TAXON 59 (1) • February 2010: 125–133
Yuan & al. • Phylogeny of Clerodendrum and allied genera
Further disintegration and redefinition of Clerodendrum (Lamiaceae):
Implications for the understanding of the evolution of an intriguing
breeding strategy
Yao-Wu Yuan,1,2 David J. Mabberley, 3,4 Dorothy A. Steane5 & Richard G. Olmstead1
1 Department of Biology, University of Washington, Box 355325, Seattle, Washington 98195-5325, U.S.A.
2 Current address: 4504 Miller Plant Sciences Building, Department of Plant Biology, University of Georgia, Athens,
Georgia 30602, U.S.A.
3 University of Washington Botanic Gardens, College of Forest Resources, Box 354115, Seattle, Washington 98195-4115, U.S.A.
4 Current address: Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AB, U.K.
5 School of Plant Science, University of Tasmania, Private Bag 55, Hobart, Tasmania 7001, Australia
Author for correspondence: Yao-Wu Yuan, yyuan@plantbio.uga.edu
Abstract The genus Clerodendrum s.l. is polyphyletic. Although recent studies have resulted in C. subg. Cyclonema and C. sect.
Konocalyx being removed to the resurrected genus Rotheca, and the unispecific genus Huxleya being sunk into Clerodendrum,
it has been unclear whether Clerodendrum as currently circumscribed is monophyletic, particularly in relation to the American
genera Aegiphila, Amasonia, and Tetraclea. This phylogenetic study employs four relatively fast-evolving chloroplast DNA regions, trnT-L, trnL-F, trnD-T, and trnS-fM, to clarify the generic boundaries of Clerodendrum and its relationship to allied genera.
The results corroborate previous studies that there are three well-supported clades in the currently recognized Clerodendrum: an
Asian clade, an African clade, and a Pantropical Coastal clade. The Asian clade and African clade are sister groups and together
form a monophyletic group. However, the Pantropical Coastal clade is more closely related to the three American genera than it
is to the other two Clerodendrum clades. In addition, a Caribbean species, C. spinosum, is found to be more closely related to the
American genera than it is to any of the three major Clerodendrum groups. These results indicate that Clerodendrum as currently
circumscribed is not monophyletic. We propose to separate the Pantropical Coastal clade and C. spinosum by reviving the genera
Volkameria (including Huxleya) and Ovieda, respectively for these, and to restrict Clerodendrum to the Asian and African clades.
Brief descriptions of the genera to be recognized are provided. All Neotropical ‘Clerodendrum’ taxa are referred to other genera,
necessitating six new combinations, which are also provided, where required, for two other well-studied Old World Volkameria
species; all names ever used in Ovieda are given their modern placings (two placed newly in synonymy). The study also sheds light
on the evolution of an intriguing breeding strategy that avoids self-pollination or/and sexual interference. This strategy involves
presentation of pollen and stigma in the centre of the flower in a sequential fashion by moving the filaments and style. It appears
to have evolved in the common ancestor of Clerodendrum, Volkameria, Ovieda, Amasonia, Tetraclea, Aegiphila and Kalaharia,
and still occurs in all of these taxa except Aegiphila, where it has been succeeded by a heterostylous system.
Keywords Aegiphila; breeding strategy; chloroplast DNA; Clerodendrum; Huxleya; Ovieda; phylogeny; Volkameria
INTRODUCTION
The genus Clerodendrum L. as delimited by nineteenthcentury botanists (Schauer, 1847; Briquet, 1895) is heterogeneous. However, this delimitation has been followed reasonably
closely by subsequent authors, even though they recognized
it to be problematic (Lam, 1919; Thomas, 1936; Moldenke,
1985; Verdcourt, 1992). Cladistic analyses of morphological
data (Cantino, 1992; Rimpler & al., 1992) provided preliminary
evidence that Clerodendrum sensu lato (s.l.) was not monophyletic. But these analyses, primarily focused at subfamily or
family level, included relatively few Clerodendrum s.l. species
and did not provide good resolution of relationships within
Clerodendrum s.l. or between the genus and other related
ones. Phylogenetic studies based on chloroplast DNA (cpDNA)
restriction site data (Steane & al., 1997) and nuclear ITS sequences (Steane & al., 1999), with extensive sampling within
Clerodendrum s.l. and related genera, strongly suggested that
Clerodendrum s.l. is polyphyletic. Subsequently, a number of
species comprising the C. subg. Cyclonema (Hochst.) Gürke
and C. sect. Konocalyx (Thomas) Verdc. were removed to the
resurrected genus Rotheca Raf. (Steane & Mabberley, 1998). In
addition, the molecular studies divided Clerodendrum (sensu
Steane & Mabberley, 1998) into three major clades that are in
general associated with geographic distribution: an Asian clade,
an African clade, and a Pantropical Coastal clade (Fig. 1A).
A more recent study (Steane & al., 2004) which included
three New World genera, Aegiphila Jacq., Amasonia L. f., and
Tetraclea A.Gray, and a unispecific Australian genus Huxleya
Ewart, put the delimitation of Clerodendrum (sensu Steane
& Mabberley, 1998) into question again. Huxleya was found
nested within the Pantropical Coastal clade and therefore was
sunk into the genus Clerodendrum (Steane & al., 2004). The
African and Asian clades were still recovered as sister groups
and together formed a monophyletic group (Fig. 1B). The three
New World genera, Aegiphila, Amasonia, and Tetraclea, each
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TAXON 59 (1) • February 2010: 125–133
Yuan & al. • Phylogeny of Clerodendrum and allied genera
represented by a single species in that study, formed a New
World clade. However, the relationships among the New World
clade, the Pantropical Coastal Clerodendrum, and the remaining Clerodendrum species (Asian + African), were unresolved
(Steane & al., 2004; Fig. 1B), leaving the possibility that Clerodendrum (sensu Steane & al., 2004) as currently circumscribed
is paraphyletic in relation to the clade of New World genera. In
addition, the phylogenetic framework presented in those studies
(Steane & al., 1997, 1999, 2004) is mainly based on cpDNA
restriction site data and nuclear ITS sequences, with only a few
chloroplast ndhF sequences. It is difficult to add more data to a
restriction site dataset, due to the nature of this type of marker.
For many Clerodendrum species the ITS region is difficult to
sequence directly without cloning, possibly because of their
being polyploids, which is indicated by the high chromosome
number, 2n = 46, 48, or 52, of most species (see the Index to
Plant Chromosome Numbers Database, http://mobot.mobot
.org/W3T/Search/ipcn.html).
The major objectives of this paper are, therefore, to: (1) test
the monophyly of Clerodendrum as currently circumscribed;
(2) present a phylogenetic framework of Clerodendrum and
its related genera based on cpDNA sequence data, to which
additional sequence data may be added easily in future studies; and (3) use this phylogenetic framework to examine the
evolution of morphological characters.
MATERIALS AND METHODS
Our sampling included 40 species of Clerodendrum (sensu
Steane & al., 2004), representing the three major clades
Fig. 1. Summarized phylogenies from
previous studies. A, results from Steane & al. (1997, 1999), showing that
Clerodendrum s.l. is polyphyletic;
B, results from Steane & al. (2004),
showing the unresolved relationship
between Asian + African Clerodendrum, Pantropical Coastal Clerodendrum, and a clade comprising
Aegiphila, Amasonia, and Tetraclea.
A
identified in previous studies, 13 species from six closely
related genera (Aegiphila, Amasonia, Tetraclea, Kalaharia
Baill., Oxera Labill., Faradaya F. Muell.), and three species
from more distantly related genera in the Lamiaceae-Ajugoideae (Ajuga L., Teucrium L., Rotheca). Voucher information
for these 56 samples is listed in Appendix 1.
Total genomic DNA was extracted from either silica-gel
dried leaf tissue or herbarium specimens using the modified CTAB method (Doyle & Doyle, 1987). Four relatively
fast-evolving non-coding cpDNA regions (Shaw & al., 2005)
were chosen for sequencing. These were trnD-trnT, trnT-trnL,
trnL-trnF (trnL intron and trnL-F intergenic spacer), and
trnS-trnfM. PCR and sequencing primers with corresponding references are listed in Appendix 2. Procedures for PCR
and sequencing are described in Yuan & Olmstead (2008).
Sequences of the two outgroup species, Verbena officinalis
L., Aloysia virgata (Ruiz & Pav.) Pers., are from Yuan &
Olmstead (2008), while sequences of all other species were
generated in this study and have been deposited in GenBank
(trnD-trnT : EU160617–EU160666, FJ951910–FJ951915; trnStrnfM : FJ951916–FJ951970; trnT-trnL: FJ951971–FJ952025;
trnL-trnF : FJ952026–FJ952081).
Sequence alignments were made manually using Se-Al
v.2.0a11 (Rambaut, 1996) based on the similarity criterion
(Simmons, 2004). The four cpDNA regions were combined
as a single dataset for phylogenetic analyses because these
regions are part of the haploid chloroplast genome and, therefore, share the same evolutionary history. Phylogenetically
informative insertions/deletions (indels) were coded as binary
characters using the simple gap coding method (Graham & al.,
2000; Simmons & Ochoterena, 2000) and appended to the end
Clerodendrum
Asian
Clerodendrum
African
Clerodendrum
Pantropical
Coastal
B
Clerodendrum
Asian
Clerodendrum
African
Aegiphila
Amasonia
Tetraclea
Oxera
Faradaya
Clerodendrum
Pantropical
Coastal
Other genera
Kalaharia
126
Clerodendrum
subg. Cyclonema
and C. sect. Konocalyx
Oxera
Outgroup
Outgroup
Faradaya
TAXON 59 (1) • February 2010: 125–133
of the dataset. Six poly-nucleotide or microsatellite regions (a
microsatellite with “AT” repeats and a poly-T region in the
trnD-trnT segment, two poly-T regions in the trnT-trnL segment, a poly-A region in the trnL-trnF segment, and a polyC/T/G region in the trnfM-trnS segment) have been excluded
from analyses due to uncertainty of homology assessment.
Both parsimony and Bayesian analyses were performed on
the final dataset.
Parsimony analysis was conducted using PAUP* v.4.0b10
(Swofford, 2002). Heuristic searches were performed with
1000 random stepwise addition replicates and TBR branch
swapping with the MULTREES option in effect. Nodal support was determined by bootstrap analyses (Felsenstein, 1985)
of 500 replicates, each with 20 random stepwise addition replicates and TBR branch swapping with MULTREES on.
Bayesian analyses were conducted using MrBayes v.3.1.2
(Ronquist & Huelsenbeck, 2003). A mixed-model approach
(Ronquist & Huelsenbeck, 2003) was employed to integrate
the phylogenetically informative gaps as binary characters
with nucleotide data. The final dataset was divided into two
partitions, the “nucleotide” partition and “gap” partition. We
used Akaike information criterion (AIC) implemented in Modeltest v.3.7 (Posada & Crandall, 1998) to determine the model
of sequence evolution that best fits the “nucleotide” partition
(GTR + G). The restriction site (binary) model in MrBayes
v.3.1.2 (Ronquist & Huelsenbeck, 2003) was used for the
“gap” partition, with ascertainment bias for gap characters
incorporated (lset coding = informative). We performed two
independent runs of 1,000,000 generations from a random
starting tree using the default priors and four Markov chains
(one cold and three heated chains), sampling one tree every
100 generations. Plots of log likelihood scores were used to
determine stationarity and trees from the first 100,000 generations were discarded as burn-in.
Yuan & al. • Phylogeny of Clerodendrum and allied genera
clades are strongly supported sister groups (100%/1.0, BB/
PP), whereas the Pantropical Coastal Clerodendrum clade is
sister to the New World clade (97%/1.0, BS/PP). Also consistent with previous studies (Steane & al., 2004), Kalaharia, a
unispecific African genus, is recovered as sister group of the
larger clade that includes all three Clerodendrum groups and
the New World clade. The Oxera/Faradaya clade is sister to
the even more inclusive clade including Kalaharia (Fig. 2).
Within the Asian clade, relationships are fairly well resolved. One strongly supported monophyletic group, in particular, is worth mentioning. It consists of species (C. floribundum, C. indicum [type of Siphonanthus L.], C. minahassae,
C. quadriloculare, C. tomentosum) that are characterized by
an extremely long and narrow corolla tube (99%/1.0, BS/PP;
Fig. 2), probably an adaptation to a particular type of pollinator. Within the African clade, however, relationships are poorly
resolved but it is noticeable that one species, C. hildebrandtii,
is strongly supported as sister to the rest of the African group
(Fig. 2). Within the Pantropical Coastal clade, branches are
short, indicating little sequence diversification between species. Within the New World clade, both Aegiphila and Amasonia are strongly supported monophyletic groups (Fig. 2).
Tetraclea is resolved to be the sister lineage of Amasonia, but
this relationship is only weakly supported (52%/0.49, BS/PP,
these values are not shown in Fig. 2). Likewise, Clerodendrum
spinosum is recovered as sister to the Amasonia/Tetraclea
clade, but weakly supported (52%/0.78, BS/PP).
Bayesian analyses gave very similar results. The only difference between the Bayesian majority consensus tree and
parsimony tree shown in Fig. 2 is on the relationship between
Aegiphila anomala, A. alba, the A. hassleri + A. brachiata
clade, and the A. elata + A. martinicensis clade, but neither
the relationship suggested by parsimony analyses nor that indicated by Bayesian inference is well supported (BS < 50%,
PP < 0.7).
RESULTS
DISCUSSION
The final dataset consisted of 44 scored gap characters
and 4002 aligned nucleotides, of which 127 from the six polynucleotide or microsatellite regions were excluded due to uncertainty of homology assessment. One of the eight maximum
parsimony trees resulting from parsimony analysis is shown in
Fig. 2. The results are consistent with previous studies (Steane
& al., 1997, 1999) in that Clerodendrum sensu Steane & al.
(2004) is divided into three major clades: an African clade, an
Asian clade, and a Pantropical Coastal clade. All three clades
are supported by 99%–100% bootstrap (BS) values and posterior probabilities (PP) of 1.0. However, our results reveal that
the Pantropical Coastal clade is more closely related to the New
World genera (Aegiphila, Amasonia, Tetraclea) than it is to the
Asian or African Clerodendrum clades (Fig. 2), a matter not
revealed by earlier studies. In addition, a Caribbean species,
Clerodendrum spinosum (L.) Spreng., is found not to belong
to any of the three major clades. Together with Aegiphila,
Amasonia, Tetraclea, it forms a well-supported (84%/1.0, BS/
PP) New World clade. The African and Asian Clerodendrum
Redefinition of Clerodendrum and revival of Volkameria and Ovieda. — Clerodendrum as currently circumscribed
(Steane & Mabberley, 1998; Steane & al., 2004) is certainly
not monophyletic (Fig. 2). In order to delimit Clerodendrum
as a monophyletic group, either the New World clade should
be incorporated in Clerodendrum or the Pantropical Coastal
clade should be removed from Clerodendrum and raised to generic level. Renaming species will therefore be inevitable. We
choose the second option here for two reasons: (1) Aegiphila,
Amasonia, and Tetraclea, have ca. 120, 8, and 2 species, respectively, whereas the Pantropical Coastal clade comprises
ca. 30 species. To minimize the number of name changes, it
is more sensible to separate the Pantropical Coastal clade into
a distinct genus, for which the earliest name is Volkameria L.
in which a number of the germane names have already been
published. (2) Retaining the generic distinction for Aegiphila,
Amasonia, and Tetraclea while resurrecting Volkameria provides increased information about evolutionary relationships
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TAXON 59 (1) • February 2010: 125–133
Yuan & al. • Phylogeny of Clerodendrum and allied genera
in the classification of this group. Besides separating the
Pantropical Coastal clade as the revived genus Volkameria,
Clerodendrum spinosum also needs to be removed from Clerodendrum. Its original name, Ovieda spinosa L., is revived for
it. Therefore, the newly delimited Clerodendrum is restricted
to the Asian and African clades. This is of no little historical
Fig. 2. One of eight most parsimonious
trees. The Bayesian consensus tree is
very similar to this in topology. Only
bootstrap values (BS) and posterior
probabilities (PP) greater than 80%/0.95
are shown along the branches to avoid
being overcrowded. Branches that collapse in the strict consensus are marked
by black dots. Geographic distributions
are shown on the right. The long-corolla-tube clade is indicated by a thickened
arrow.
100/1.0
100/1.0
100/1.0
100/1.0
128
C. bungei
C. lindleyi
C. canescens
C. cyrtophyllum
100/1.0
C. chinense var. simplex
C. fortunatum
100/1.0
C. trichotomum
95/1.0
100/1.0
C. japonicum
100/1.0
C. paniculatum
C. sp.
100/1.0
100/1.0 ‘C. buchananii ’
C. speciosissimum
100/1.0
C. tomentosum
C. floribundum
long, narrow
C. indicum
corolla tube
99/1.0
C. minahassae
C. quadriloculare
C. schweinfurthii
C. johnstonii
100/1.0
C. polycephalum
C. splendens
C. umbellatum
C. bipindense
89/1.0
C. thomsoniae
96/ 1.0
C. volubile
97/ 1.0
C. capitatum
C. cephalanthum subsp. mashariki
C. cephalanthum subsp. montanum
C. poggei
99/1.0
C. rotundifolium
C. hildebrandtii
99/1.0
Aegiphila elata
100/1.0
Aegiphila martinicensis
100/1.0
Aegiphila hassleri
88/1.0
Aegiphila brachiata
Aegiphila alba
100/1.0
Aegiphila anomala
Aegiphila multiflora
84/ 1.0
100/1.0
Amasonia sp.
Amasonia hirta
100/1.0
Tetraclea coulteri
C. spinosum
C. emirnense
100/1.0 C. glabrum
97/1.0
C. aggregatum
85/1.0
C. pittieri
100/1.0
C. aculeatum var. gracile
C. ligustrinum
100/1.0
C. linifolium
100/1.0
C. inerme
Kalaharia uncinata
100/1.0
Oxera pulchella
Faradaya splendida
Ajuga chamaepitys
Teucrium pyrenaicum
Rotheca sp.
Aloysia virgata
Verbena officinalis
Pantropical
Coastal
New World
African
Asian
97/1.0
99/1.0
10 changes
interest in that molecular work has confirmed three of the four
generic concepts used by Linnaeus for this group (see Taxonomy). It is also noteworthy that the long narrow corolla tube
has evolved at least twice independently in the group: once in
Ovieda and also in the common ancestor of the Asian clade
comprising C. indicum (which was independently described
TAXON 59 (1) • February 2010: 125–133
Yuan & al. • Phylogeny of Clerodendrum and allied genera
in Ovieda at least three times; see below), C. quadriloculare,
and others, as mentioned above.
Although it is difficult to find unique morphological synapomorphies to separate Clerodendrum, Volkameria, and
Ovieda, no doubt a cardinal reason why a broad view of
Clerodendrum has prevailed for so long, a combination of
several characters, as listed in Table 1, can be readily used to
distinguish the three genera.
Phylogenetic position of C. hildebrandtii. — Within the
African clade, one species, C. hildebrandtii, is sister to the rest
of the African group. This species is distinguished from other
African species by its large corolla (few flowers in each inflorescence) and large cylindrical calyx. In fact, C. hildebrandtii
is the sole member of Verdcourt’s (1992) C. sect. Cylindrocalyx
(Thomas) Verd. in his treatment of the genus in East Africa.
However, approximately 20 species of Clerodendrum that are
restricted to Madagascar closely resemble C. hildebrandtii
in morphology. Unfortunately, we were unable to obtain any
living material of these species or herbarium specimens of
sufficient quality for DNA extraction. But we predict that this
particular Madagascan group, together with C. hildebrandtii,
will form a clade that is sister to the rest of the African clade.
A future study with extensive sampling of this group will
shed light on the evolution of this, perhaps the most beautiful,
Clerodendrum group.
Evolution of an intriguing breeding strategy. — An interesting breeding strategy has been reported in some species
of Clerodendrum sensu stricto (s.str.) and Volkameria (Corner,
1940; Primack & al., 1981; Reddy & Reddi, 1995). The stamens
and the style are curled upwards tightly inside the flower bud.
When the flower opens, the filaments and style start uncoiling.
While the filaments project to the centre, the style continues
to bend down towards the lower side of the flower. The flower
is strongly protandrous and this is the functional male phase.
After pollen has been released and the anthers wither, the filaments curl back sideways and the style with its receptive stigma
projects back to the centre, taking the position occupied by the
stamens in the male phase (see Fig. 3; also see illustration and
a detailed description in Reddy & Reddi, 1995). This strategy
was first noted by Corner (1940: 700). He mentioned this as
typical of species of the genus native in the Malay Peninsula except for C. serratum, which is indeed referable to another genus
as Rotheca serrata (L.) Steane & Mabb., where “the stamens
and style arch over the top of the flower and one of the petals
is modified into a lower lip or landing platform” (Corner 1940:
700). Four decades later the same strategy was described by
Primack & al. (1981) in Volkameria inermis (as Clerodendrum
inerme). Then in 1995, a detailed description was made by
Reddy & Reddi from their observation of C. infortunatum, an
African species. Recently, it was observed in C. trichotomum,
an Asian species, and C. thomsoniae, an African species, by
the first author of this paper before he was aware of the earlier
work. This presentation of pollen and stigma in the centre of
the flower in a sequential fashion by moving the filaments and
style is an elegant combination of dichogamy and herkogamy,
that avoids self-fertilization or/and sexual interference (i.e.,
receiving pollen by stigmas and exporting pollen from anthers:
Lloyd & Webb, 1986; Webb & Lloyd, 1986).
A subsequent search for floral images has revealed that not
only Clerodendrum s.str. and Volkameria, but also Ovieda,
Amasonia, Tetraclea, and Kalaharia, all display this particular
floral presentation with curled stamens and style at different
stages (Fig. 3). Field observations of the pollination ecology
of Oxera and Faradaya by de Kok (1997) found these two
genera resemble the aforementioned taxa by having protandrous flowers, but not in displaying the alternating movement
between the filaments and style. In addition, floral presentation is heterogeneous in Oxera and Faradaya (de Kok, 1997),
by contrast with the uniform system found in Clerodendrum
s.str. and allies. Clerodendrum s.str., Volkameria, Ovieda, Aegiphila, Amasonia, Tetraclea, and Kalaharia together form a
strongly supported clade (Fig. 2). Lamiaceous taxa outside
this clade do not show such floral presentation. Therefore,
this breeding strategy appears to have evolved only once in
the common ancestor of these lineages and is a synapomorphy defining this clade. It has also been lost once and been
replaced by a heterostylous system on the path leading to the
extant Aegiphila lineage (Fig. 3G–H). This shift has interesting
implications for the understanding of evolutionary pathways
from homostyly to heterostyly.
Our examination of this intriguing breeding strategy in
a phylogenetic context provides a striking example of how
molecular phylogenetics can re-direct our effort in finding
and re-interpreting overlooked morphological characters. The
Table 1. Comparison of morphological characters of Clerodendrum s.str., Volkameria, and Ovieda.
Clerodendrum
Volkameria
Ovieda
Branches
Not tuberculate
Not tuberculate
Tuberculate
Leaf
Blade frequently longer than 6 cm,
never spiny; venation not camptodromous
Blade usually shorter than 6 cm, never
spiny; venation not camptodromous
Blade longer than 6 cm, margin usually with
spiny teeth; venation camptodromous and
reticulate with pronounced abaxial relief
Inflorescence
Usually terminal
Frequently axillary
Terminal
Fruiting calyx
Accrescent, larger than fruits, brightly
coloured
Rarely accrescent, smaller than fruits,
enclosing the fruit base, not brightly
coloured
Accrescent, enclosing fruit, not brightly
coloured
Fruits
Often fleshy, with bright colour contrast- Usually dryish, not brightly coloured
ing with calyx
Not recorded recently (Burman in Plumier,
1760, has ‘bacca obovata’), apparently not
brightly coloured
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TAXON 59 (1) • February 2010: 125–133
Fig. 3. Representative floral images of Clerodendrum s.str. and allied genera. A–B, Clerodendrum trichotomum Thunb. (photos by Y.-W. Yuan).
A, flower at male phase. Note the stamens project to the centre, whereas the style bends down towards the lower side of the flower. B, flower at
female phase. The filaments curl back sideways and the style with its receptive stigma projects back to the centre. C, Ovieda spinosa L. (photo
courtesy of Jackeline Salazar). D, Volkameria inermis L. (photo courtesy of Forest & Kim Starr). E, Tetraclea coulteri A. Gray (photo courtesy
of Burr Williams). The red and blue arrows indicate the flower at male and female phase, respectively. F, Amasonia campestris Moldenke (photo
courtesy of Robin Foster). The red arrow indicates the flower at male phase. G–H, Aegiphila sp. (photos courtesy of Kevin Nixon, www.plantsystematics.org), showing the heterostylous system. G, thrum flower; H, pin flower.
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“Clerodendrum s.str. + Volkameria + Ovieda + Aegiphila +
Amasonia + Tetraclea + Kalaharia” clade recovered by molecular data has never been recognized in traditional classification schemes. But, after finding that this complex breeding
strategy is shared by these taxa, it becomes obvious that they
are all closely related as indicated by DNA sequences.
TAXONOMY
Genera recognized (see also Steane & Mabberley, 1998 for
Rotheca) as a result of this work:
1. Clerodendrum L., Sp. Pl. 2: 637. 1753 – Type: C. infortunatum L.
= Siphonanthus L., Sp. Pl. 1: 109. 1753 – Type: S. indicus L.
(‘indica’) = Clerodendrum indicum (L.) Kuntze
= Cryptanthus Osbeck, Dagb. Ostind. Resa.: 215. 1757 –
Type: C. chinensis Osbeck = Clerodendrum chinense
(Osbeck) Mabb.
Trees, shrubs sometimes suckering, lianes or subherbaceous perennials. Leaves simple (sometimes lobed), decussate
or (rarely) whorled, never spiny. Inflorescences cymose, usually terminal. Flowers bisexual; calyx campanulate to tubular,
variously lobed, often coloured, usually accrescent; corolla red
to yellow, pink or white, with narrow tube, 5-lobed, the lobes
usually unequal; stamens 4 (or 5), didynamous, inserted within
corolla tube, usually long-exserted; ovary imperfectly 4-locular, each locule with 1 ovule, style terminal, elongate, shortly
2-lobed. Fruit a drupe, often 4-sulcate or 4-lobed; endocarp
tough, separating into 4 (or 2 pairs of) pyrenes (sometimes
only two maturing), each with one seed.
Circa 150 species in tropical Old World with some species
found as far south as Australia and as far north as China and
Japan.
2. Ovieda L., Sp. Pl. 2: 637. 1753 – Type: O. spinosa L. ≡
Clerodendrum spinosum (L.) Spreng.
Shrub to 1.5 m, sometimes subherbaceous; branches tuberculate. Leaves simple, decussate (occasionally some in
spirals), coriaceous, margin toothed, teeth usually spiny, venation camptodromous, pinnate-reticulate, with conspicuous
pronounced venation in relief on abaxial surface. Inflorescences corymbose, terminal. Flowers bisexual; calyx large,
campanulate with 5 acute lobes, accrescent enclosing fruit,
not brightly coloured; corolla white with long narrow tube,
mouth 5-lobed; stamens 4, exserted; style solitary, as long as
stamens; ovary globose. Fruit a drupe, globose to obovate,
with 2 locules, each with one seed.
One species, restricted to Hispaniola.
Ovieda spinosa L., Sp. Pl. 2: 637. 1753 – Lectotype (designated
here): Burman in Plumier, Pl. Amer.: t. 256. 1760.
Notes. – Hitherto type material has not been designated
(Jarvis, 2007: 716). Linnaeus cited Plumier (1703, as Valdia)
but that shows insufficient detail to be the basis for his description. A much more detailed description, together with a plate
Yuan & al. • Phylogeny of Clerodendrum and allied genera
that shows the inflorescence and leaf features that Linnaeus
described in 1753 are shown in Burman’s 1760 work. Burman’s plate is based on a tracing of Plumier’s drawing that
was made by Claude Aubriet for Herman Boerhaave, and later
prepared for publication by Burman. Burman sent proof copies
to Linnaeus ahead of their publication, and it seems clear that
Linnaeus must have received this one prior to 1753, hence its
being appropriate as type material, even though published after
Linnaeus’s own work (Jarvis, 2007: 151).
Note: Ovieda Spreng. (1824) = Lapeirousia Pourr. (Iridaceae). For Clerodendrum s.l., Baillon (1891) resurrected
Ovieda L., which had been made a synonym of Clerodendrum by authors from the 1820s onwards, so his action was
inadmissible, though Ovieda as the name for Clerodendrum
s.l. (including Volkameria) gained some currency in American
publications (*Ovieda aculeata (L.) Baill., Hist. Pl. 11: 95.
1891 non O. aculeata Klatt (1864 = Lapeirousia fabricii (de
la Roche) Ker, Iridaceae) = Volkameria aculeata L.; *O. bracteosa (Kostel.) Baill., l.c. (C. bracteosum Kostel. [type (icon):
Rheede, Hort. Malab. 4: t. 29. 1683] = Rotheca serrata (L.)
Steane & Mabb. [syn. nov.]); O. fragrans (Willd.) Hitchcock
(= C. chinense (Osbeck) Mabb.); O. inermis Burm. f. (= C. indicum (L.) Kuntze); *O. infortunata (L.) Baill., l.c. (= C. infortunatum L.); O. mitis L. (= C. indicum (L.) Kuntze); O. ovalifolia
A. Juss. (C. ovalifolia (A. Juss.) Bakh. [type: India, Pondichéry,
Commerson s.n. in Hb. Juss. (microfiche 347/19-P-JUSS)] =
V. inermis L. [syn. nov.]); *O. trichotoma (Thunb.) Baill., l.c.
(= C. trichotomum Thunb.); O. verticillata Roxb. ex D. Don
[nom. in synon.] = C. indicum (L.) Kuntze).
*Additions to Index kewensis and other standard lists.
3. Volkameria L., Sp. Pl. 2: 637. 1753 – Type: V. aculeata L.
≡ Clerodendrum aculeatum (L.) Schldl.
= Huxleya Ewart in Proc. Roy. Soc. Victoria, ser. 2, 25: 109.
1912, syn. nov. – Type: H. linifolia Ewart & B. Rees, l.c.
≡ C. linifolium (Ewart & B. Rees) de Kok = V. linifolia
(Ewart & B. Rees) Mabb. & Y.W. Yuan, comb. nov. – Type:
Australia, Northern Territory, Darwin, 1892, N. Holtze
1322 (lecto MEL).
Shrubs, sometimes subherbaceous, lianes, rarely small
trees; branches ± tetragonal, usually ash-grey, nodes swollen.
Leaves decussate (to ternate), subglabrous,with entire margin,
never spiny, venation arcuate-reticulate. Inflorescences axillary to supra-axillary cymes. Flowers usually fragrant; calyx
campanulate, only rarely accrescent, margin with 5 broadly
triangular small teeth; corolla hypocrateriform, white, sometimes pink or purple, lobes unequal; stamens 4 (or 5), didynamous, inserted within corolla tube, exserted; ovary cylindrical; stigma shortly bifid. Fruits generally globose to obovoid,
becoming black or brown and separating into 4 corky pyrenes,
each with 1 seed.
Approximately 25–30 species, pantropical but with apparently only one species in Asia (V. inermis L.)
Notes. – Pending a critical review of Volkameria taxa of
Madagascar, where they appear to be numerous (Moldenke,
1956), the germane species are not transferred from Clerodendrum here, though one at least already has a name in
131
Yuan & al. • Phylogeny of Clerodendrum and allied genera
Volkameria: V. heterophylla Vent. (C. heterophyllum (Vent.)
R. Br., Mascarenes, Madagascar), nor are those of Australia
except C. linifolium above. However, all the five species native
in Mesoamerica can now be placed as they have been monographed by Rueda (1993, see for species descriptions). To these
can be safely added two widespread African species to add to
those already with names in Volkameria, plus C. aggregatum
used in our analysis:
1. Volkameria acerbiana Vis. ≡ Clerodendrum acerbianum
(Vis.) B.D. Jacks.
Tropical Africa. See Verdcourt (1992) for a description.
2. V. aculeata L. ≡ C. aculeatum (L.) Schldl.
Tropical America.
3. Volkameria aggregata (Gürke) Mabb. & Y.W. Yuan, comb.
nov. ≡ Clerodendrum aggregatum Gürke in Bot. Jahrb.
Syst. 18: 177. 1894 – Type: Madagascar, Loko-be, Hildebrandt 3339 (B† holo; K iso, NY iso).
Tropical Africa.
4. Volkameria costaricensis (Standl.) Mabb. & Y.W. Yuan,
comb. nov. ≡ Clerodendrum costaricense Standl. in Publ.
Field Mus. Nat. Hist., Bot. Ser. 18: 1002. 1938 – Type: Costa
Rica, La Pena de Zarcero, Smith H588 (H holo; MO iso,
NY fragm.).
Caribbean.
5. Volkameria eriophylla (Gürke) Mabb. & Y.W. Yuan,
comb. nov. ≡ Clerodendrum eriophyllum Gürke in Bot.
Jahrb. Syst. 18: 178. 1894 – Type: [Tanzania] Fischer ser.
I, 331 (B† holo).
Tropical Africa. See Verdcourt (1992) for a description.
6. Volkameria glabra (E. Mey.) Mabb. & Y.W. Yuan, comb.
nov. ≡ Clerodendrum glabrum E. Mey., Comm. Pl. Afr.
Austr.: 273. 1837 – Type: South Africa, Cape Province, R.
Basche, Drège s.n., (B† holo; K iso).
See Verdcourt (1992) for a description.
7. V. inermis L. ≡ C. inerme (L.) Gaertn.
Tropical Asia and Pacific. See Mabberley (2004) for a description.
8. V. ligustrina Jacq. ≡ C. ligustrinum (Jacq.) R. Br.
Tropical America.
9. V. linifolia (Ewart & B. Rees) Mabb. & Y.W. Yuan (see
above).
Northern Australia.
10. Volkameria mollis (Kunth) Mabb. & Y.W. Yuan, comb.
nov. ≡ Clerodendrum molle Kunth., Nov. Gen. Sp. 2,
quarto ed.: 244. 1818 – Type: Ecuador, Bonpland 3387 (PHB 6209.46: III: 1 (microfiche).
Tropical America.
132
TAXON 59 (1) • February 2010: 125–133
11. Volkameria pittieri (Moldenke) Mabb. & Y.W. Yuan, comb.
nov. ≡ Clerodendrum pittieri Moldenke in Phytologia 1: 416.
1940 – Type: Peru, Pittier 4965 (US holo; MO iso).
Caribbean.
ACKNOWLEDGEMENTS
We would like to thank all the people who provided plant material; these include Shixiao Luo, Scot Zona, Rogier de Kok, Jun Wen,
John Tan, and Robert Jansen. Thanks are also due to the directors/
curators of the following herbaria for the loan of herbarium specimens and permission to take tissue samples: MAPR (Gary Breckon),
MO (Jim Solomon), L (Erik Smets), and US (Jun Wen, Vicki Funk).
We are grateful to Rogier de Kok (Royal Botanic Gardens Kew) for
communicating his observations on the pollination biology of Oxera
and Faradaya, and to Kevin Nixon, Jackeline Salazar, Burr Williams,
Robin Foster, Forest & Kim Starr for permission to use thei r floral
images. We also thank James Wearn (Royal Botanic Gardens Kew)
for help in preparing a generic description of Ovieda and its typification, and thank Phil Garnock-Jones and an anonymous reviewer for
helpful comments on the manuscript. Funding for this research was
provided by a McIntire-Stennis Formula Fund to DJM and a NSF
Grant (DEB 0542493) to RGO.
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Appendix 1. Plant material used in this study. Each entry consists of: taxon name, country in which it was collected, year of collection, collector with collection number, and herbarium (accession number when available) where voucher was deposited.
Aegiphila alba Moldenke, Ecuador, 2004, J. Clark 7960, US; A. anomala Pittier, Costa Rica, 1995, J.F. Morales & V. Urena 3760, MO (5748376); A. brachiata
Vell., Brazil, 2003, A. Kegler 1581, MO (5772239); A. elata Sw., Panama, 1986, G. McPherson 8473, MO (4290179); A. hassleri Briq., Argentina, 2000, De
Romero & al. 2201, MO (5830202); A. martinicensis Jacq., Puerto Rico, 1980, J.C. Solomon 5732, MO (2897682); A. multiflora Ruiz & Pav., Bolivia, 1983,
St. G. Beck 8688, MO (4275754); Ajuga chamaepitys (L.) Schreb., Cantino 185, K; Amasonia hirta Benth., Brazil, 1982, B.A.S. Perecira 251, MO (2994726);
Amasonia sp., Brazil, 1997, Giulietti & al., PCD 6176, K; Clerodendrum aculeatum (L.) Schldl. var. gracile Griseb. ex Moldenke, Fairchild Tropical Botanic
Garden, 2006, Zona 1100 & Gillis 9169, FTG; C. aggregatum Gürke, Madagascar, 1996, Gautier & S.T. Be, LG 2873, MO (5208533); C. bipindense Gürke,
Guinea, 1987, Carvalho 3033, MO (4322999); C. buchananii auctt., non (Roxb.) Walp., Oxford Botanic Garden, Steane 76, FHO; C. bungei Steud., Oxford
Botanic Garden, Steane 78, FHO; C. canescens Wall. ex Walp., China, S.X. Luo 242, IBSC; C. capitatum (Willd.) Schumach. & Thonn., Tanzania, 1998,
O.A. Kibure 183, MO (5310537); C. cephalanthum Oliv. subsp. mashariki Verdc., Tanzania, 1999, M.A. Mwangoka 974, MO (5290487); C. cephalanthum
subsp. montanum (Thomas) Verdc., Tanzania, 2003, O.A. Kibure 982, MO (04473598); C. chinense (Osbeck) Mabb. var. simplex (Moldenke) S.L.Chen,
Fairchild Tropical Botanic Garden, 2006, Fantz 3419, FTG; C. cyrtophyllum Turcz., China, S.X. Luo 253, IBSC; C. emirnense Boj. ex Hook., Madagascar,
1990, P.B.Phillipson & al. 3414, MO (3842769); C. floribundum R. Br. Australia, 1989, C.R. Dunlop 8055, L(0625213); C. fortunatum L., China, S.X. Luo
252, IBSC; C. glabrum E. Mey., Oxford Botanic Garden, Steane 87, FHO; C. hildebrandtii Vatke var. puberula Verdc., Tanzania, 1999, C.J. Kayombo 2302,
MO (5291257); C. indicum (L.) Kuntze, Singapore, RK 5394; C. inerme (L.) Gaertn., Oxford Botanic Garden, Steane 86, FHO; C. japonicum (Thunb.) Sweet,
China, S.X. Luo 254, IBSC; C. johnstonii Oliv., Tanzania, 1999, P. Phillipson & J. Mlwangwa 2017, MO (5189370); C. ligustrinum (Jacq.) R. Br., Mexico,
1998, R. Novelo & Ay Ramos V.L. 2901, MO (5300788); C. lindleyi Decne. ex Planch. China, S.X. Luo 251, IBSC; C. linifolium (Ewart & B. Rees) de Kok,
Australia, 1999, Cowie 8213, K; C. minahassae Teijsm. & Binn., Fairchild Tropical Botanic Garden, 2006, Houghton & White 1145, FTG; C. paniculatum L.,
Palau (in cultivation), 1966, N.H. Cheatham 32, US(3356180); C. pittieri Moldenke, Peru, 1976, D.C. Wasshausen & F. Encarnarium 686, US (2956667); C.
poggei Gürke, Tanzania, 1999, G. Gobbo 281, MO (5290499); C. polycephalum Bak., Ghana, 1994, C.C.H. Jongkind & H.H. Schmidt 1735, MO (04667183);
C. quadriloculare Merr. Fairchild Tropical Botanic Garden, 2006, Zona 1104, FTG; C. rotundifolium Oliv., Tanzania, 2000, S. Bidgood & al. 4819, MO
(5658503); C. splendens G. Don, National Botanic Garden, Zimbabwe; C. schweinfurthii Gürke, Oxford Botanic Garden, Steane 82, FHO; C. sp., Indonesia,
2001, Ramadhanil & al. 461, L (0334140); C. speciosissimum Hort. Gand. ex Drapiez, Oxford Botanic Garden, Steane 90, FHO; C. spinosum (L.) Spreng.
Dominican Republic, 2001, F. Jimenez 3332, MAPR (26103); C. thomsoniae Balf., UW Greenhouse, 2002, RGO 2002-07, WTU; C. tomentosum (Vent.) R.
Br., Australia, 1984, S.J. Forbes 2510, L (0625219); C. trichotomum Thunb., R.G. Olmstead home garden, 2002, RGO 2002-134, WTU; C. umbellatum Poir.,
Tanzania, 1999, G. Gobbo 486, MO (5290496); C. volubile P. Beauv, Ghana, 1996, M. Merello & al. 1345, MO (05030536); Faradaya splendida F. Muell.,
H. Rimpler 2144, FB; Kalaharia uncinata (Schinz) Moldenke, Tanzania, 2002, N.A. Mwangulango 973, MO (5721485); Oxera pulchella Labill., H. Rimpler 1328,
FB; Rotheca sp., Madagascar, Wen 9487, US; Tetraclea coulteri A. Gray, U.S.A., Ki-Joong Kim 100026, TEX; Teucrium pyrenaicum L., Voucher unknown.
Appendix 2. Primers used for PCR and sequencing; the ones that were specifically designed for this study are marked by an asterisk (*).
trnL-F: c, d, e, f (Taberlet & al., 1991); trnS-fM: trnSUGA & trnfMCAU (Shaw & al., 2005), psbZF(V) (Yuan & Olmstead, 2008), psbZR(C)* (5 -CATCAATCTTATTGATTAGCGTA-3 ); trnD-T: trnDGUCF & trnTGGU R (Shaw & al., 2005), trnD-TE2T* (5 -AATTCGAATCCCCGCTGCCTCC-3 ), trnD-TE2D*
(5 -CATTCCATTATATTGACAATT-3 ); trnT-L: a (Taberlet & al., 1991), R(Cler.)* (5 -ACCTATAGGAAACCCATATT-3 ).
133