F); cult
RBGE 19832265 (atpB-rbcL)
A.Dahl702 (trnL-F); cult
RBGE 19687553 (atpB-rbcL)
E
E
Tetrachondraceae
Polypremum procumbens L.
Tetrachondra patagonica Skottsb.
Struwe 1000
Martinsson and Swenson 314
UPS
UPS
—
—
Scrophulariaceae
Scrophularia canina L.
Verbascum speciosum Opiz
Perret S1.119
cult. HBV; Kiehn s.n.
G
WU
Oleaceae
Olea europaea L.*
Forsythia ×intermedia Zabel
Plantaginaceae
Antirrhinum majus L.*
Tetranema roseum (Martens & Galeotti)
Standl. & Steyerm. [= T. mexicanum
Benth. ex Lindl.*]
Veronica incana L.
Veronica incana L.
Calceolariaceae
Calceolaria arachnoidea Graham
Jovellana punctata Ruiz & Pavon*
cult. HBV
cult. HB München, Dec. 1997;
Kiehn s.n. (27.4.98)
cult. HB Bonn ex HB Mainz
no. XX-0-MJG-19–47720;
Albach 155
unknown
cult. RBGE 19912379
cult. RBGE 19980599
Gesnerioid
Achimenes admirabilis Wiehler
cult. CJBG, Nov. 1997,
Chautems & Perret 01–033
cult. RBGE 19822666;
Besleria labiosa Hanst.
Wiehler & Steyermark 72453
Besleria melancholica (Vell.) C.V.Morton Chautems, Leitman &
Matinelli 240, 21.5.1987
cult. RBGE 19802568;
Chrysothemis pulchella (Donn ex Sims)
Wiehler
Decne.*
cult. RGBE 19822676;
Cobananthus calochlamys (Donn. Sm.)
H.Wiehler 7553
Wiehler*
cult. HBV, ex HB St. Gallen
Columnea sanguinea (Pers.) Hanst.
1987; Kiehn s.n.
cult. RBGE 19570361
Episcia cupreata (Hook.) Hanst.
cult. RBGE 19782220
Eucodonia verticillata (Martens &
Galeotti) Wiehler*
Skog 7714
Chautems & Perret 97–020
Gesneria humilis L.*
Mendoza-T. et al. 506
Glossoloma bolivianum (Britt.) Wiehler
Chautems & Perret 01–034
Gloxinia erinoides (DC.) Roalson &
Boggan
cult. RBGE 19821486;
Kohleria hirsuta (Kunth) Regel var.
M.Koehnen
hirsuta [K.eriantha (Benth.) Hanst.]
Chautems & Perret 97–018
Kohleria spicata (Kunth) Oerst.
Napeanthus reitzii (L.B.Smith) B.L.Burtt
ex Leeuwenb.
A. Cervi & al. AC479
Nautilocalyx melittifolius (L.) Wiehler
Chautems & Perret 01–025
Nematanthus villosus (Hanst.) Wiehler
Paliavana prasinata (Ker Gawl.) Benth.
Rhytidophyllum tomentosum (L.) Mart.*
Seemannia aff. purpurascens Rusby
Sinningia cardinalis (Lehm.) H.E.Moore
Sinningia schiffneri Fritsch
Smithiantha lauii Wiehler
Perret 99–041
Chautems & Perret 00–013
cult. HBV; Kiehn s.n.
Chautems & Perret 97–019
Chautems & Perret 97–015
Chautems & Perret 97–010
cult. GRF (Gesneriad Research
Foundation, Sarasota, Fl.,
USA), cult. ID = G-3588
Sequence by M. Perret
Origin
atpB-rbcL
trnL-F
ITS1/ITS2
Cyprus; Troodos
FJ501367
AF231866
—
cultivar
FJ501368
AF231824
—
—
—
AJ430938
AJ430939
—
—
—
Austria, exact origin
unknown
AY423105
AJ490885
AY423123
AJ492271
—
—
no voucher unknown origin
WU
Mexico; exact origin
unknown
AJ490883
AJ490884
AJ492270
AJ492272
—
—
WU
unknown origin
—
AY486449
—
—
unknown origin
AY818908
—
—
E
E
Chile, Los Lagos
Chile, Biobío, Prov. de
Arauco:
AY423108
AY423109
AY423126
AY423127
—
—
G
unknown origin
AJ439982
AJ439827
—
E
AY423110
AY423128
—
AJ490923
AJ492310
—
E
Venezuela; Distrito
Federal, Cerro Narguata.
Brazil, Rio de Janeiro,
Macaé de Cima
unknown origin
AJ490925
AJ492312
—
E
Guatemala, Coban
AJ490926
AJ492313
—
WU
unknown origin
AJ490927
AJ492314
—
E
E
unknown origin
unknown origin
AJ490928
FJ501369
AJ492315
—
—
—
USBRG 86–097
cult. CJBG, Oct. 1997
unknown origin
cult. CJBG, Nov. 1997
—
AJ439976
—
AJ439983
AY047120
AJ439821
AY047156
AJ439828
—
—
—
—
E
Ecuador, unknown locality AY423114
AY423132*
—
G
cult. CJBG
AJ439975,
part
AJ493036
AJ439820
—
AJ492321
—
AJ439984,
part
AJ439980
AJ490932
AJ490930
AJ439977
AJ490931
AJ439900
AJ439978
AJ439829
—
AJ439825
AJ492319
AJ492317
AJ439822
AJ492318
AJ439745
AJ439823
—
—
—
—
—
—
—
G
US
G
US
G
UPCB
G
G
G
WU
G
G
G
G
Brazil, PR, Morretes,
Route de la Graciosa,
Volta Grande
unknown origin
cult. CJBG, Sept. 1998
cult. CJBG
unknown origin
cult. CJBG, Oct. 1998
cult. CJBG,
cult. CJBG Oct. 1997
unknown origin
May 2009]
Möller et al.—Phylogeny of didymocarpoid Gesneriaceae
1005
Appendix 1. Continued.
Taxon
Vanhouttea calcarata Lem.*
Coronantheroid
Asteranthera ovata (Cav.) Hanst.*
Fieldia australis Cunn.*
Lenbrasssia australiana (C.T.White)
G.W.Gillett var. australiana*
Mitraria coccinea Cav.*
Rhabdothamnus solandri Cunn.*
Sarmienta scandens (J.D.Brandis) Pers.*
Epithematoid
Epithema benthamii C.B.Clarke
Epithema membranaceum (King) Kiew
Voucher number
Carvalho et al. 526
Deposited in
Origin
atpB-rbcL
trnL-F
ITS1/ITS2
CEPEC
Brazil, State of Rio de
Janeiro, Nova Friburgo
AJ490933
AJ492320
—
Chile, Los Lagos, Prov. de FJ501371
Palena, Chaitén
Australia, unknown
AY423112
locality
Australia, Queensland
AJ490921
FJ501427
—
AY423130
—
AJ492308
—
—
AY423131
—
FJ501370
FJ501426
—
AJ490922
AJ492309
—
Philippines, Luzon,
Isabela
AY423118
AY423135
—
Peninsula Malaysia,
Pahang, Jerantut distr.
Peninsula Malaysia,
Perak, Kinta distr.; Sg.
Siput Selatan
Taiwan, Kaohsiung Hsien:
Tengshih
Cameroon, Kupe village
Peninsula Malaysia,
Pahang; Pulau Tioman
Peninsula Malaysia, near
Sungai Siput Selatan
Borneo, Sarawak, Bkt.
Mentawa
Peninsula Malaysia,
Selangor, Gua Batu
AJ490887
AJ492274
—
AJ490888
AJ492275
—
AJ490889,
part
AJ490890
AJ490891
AJ492276
—
AJ492277
AJ492278
—
—
AJ490892
AJ492279
—
AJ490893
AJ492280
—
AJ490894
AJ492281
—
U91315
AJ492269
—
AJ490895
AJ492282
—
AJ490896
AJ492283
—
AJ490897
AJ492284
—
AJ490898
AJ492285
—
AJ490899
AJ492286
—
AJ490900
AJ492287
—
—
FJ501428
—
AJ490901
AJ492288
—
AJ490902
AJ492289
—
—
FJ501396
FJ501454
FJ501500
FJ501306
—
—
—
AF349218 /
AF349299
—
—
FJ501501
—
—
AY047099
—
AF349203 /
AF349284
AY047040
cult. RBGE 19980608;
UCEXC 362
RBGE 19696862
E
cult. RBGE19970901;
P.D.Hint 6654
cult. RBGE 19792696;
M.Mason
cult. RBGE 19660192
—
cult. RBGE 19882757;
M.Gardner & S.Knees 4033
E
cult RBGE 19972563;
Philippine Expedition 1997
SM9
Weber 860908–2/1
E
E
E
E
WU
Epithema saxatile Blume
Weber & Anthonysamy
870521–3/2 (WU); cult. HBV
WU
Epithema taiwanense S.S.Yin
C.-N. Wang & al.
TNU
Epithema tenue C.B.Clarke
Loxonia hirsuta Jack*
cult. RBGE ex DTH 5815
Weber 870602–1/5
E
WU
Monophyllaea elongata B.L.Burtt
Weber & Antonysamy
870518–1/1
Vogel & Weber 790106–1/1
WU
Chin & Weber, Chin 2107
(KLU) = Vogel & Weber
790801
cult. HBV, seeds rec. from
RBGE
Huber & Weissenhofer 722
WU
Monophyllaea glauca C.B.Clarke
Monophyllaea hirticalyx Franch.
Monophyllaea horsfieldii R.Br.*
Rhynchoglossum azureum (Schltdl.)
B.L.Burtt
Rhynchochlossum notonianum (Wall.)
B.L.Burtt
Rhynchoglossum obliquum Blume*
[Malay Peninsula]
Rhynchoglossum obliquum Blume*
[Philippines]
cult. HB München
Weber 870510–1/3
Mendum & al. 25349
C.-N. Wang & al.
Rhynchoglossum obliquum Blume var.
hologlossum (Hayata) W.T.Wang [Taiwan]
Weber 870602–1/1
Stauranthera grandiflora Benth.*
Whytockia purpurascens Y.Z.Wang
MMO 01–87
Whytockia sasakii (Hayata) B.L.Burtt
C.-N. Wang & al.
Whytockia tsiangiana (Hand.-Mazz.)
A.Weber
1986 Sino-Amer. Exedition
Nr. 200
Didymocarpoid:
Acanthonema strigosum Hook.f.*
Aeschynanthus austroyunnanensis
W.T.Wang
Aeschynanthus austroyunnanensis
W.T.Wang
Aeschynanthus bracteatus Wall. ex DC.
Aeschynanthus bracteatus Wall. ex DC.
Aeschynanthus hildebrandtii Hemsl.
B.Macinder 49
MMO 01–79
WU
Argentina, Bariloche
Region
New Zealand, North
Island
Chile, Región X Los
Lagos, Prov. de Osorno
WU
Peninsula Malaysia,
Selangor, Batu Caves
WU
Costa Rica, Prov.
Alajuela; Valle Virgen
no voucher unknown origin
WU
E
TNU
WU
E, WU
TNU & E
WU
K
E, WU
Peninsula Malaysia,
Pahang, Lipis district
Philippines, Palawan,
betw. San Rafael and
Cleopatra Needle
Taiwan, Kaohsiung Hsien:
Tengshih
Peninsula Malaysia,
Pahang; Pulau Tioman
China, Yunnan, Maguan
county
Taiwan, Hualian Hsien,
Hsiulin Hsiang
China, Guizhou Prov.,
Jiangkou county
cult RBGE 19951561; A.Reid
& J.Fernie 004
E
Wang 991113
cult RBGE 19970165;
R.Cherry 123
Skog 7777
PE
E
Cameroon, Kupe village
China, Yunnan, Hekou
county,
China; Yunnan,
Xishuangbanna Dai Aut.
Pref.
China, Yunnan, Xichou
Viet Nam; Lao Cai
US
unknown origin
American Journal of Botany
1006
[Vol. 96
Appendix 1. Continued.
Taxon
Voucher number
Deposited in
Aeschynanthus lancilimbus W.T.Wang
Aeschynanthus longiflorus (Blume) DC.
Wang S-10868
Weber 950905 (photo record)
PE
WU
Aeschynanthus longiflorus (Blume) DC.
Agalmyla biflora (Elmer) O.M.Hilliard &
B.L.Burtt
cult RBGE 19680624
cult. RBGE 19980287, DNA
no. AG04
E
E
Agalmyla biflora (Elmer) O.M.Hilliard &
B.L.Burtt
Agalmyla clarkei (Elmer) B.L.Burtt
E
Agalmyla clarkei (Elmer) B.L.Burtt
cult RBGE 19980292, RBGEPNHE1998–25517
cult. RBGE 19991911, Royal
Botanic Garden EdinburghPhilippine National Herbarium
Expedition 1999(P99) 13
cult RBGE 19972530A,
Agalmyla parasitica (Lam.) Kuntze*
5.9.95 Weber
WU
Ancylostemon aureus (Franch.)
B.L.Burtt
Ancylostemon convexus Craib
MMO 01–153
E, WU
MMO 01–176
E, WU
E
E
Anna mollifolia (W.T.Wang)
W.T.Wang & K.Y.Pan
Anna submontana Pellegr.*
MMO 01–146
E, WU
MMO 01–85
E, WU
Boea hygrometrica (Bunge) R.Br.
Boea hygroscopica F.Muell.
Gu 01–6184
Weber 810808–1/1
KUN
WU
Boea hygroscopica F.Muell.
B. Tan, R.G.Coveny &
E.A.Brown 443, cult
19970386
Lambinon 87/830
Boea magellanica Lam.*
MMO 01–182B ex Zhang
Chang Qin 200012
Gu 99–705
Boeica porosa C.B.Clarke
Briggsia longipes (Hemsl. ex Oliv.) Craib MMO 01–122
Boeica ferruginea Drake
E
L
E, WU
KUN
E, WU
Briggsia mihieri Craib
Wang 11315B
PE
Briggsia muscicola (Diels.) Craib
Briggsia rosthornii (Diels) B.L.Burtt
Kew (1995–2229)
Sino-Amer. Guizhou Botanical
Expedition 398 (US 229325)
MMO 01–141
K
US
Calcareoboea coccinea C.Y.Wu ex
H.W.Li*
Chirita asperifolia (Blume) B.L.Burtt [L] P.Woods 1071, 30.4.1968
(C6570)
cult. HBV GS-96–02 ex HB
Chirita caliginosa C.B.Clarke [M]
München-Nymphenburg;
Kiehn & Pfosser 2000–1
cult. Smithsonian 94–085,
Chirita flavimaculata W.T.Wang [G]
Skog 7735 (US 590933)
cult. RBGE 19941913,
Chirita gemella D.Wood [G]
Averyanov, L. 1987
Panigrahi 12231, 1969
Chirita hamosa R.Br. [M]
(C8032H)
cult RBGE 19972897
Chirita lacunosa (Hook f.) B.L.Burtt
[C]
Chirita lavandulacea Stapf. [M]
Chirita longgangensis W.T.Wang [G]
Chirita pinnata W.T.Wang [G]
Chirita pinnatifida (Hand.-Mazz.)
B.L.Burtt [G]
Chirita pumila D.Don [C]
cult. RBGE 20000897
cult. RBGE 19941915.
Takhtajan, A. & Aruzytov, N.
1975
Expedition Beijing 896526
(US 294374)
Xie Qingjian J-037 (US
422838)
cult. RBGE 19962271,
Gaoligong Shan Expedition
1996 7938
E, WU
E
WU
US
Origin
China, unknown locality
—
Peninsula Malaysia,
AJ490920
Perak, Larut distr.
Peninsula Malaysia
—
Philippines, Palawan,
FJ501421
Near summit of Cleopatra
Needle
Philippines; Palawan, near
—
Thumb Peak
Philippines, Leyte, Leyte
—
Island, Mt. Lobi,
Philippines, Luzon,
Barangay Penicuason
Peninsula Malaysia;
Maxwell’s Hill
China, Yunnan, Binchuan
county,
China, Yunnan, Dali Co.,
Yu Dai Lu, Cang Shan,
China, Guangxi, Napo
county
China, Yunnan, Maguan
county
China, unknown locality
Australia, N Queensland,
Palmerston N.P.
Australia, N Queensland,
Tchupala Falls
US
E
—
trnL-F
ITS1/ITS2
FJ501499
AJ492307
—
—
—
FJ501541
FJ501333
-
—
FJ501361
FJ501540
—
—
FJ501360
FJ501420 FJ501539, part
—
FJ501398
FJ501505
FJ501336
—
FJ501506
FJ501337
—
FJ501543
FJ501422
FJ501542
AF055050 /
AF055051
FJ501362
—
—
FJ501476
FJ501577
FJ501319
—
—
—
FJ501320
—
FJ501478
FJ501321
FJ501379
FJ501440
—
FJ501380
FJ501423
FJ501441
FJ501545
—
FJ501544
—
AF055052 /
AF055053
FJ501363
—
FJ501425
FJ501548
FJ501547
FJ501366
FJ501365
FJ501406
FJ501516
FJ501365
FJ501419,
part
FJ501391
FJ501538
FJ501359
FJ501488
FJ501325
—
FJ501525
—
FJ501408
FJ501523
FJ501345
FJ501392
FJ501489
—
FJ501384,
part
FJ501458
FJ501308
FJ501390
AJ490903
FJ501487
AJ492290
FJ501324
FJ501347
China, Guangxi, Rongshui
—
Xian
China, Guangdong Prov.,
—
Lianxian county
China, Yunnan, Nujiang
FJ501393,
Lisu Aut. Pref., Fugong
part
county
FJ501526
FJ501349
FJ501527
FJ501350
FJ501491
FJ501327
Papua New Guinea,
Morobe Province
China, SE Yunnan
China, unknown locality
China, Yunnan, Xichou
county
China, Chongqing,
Nanchuan
unknown origin
China, Guizhou Prov.,
Jiangkou Xian
China, Guangxi, Napo
county
Indonesia, Java, forest
above Tjibodas Garden
Peninsula Malaysia
China, Guangxi, leg. in
US 11.03.1996
E
Viet Nam, Hong Quang
Special Region, Cat Hai
E
India, Allahabad,
Meizapus
no voucher Peninsula Malaysia,
Pahang, Lipis distr., Gua
Rusa
E
China
E
Viet Nam
US
atpB-rbcL
May 2009]
Möller et al.—Phylogeny of didymocarpoid Gesneriaceae
1007
Appendix 1. Continued.
Taxon
Voucher number
cult. RBGE 19791050.
Godfrey,
T.C. 369
ex Smithsonian Institute 94–
Chirita spadiciformis W.T.Wang [G]
087, cult. RBGE 19951205
Chirita urticifolia Buch.-Ham. ex D.Don* EMAK 109 H 20.9.1991
(Edinburgh-Makalu
[C]
Expedition 1991)
Skog 7736 (US 590934)
Chirita walkeri Gardner [C]
Chirita sinensis Lindl. [G]
Chiritopsis repanda W.T.Wang var.
guilinensis W.T.Wang*
Colpogyne betsiliensis B.L.Burtt*
Conandron ramondioides Sieb. & Zucc.*
Deposited in
Origin
atpB-rbcL
trnL-F
ITS1/ITS2
E
China, Hong Kong
FJ501409,
part
FJ501524
FJ501348
E
China
AJ490904
AJ492291
FJ501346
E
Nepal, Sankhuwasabha
distr., Arun valley
—
FJ501492
FJ501328
FJ501490
FJ501326
AJ492292
FJ501351
FJ501445
FJ501515
FJ501302
FJ501340
FJ501432
—
FJ501431
—
FJ501430
—
US
cult. RBGE 19951206
E
MM 9894C
cult. RBGE 19691267; Takeda
Herbal Garden Kyoto
MMO 01–138
E
E
Sino-America Bot. Expedition
1429
cult. RBGE 19943415A, AGS
Expedition 1994–1622
US
Corallodiscus conchifolia Batalin
Cyrtandra cupulata Ridl.
Wang, Hong et al 105
Weber 840806–2/4
E
WU
Cyrtandra glabra Banks ex Gaertn.
Cronk & Percy T91
Cyrtandra longifolia (Wawra) Hillebr. ex
C.B.Clarke
Cyrtandra pendula Blume
cult. HBV; Kiehn 920825–2/1
WU
China, Yunnan, Xichou— FJ501374
Napo
China, Yunnan Prov.,
FJ501373
Kunming Municipality
China, Yunnan, Dêqên
—
Zang Aut. Reg.,
Zhongdian county
China, unknown locality
FJ501375
Pensinsula Malaysia,
FJ501414
Perak, Maxwell’s Hill
French Polynesia: Society AY423119
Is.: Tahiti: Mt. Tearoa Col
USA, Hawaii, Kauai
FJ501413
cult. HBV; Weber &
Anthonysamy 860730–1/2
cult. HBV; Smith 3905/GES
WU
Peninsula Malaysia
Corallodiscus lanuginosus
(Wall. ex R. Br.) B.L.Burtt (G79)*
Corallodiscus lanuginosus
(Wall. ex R. Br.) B.L.Burtt (G8)*
Corallodiscus sp.
E, WU
cult. Smithsonian 94–250,
—
origin: Sri Lanka; leg. in
US 11.03.1996
China, Guangxi, Zhuang
AJ490905
Aut. Reg.
Madagascar, Fianarantsoa
—
Japan
FJ501405
E
E
USA, Hawaii, Maui, East
Maui
Kapua & al. s.n.
SRP (photo USA, Hawaii, Oahu
Cyrtandra sessilis H.St.John
voucher)
WU
Peninsula Malaysia,
Didissandra frutescens (Jack) C.B.Clarke Weber 840805–1/2 (DI01)
Perak, Maxwell´s Hill
WU
Peninsula Malaysia,
Didissandra frutescens (Jack) C.B.Clarke Weber 840805–1/2 (MB)
Perak, Maxwell´s Hill
cult. RBGE 19650167, Jong
E
Peninsula Malaysia,
Didymocarpus antirrhinoides A.Weber
9009
Perak, Bujong Melakah,
Ipoh.
GZU
Nepal, Langtang Area (N
Didymocarpus aromaticus Wall. ex D. Don Poelt s.n. sub GZU Inv.-Nr.
109–86
Kathmandu)
cult. RBGE 19830510; P.Davis
E
Peninsula Malaysia,
Didymocarpus citrinus Ridl.
69437
Perlis, Kedat Peak
Weber 860816–2/1
WU
Peninsula Malaysia,
Didymocarpus cordatus Wall. ex DC.
Perak, Maxwell’s Hill
Noltie, Pradhan, Sherub &
E
Bhutan, Deothang District
Didymocarpus podocarpus C.B.Clarke
Wangdi 193, NPSW 193
Wang 991106
PE
China, Yunnan, Pingbian
Didymocarpus purpureobracteatus
W.W.Sm.
MMO 01–70
CM
China: Yunnan, Pingbian
Didymocarpus purpureobracteatus
W.W.Sm.
MMO 01–156
E, WU
China, Yunnan, Binchuan
Didymocarpus stenanthos C.B.Clarke
county
Weber & Anthonysamy
WU
Peninsula Malaysia,
Emarhendia bettiana (M.R.Hend.)
860825–1/1; cult. HBV.
Pahang, Kuantan distr.
Kiew, A. Weber & B.L.Burtt*
cult. RBGE 19754106
E
(Greece)
Haberlea rhodopensis Friv.*
cult. RBGE 19951207
E
unknown origin
Hemiboea bicornuta (Hayata) Ohwi
Gu G3
KUN
China, unknown locality
Hemiboea cavaleriei H.Lev.
Wang 11317
PE
China, Chongqing,
Hemiboea gracilis Franch.
Nanchuan
Wang 11306
PE
China, Chongqing,
Hemiboea subcapitata C.B.Clarke
Chengkou
Weber 840805–1/12
WU
Peninsula Malaysia,
Henckelia albomarginata (Hemsl.)
Perak, Maxwell’s Hill;
A.Weber
base
Cyrtandra platyphylla A.Gray
SRP
FJ501433
FJ501532
—
AY818826 /
AY818861
AY423136* FJ501353
FJ501531
FJ501412
FJ501530
AY818846 /
AY818881
FJ501354
FJ501410
FJ501528
—
FJ501411
FJ501529
—
U91313
FJ501521
—
—
FJ501522
—
—
FJ501513
DQ912671
FJ501402
FJ501511
—
AJ490906
AJ492293
DQ912669
—
AJ492294
DQ912673
FJ501404
FJ501514
DQ912688
FJ501401
FJ501510
—
—
—
DQ912676
FJ501403
FJ501512
DQ912687
AJ490908
AJ492295
—
AJ490909
FJ501416
FJ501415
—
AJ492296
FJ501534
FJ501533
FJ501536
—
FJ501356
FJ501355
—
FJ501417
FJ501535
FJ501357
AJ490910
AJ492297
—
American Journal of Botany
1008
[Vol. 96
Appendix 1. Continued.
Taxon
Henckelia corrugata Mendum
Henckelia ericii A. Weber [= Loxocarpus
holttumii M.R.Hend.]
Henckelia floccosa (Thwaites) A.Weber &
B.L.Burtt
Henckelia humboldtiana (Gardner)
A.Weber & B.L.Burtt
Hovanella madagascarica (C.B.Clarke)
A.Weber & B.L.Burtt*
Hovanella sp. nov.
Jancaea heldreichii Boiss.*
Kaisupeea herbacea (C.B.Clarke)
B.L.Burtt*
Leptoboea multiflora (C.B.Clarke)
Gamble* subsp. grandifolia B.L.Burtt
Loxostigma cavaleriei (H.Lev. & Van.)
B.L.Burtt
Loxostigma fimbrisepalum K.Y.Pan
Loxostigma griffithii (Wight) C.B.Clarke*
Voucher number
Deposited in
Origin
atpB-rbcL
trnL-F
ITS1/ITS2
cult RBGE 19981788, RBGEPNH Expedition 1998, DNA
no. D12
Weber 840723–1/2
E
Philippines, Palawan,
Cleopatra Needle
—
FJ501484
—
WU
Malaysia, Malaya
—
FJ501479
—
G 157 Jang
WU
Sri Lanka
—
FJ501486
—
Sri Lanka, Gombiya
Ridge
Madagascar, Antsiranana
Prov.
Madagascar, Toamasina
FJ501389
FJ501485
—
—
FJ501451
—
—
FJ501452
—
Greece, Mt Olymp
Thailand, Prov.
Chachoengsao, Khao Tak
Groep
Thailand, SE, Khaso Phra
Bat, N of Chanthaburi
China, Yunnan, Xichou
Co., Far Dou
China, Yunnan, Jinping
Nepal, Yamphudin
FJ501378
FJ501385
FJ501439
FJ501459
—
FJ501309
FJ501381
FJ501442
—
—
FJ501509
FJ501355
FJ501399
FJ501400
FJ501507
FJ501508
—
FJ501338
E
China, Yunnan, Nujiang
AY423137
Lisu Aut. Pref., Gongshan
AY423137
—
PE
E
China, unknown locality
China, Yunnan, Nujiang
Lisu Aut. Pref.,
—
FJ501394
FJ501498
FJ501495
FJ501332
AF349152 /
AF349233
China, Yunnan, road to
Xichou, Cheng Jia Po
China, Yunnan, road to
Xichou, Cheng Jia Po
Japan, unknown locality
China, unknown locality
China, Hunan Prov.,
Xining county
China, Guizhou Prov.
Yinjiang county
China; Guizhou, Jiangkou
FJ501395
FJ501497
FJ501331
—
FJ501496
—
FJ501424
—
—
FJ501546
FJ501483
FJ501482
FJ501364
—
—
—
FJ501481
—
—
—
FJ501323
Thailand, Chiang Mai,
Doi Chiang Dao
China, Yunnan, Xichou
Thailand; Chiang Mai,
Grasshopper cave
Peninsula Malaysia,
Kedah, Pulau Langkawi,
Bukit Terbak
Peninsula Malaysia,
Pahang, Lipis distr., Gua
Bama
Peninsula Malaysia,
Perak, Kinta distr.
China, Yunnan, Maguan
county
China, Guangdong Prov,
Lianxian county
Peninsula Malaysia,
Kedah, Pulau Langkawi,
Selat Panchar
Peninsula Malaysia,
Kedah, Pulau Langkawi,
Pulau Dayang Bunting
Peninsula Malaysia,
Kedah, Pulau Langkawi
FJ501387
FJ501461
FJ501312
—
FJ501386
FJ501462
FJ501460
FJ501313
FJ501311
—
FJ501464
FJ501314
—
FJ501465
—
AJ490911
AJ492298
FJ501315
—
FJ501472
FJ501318
—
FJ501463
—
—
FJ501471, part
—
—
FJ501467
—
—
FJ501466
—
Kostermans 28519
L
MM 9880A
E
T.Sieder & M.Pfosser 101;
9.2.2000
cult. RBGE 19771605
cult. RBGE 19972918;
K.Larsen 44272, 6 Nov 1993.
Larsen et al. 32065, 26.8.1972
MMO 01–131
WU
photo E
E
E
E, WU
Lysionotus pauciflorus Maxim.
Wang 991005
cult. RBGE 19892473A; Kew/
Edinburgh Kanchenjunga
Expedition (1989) 940.
cult. RBGE 19962309,
Gaoligong Shan Expedition
1996 GSE96–7668
Wang S-10669
cult. RBGE 19962269A,
Gaoligong Shan Expedition
1996 7925
MMO 01–101
E, WU
Lysionotus petelotii Pellegr.
MMO 01–100
E, WU
Opithandra primuloides (Miq.) B.L.Burtt*
Oreocharis aurea Dunn.
Oreocharis auricula
(S. Moore) C.B.Clarke G03
Oreocharis auricula
(S. Moore) C.B.Clarke G04
Oreocharis auricula (S. Moore)
C.B.Clarke G04
Ornithoboea arachnoidea (Diels)
Craib
Ornithoboea wildeana Craib
Ornithoboea sp. nov.
cult. RBGE 19842178A
Wang S-10725
Luo Lin-bo 0125
E
PE
WU
Sino-America Expedition 1832
WU
Loxostigma sp.
Lysionotus chingii Chun ex W.T.Wang
Lysionotus forrestii W.W.Sm.
PE
E
MMO 03–304
E
cult RBGE 19972903
E
Wang 00401
MMO-04–439
PE
E
Paraboea acutifolia (Ridl.) B.L.Burtt
Weber 86805–2/1
WU
Paraboea brachycarpa (Ridl.) B.L.Burtt
Weber 870508–2/6
WU
Paraboea capitata Ridl. var. capitata
Weber 870522–5/2; cult. HBV.
WU
Paraboea crassifolia (Hemsl.) B.L.Burtt
MMO 01–83
Paraboea dictyoneura (Hance) B.L.Burtt
Paraboea ferruginea (Ridl.) Ridl.
Xie Qingjian J-040 (US
422817)
Weber 860806–1/2
WU
Paraboea lanata (Ridl.) B.L.Burtt
Weber 860807–1/2
WU
Paraboea laxa Ridl.
C 4197
E, WU
US
E
May 2009]
Möller et al.—Phylogeny of didymocarpoid Gesneriaceae
1009
Appendix 1. Continued.
Taxon
Paraboea rufescens (Franch.) B.L.Burtt
(G23b)
Paraboea rufescens (Franch.) B.L.Burtt
(G72)
Paraboea rufescens (Franch.)
B.L.Burtt var. umbellata (Drake) K.Y.Pan
Paraboea sinensis (Oliv.) B.L.Burtt (G20)
Paraboea sinensis (Oliv.)
B.L.Burtt (G21b)
Paraboea swinhoei (Hance) B.L.Burtt
Petrocodon dealbatus Hance*
Petrocosmea kerrii Craib
Petrocosmea minor Hemsl.
Petrocosmea nervosa Craib
Petrocosmea sericea C.Y.Wu ex H.W.Li
Platystemma violoides Wall.
Voucher number
Deposited in
Sino-Amer. Bot. Exped 1566
(US 64646)
MMO 01–99
E, WU
MMO 01–147
E, WU
Wen He Qun W049 (US
329798)
Xie Qingjian J-003 (US
422825)
Wagner 6640 (US 427725)
Xie Qingjian J-042 (US
422841)
cult. RBGE 19715592
Sino-Amer. Bot. Exped. 1574
(US 56119)
cult. RBGE 19933232,
SI.78–057
Gu 99–1104
Projektteam 197–241
US
US
US
US
US
E
US
E, US
KUN
WU
cult. RBGE 19951540, Xie,
Q.J. & Ye, C.X.
cult. RBGE 19711477
cult. RBGE 19784020
E
Raphiocarpus begoniifolius (H.Lev.)
B.L.Burtt
Raphiocarpus sp. (G61)
Wang 991108
PE
MMO 01–55
E, WU
Raphiocarpus sp. (G64)
MMO 01–69
E, WU
Raphiocarpus sp.
Beijing Youth team 572
Primulina tabacum Hance*
Ramonda myconi (L.) Rchb.*
Ramonda nathaliae Panc. & Petr.
Raphiocarpus petelotii (Pellegr.)B.L.Burtt cult RBGE 19982405;
S.Goodwin & R.Cherry
92/208
ex Kew 1988 4866
Rhabdothamnopsis sinensis Hemsl.*
RBGE 1997 2562; RBGERhynchotechum discolor (Maxim.)
PNH Expedition 1997/SM8
B.L.Burtt
M.Mendum, G.Argent,
Rhynchotechum parviflorum Blume
Hendrian 00148; coll
25.2.2000
Weber 870420–2/4
Ridleyandra porphyrantha (Kiew & A.
Weber) A. Weber
Saintpaulia tongwensis B.L.Burtt
Saintpaulia velutina B.L.Burtt
Schizoboea kamerunensis K.Fritsch
(B.L.Burtt)*
Spelaeanthus chinii Kiew, A.Weber
& B.L.Burtt*
E
E
PE
E
K
E
E
WU
cult. RBGE 19850668,
I.C.Mather 2
cult. RBGE 19872179
E
J.Lewalle 6693, 9.4.1972
E
Weber 860709–2/2
E
WU
Origin
atpB-rbcL
trnL-F
ITS1/ITS2
—
FJ501468
—
FJ501388
FJ501469
FJ501316
—
FJ501470
FJ501317
—
FJ501473
—
—
FJ501474
—
—
FJ501418
FJ501475
FJ501537
—
FJ501358
FJ501397,
part
—
FJ501502
FJ501334
FJ501504
—
AJ490912
AJ492299
FJ501335
—
FJ501382
FJ501503
FJ501443
—
—
AJ490913
AJ492300
FJ501352
AJ490914
—
AJ492301
FJ501438
—
—
—
FJ501517
FJ501342
—
FJ501493
FJ501329
—
FJ501494
FJ501330
FJ501407
FJ501519
FJ501344
—
FJ501518
FJ501343
China, unknown locality
Philippines; Luzon,
Isabela
Central Sulawesi, Mt
Sojol.
AJ490915
FJ501376
AJ492302
FJ501436
FJ501310
—
FJ501377
FJ501437
—
Malaysia, Pahang, side
ridge of Gunung Bunga
Buah
Tanzania, Tanga Region
—
FJ501520
—
—
FJ501446
FJ501303
AJ490916
AJ492303
FJ501304
—
FJ501453
FJ501305
—
FJ501457
FJ501307
—
FJ501449
AF316903
—
FJ501448
AF316905
—
FJ501456
AF316951
—
FJ501450
AF316907
AJ492304
AF316917
FJ501455
AF316926
China, Yunnan Prov.,
Lunan Xian
China, Yunnan, Xichou,
Cheng Jia Po
China, Guangxi, Napo,
Nong Bu
China, Guangxi Prov.,
Napo county
China, Guangxi Prov.
Jingxi county
Taiwan, Taoyuan Hsien
China, Guangdong Prov.,
Lianxian county
unknown origin
China, Yunnan Prov.,
Lunan Xian
China, N Yunnan
China, unknown locality
Nepal, SE Kathmandu
Pulchoki
China, Guangdong, Lian
River
Spain, Pyrenees
Macedonia, unknown
locality
China, Yunnan, Yuanyang
China, Yunnan, Pingbian
Co., Dar Wei Shang
China, Yunnan, Pingbian
Co., Dar Wei Shang
China, Kwangsi
(Guangxi)
Viet Nam, Lao Cai Prov.
Tanzania; unknown
locality
Burundi, Muramvya,
Mount Teza
Peninsula Malaysia,
Pahang, Jerantut distr.,
Taman Negara
Madagascar, Tuléar Prov.,
Ranomafana
Madagascar, Tuléar Prov.,
Ranomafana
Swaziland, Mbabane
MM 9717
E
MM 9715
E
E
Streptocarpus hilsenbergii R.Br.
cult. RBGE 19941745, Isobel
La Croix
cult. RBGE 19631505
E
Madagascar, Mandrake
Valley
Streptocarpus holstii Engl.
cult. RBGE 19592272
E
Streptocarpus ibityensis Humbert
cult. RBGE 19932867,
E.Fischer 250/93
E
Tanzania, unknown
AJ490917
locality
Madagascar, Antananarivo
—
Prov.
Streptocarpus andohahelensis
Humbert
Streptocarpus beampingaratrensis
Humbert var. beampingaratrensis
Streptocarpus dunnii Hook.f.
American Journal of Botany
1010
Appendix 1. Continued.
Taxon
Voucher number
Deposited in
atpB-rbcL
trnL-F
ITS1/ITS2
—
FJ501480
FJ501322
—
FJ501444
AF316929
AJ490918
AJ492305
AF316979
FJ501383
—
FJ501447
—
—
AF316914
—
FJ501434
—
—
FJ501435
—
AJ490919
AJ492306
—
no voucher India
FJ501372
E
Taiwan, unknown locality AY423111
FJ501429
AY423129
—
—
Streptocarpus orientalis Craib
A.Weber & M.Kiehn 29.9.98
Streptocarpus papangae Humbert
MM 9718
E
Streptocarpus rexii Lindl.*
cult. RBGE 19870333, K.Jong
E
Streptocarpus saxorum Engl.
Streptocarpus saxorum Engl.
Tetraphyllum roseum Stapf (G113)
Chautems & Perret 01–023
cult. RBGE 19721499;
I.C.Mather 4
Kurzweil HK 798
Tetraphyllum roseum Stapf (G124)
Larsen & al. 31190
E
Trisepalum speciosum (Ridl.) B.L.Burtt
Weber 860805–1/1
WU
Unassigned:
Jerdonia indica Wight*
Titanotrichum oldhamii (Hemsl.)
Soler.*
G 155 Jang
cult. RBGE 19973433
E, WU
MP
WU
Origin
Thailand, Prov. Chiang
Mai
Madagascar, Tuléar Prov.,
Ranomafana
South Africa, NE Cape
Prov., Grahamstown
cult. CJBG
Tanzania, Tanga region
Thailand, Krabi Prov., c.
20km N of Krabi
Thailand, Lam Tok Lam
Pae
Peninsula Malaysia,
Kedah, Pulau Langkawi,
Bukit Puteh