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An evaluation of tribes and generic relationships in Melioideae (Meliaceae) based on nuclear ITS ribosomal DNA

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Phylogenetic analyses of Melioideae, including representatives of all currently recognized tribes, were carried out using nuclear ITS ribosomal DNA sequence data. The secondary structure models employed for ITS1 and ITS2 allowed optimization of the alignment across Meliaceae genera of both subfamilies, yielding a maximum amount of information without the exclusion of some highly variable sites. This study is the first to assess the current circumscription of Melioideae and its tribes in detail, with data independ-ent of morphology. Maximum parsimony, maximum likelihood and Bayesian analyses of nuclear ITS, in contrast to analyses based on plastid rbcL, confirm monophyly for Aglaieae, Sandoriceae and Melieae, an isolated position for Vavaeeae, the position of Pterorhachis and Quivisianthe in Melioideae, and a close relationship between Turraeeae and Trichilieae. Trichilieae are morphologically and genetically the most complex tribe. Trichilieae cannot be separated from Turraeeae, Vavaeeae and Sandoriceae. Anthocarapa and "Pseudocarapa" form a clade but exhibit a high number of autapomorphies, which needs further investiga-tion. We propose to keep Naregamia separate from Turraea, and to reconsider the present circumscription of Trichilieae.
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98
TAXON 57 (1) • February 2008: 98–108Muellner & al. • Tribes and generic relationships in Melioideae
An evaluation of tribes and generic relationships in Melioideae
(Meliaceae) based on nuclear ITS ribosomal DNA
Alexandra N. Muellner
1,2
, Rosabelle Samuel
3
, Mark W. Chase
1
, Annette Coleman
4
&
Tod F. Stuessy
3
1
Molecular Systematics Section, Jodrell Laboratory, Royal Botanic Gardens Kew, Richmond, Surrey TW9
3DS, U.K.
2
Present Address: Grunelius-Moellgaard Laboratory, Department of Botany and Molecular Evolution,
Research Institute Senckenberg, Senckenberganlage 25, 60325 Frankfurt am Main, Germany.
alexandra.muellner@senckenberg.de (author for correspondence)
3
Department of Systematic and Evolutionary Botany, Faculty Center Botany, University of Vienna,
Rennweg 14, 1030 Vienna, Austria
4
Division of Biology and Medicine, Brown University, Providence, Rhode Island 02912, U.S.A.
Phylogenetic analyses of Melioideae, including representatives of all currently recognized tribes, were
carried out using nuclear ITS ribosomal DNA sequence data. The secondary structure models employed
for ITS1 and ITS2 allowed optimization of the alignment across Meliaceae genera of both subfamilies,
yielding a maximum amount of information without the exclusion of some highly variable sites. This study
is the first to assess the current circumscription of Melioideae and its tribes in detail, with data independ-
ent of morphology. Maximum parsimony, maximum likelihood and Bayesian analyses of nuclear ITS, in
contrast to analyses based on plastid rbcL, confirm monophyly for Aglaieae, Sandoriceae and Melieae, an
isolated position for Vavaeeae, the position of Pterorhachis and Quivisianthe in Melioideae, and a close
relationship between Turraeeae and Trichilieae. Trichilieae are morphologically and genetically the most
complex tribe. Trichilieae cannot be separated from Turraeeae, Vavaeeae and Sandoriceae. Anthocarapa and
Pseudocarapa” form a clade but exhibit a high number of autapomorphies, which needs further investiga-
tion. We propose to keep Naregamia separate from Turraea, and to reconsider the present circumscription
of Trichilieae.
KEYWORDS: internal transcribed spacer (ITS), Meliaceae, Melioideae, molecular phylogenetics, rbcL
INTRODUCTION
Meliaceae are a widely distributed subtropical and
tropical angiosperm family occurring in a variety of habi-
tats, from rain forests and mangrove swamps to semi-
deserts (Pennington & Styles, 1975; Pennington & al.,
1981; Pannell, 1992; Mabberley & al., 1995). Together
with the contributions on Meliaceae in Flora Neotropica
by Pennington & al. (1981) and in Flora Malesiana by
Mabberley & al. (1995), the most authoritative work on the
family is the generic monograph by Pennington & Styles
(1975). Currently recognized are 49 to 51 genera with
about 565 species (Pennington & Styles, 1975; Mabberley
& al., 1995; Cheek, 1996; Chase & al., 1999; Mabberley,
2000). Pennington & Styles (1975) recognized four sub-
families, of which Melioideae and Swietenioideae consist
of seven tribes with 34 to 36 genera and three tribes with
13 genera, respectively. Quivisianthoideae and Capu-
ronianthoideae each contain a single monotypic genus
(Quivisianthe Baill. and Capuronianthus Leroy) and were
newly recognized by Pennington & Styles (1975). A re-
cent reassessment of the circumscription of the four sub-
families by means of phylogenetic analyses of sequence
data from three regions (plastid rbcL, matK, nuclear 26S
rDNA) showed that the members of the two small mono-
generic subfamilies, Quivisianthe and Capuronianthus,
fall within Melioideae and Swietenioideae, respectively,
supporting their taxonomic inclusion in these groups (Mu-
ellner & al., 2003).
Pennington & Styles (1975) found a wide range
of morphological variation especially in the subfamily
Melioideae. To obtain an improved tribal scheme com-
pared to that of Harms (1940), Pennington & Styles (1975)
subordinated the supposed evolutionary significance of
individual characters in favour of groupings based on
correlations between the maximum number of characters
of use at this level of classification and on detection of
discontinuities in variation of these characters. Penning-
ton & Styles (1975) argued that the most natural group-
ing of genera was obtained by basing classification on a
large number of characters; thus, artificial assemblages
resulting from the weighting of a few characters were
99
Muellner & al. • Tribes and generic relationships in MelioideaeTA XON 57 (1) • February 2008: 98–108
avoided. Using these principles, Pennington & Styles
(1975) recognized seven tribes within subfamily Melioi-
deae but stated that limits of Trichilieae, Aglaiaeae and
Guareeae could only be defined by overlapping mor-
phological, anatomical and palynological characters. All
tribes of Melioideae are represented in Malesia, but only
two (Guareeae, Trichilieae) are pantropical and two other
ones are restricted to the Old World (Turraeeae, Melieae);
the remainder are restricted to Indomalesia and the west-
ern Pacific (Vavaeeae, Aglaieae, Sandoriceae; Mabberley
& al., 1995).
The internal transcribed spacers (ITS) of nuclear ri-
bosomal DNA (nrDNA), defined as the unit containing
the ITS1 spacer, 5.8S rRNA gene and ITS2 spacer, are not
only useful in assessing relationships at the infrageneric,
but also at higher taxonomic levels (Hershkovitz & Zim-
mer, 1996; Soltis & Soltis, 1998). Secondary structure
models of RNA transcripts, employed in the taxonomic
group under investigation, allow for optimizing alignment
of variable and putatively phylogenetically informative
regions of ITS even across more distantly related taxa.
This is due to the fact that the secondary structure of ITS
is more conserved than the primary sequence (Mai &
Coleman, 1997; Coleman & al., 1998).
In this study we performed maximum parsimony,
maximum likelihood and Bayesian analyses of sequence
data from nuclear ITS to estimate phylogenetic relation-
ships within subfamily Melioideae for which former anal-
yses of plastid rbcL, matK and nuclear 26S rDNA did not
provide sufficient information (Muellner & al., 2003).
Based on 51 species, including representatives of all cur-
rently recognized tribes, this study thus provides the first
detailed reassessment of tribal and generic relationships
in Melioideae. The ITS data are compared to rbcL data
recently collected in the course of a survey on the biogeo-
graphic history of Meliaceae (Muellner & al., 2006).
MATERIALS AND METHODS
Plant material.
We analysed ITS sequences of 51
species of subfamily Melioideae (ingroup) and one species
each of genera Swietenia Jacq., Khaya A. Jussieu, Toona
(Endl.) M. Roem. and Cedrela P. Browne of subfamily
Swietenioideae as outgroups (Appendix). The justification
for the inclusion of the ingroup taxa in Melioideae and
Swietenia, Khaya, Toona and Cedrela in Swietenioideae
was based on a previous evaluation of the higher-level
classification of Meliaceae (Muellner & al., 2003).
Plant material was collected during excursions to
Thailand, Malaysia, Sri Lanka and Australia and from the
living collections of Forestry Research Institute Malaysia
(FRIM), Kebun Raya (Bogor Botanic Garden), Indonesia,
and the Royal Botanic Gardens, Kew, U.K. Herbarium
specimens are deposited at FHO, FR, K, NBG, NCU
and WU.
Isolation of DNA and amplification. —
Field-
collected material was dried and stored in silica gel prior
to DNA extraction (Chase & Hills, 1991). DNA extraction
and PCR amplification followed Muellner & al. (2005).
The fragment size amplified was between 627 and 664
bp for the entire ITS region. After amplification, samples
were gel purified using the QIAquick gel extraction kit
(QIAGEN, Margaritella, Vienna, Austria).
Sequencing.
PCR primers were also used for
sequencing. Cycle-sequencing followed Muellner & al.
(2005). Sequencing reactions were run on an ABI PRISM
377 DNA Sequencer and on an ABI 3100 capillary se-
quencer following the manufacturer’s protocols.
Sequence editing and alignment. —
For editing
and assembly of the complementary strands, the software
programs Autoassembler version 1.4.0 (Applied Biosys-
tems) and DNA STRIDER version 1.2 (Christian Marck,
CEA – Commissariat à Lènergie Atomique/Saclay, France)
were used. ITS sequences were explored for the presence
of several structural motifs. Thus, in the ITS1 region we
searched for the presence of the conserved angiosperm mo-
tif GGCRY-(4 to 7 n)-GYGYCAAGGAA (Liu & Schardl,
1994), which was also found in several gymnosperms
(Maggini & al., 1998). We also looked for the presence
of the conserved (C1C6) and variable (V1V6) domains
determined for plant ITS2 sequences (Hershkovitz &
Zimmer, 1996), as well as for the conserved angiosperm
motif 5-GAATTGCAGAATCC-3 within the 5.8S rDNA
gene, which can be used to differentiate between flower-
ing plants, fungi and algae (Jobes & Thien, 1997). Folding
predictions of secondary structures of the ITS1 and ITS2
RNA transcripts were made at the M. Zuker web server
(http://www.bioinfo.rpi.edu/~zukerm/) by use of the mfold
program version 3.1 (Mathews & al., 1999; Zuker & al.,
1999). Foldings were conducted at 37°C. After a first rough
alignment with CLUSTAL version X (Thompson & al.,
1997), corrections were made manually by using second-
ary structure predictions of ITS1 and ITS2 RNA transcripts
as a guide for alignment across genera. Secondary struc-
ture predictions were confirmed by hemi-compensatory
base changes (hemi-CBCs) and full compensatory base
changes (CBCs) that preserved the predicted folding pat-
tern. First, the secondary structure used was not always the
energetically most favourable, but rather the folding that
was common to all genera and species and supported by
CBCs and hemi-CBCs. Second, the structural motifs com-
mon to all eukaryote ITS2 (Coleman, 2007) were present
there, exactly in their expected positions in the secondary
structure. These were the most conserved sequences, as
also expected. A total of 794 aligned positions were in-
cluded in the matrices for phylogenetic analyses for ITS
(including ITS1, 5.8S rDNA and ITS2). Gaps were coded
100
TAXON 57 (1) • February 2008: 98–108Muellner & al. • Tribes and generic relationships in Melioideae
as missing data. All sequences are deposited in GenBank
(http://www.ncbi.nlm. nih.gov/).
Phylogenetic analysis. —
Individual maximum
parsimony (MP) analyses of the ITS and the rbcL dataset
(data for the latter region were obtained from Muellner &
al., 2006) were performed using PAUP*4.0b10 (Swofford,
2002). Visual inspection of the individual bootstrap con-
sensus trees was used for determining congruence of da-
tasets (Whitten & al., 2000). Although there were strongly
supported ( > 85% bootstrap), incongruent patterns among
the individual analyses, direct combination was carried
out to confirm observations based on the separate analyses
(trees not shown). Substitutions at each nucleotide posi-
tion were treated as independent, unordered, multi-state
characters of equal weight (Fitch parsimony; Fitch, 1971).
Heuristic searches were performed using 1,000 random
additions of taxa, tree bisection-reconnection (TBR)
branch swapping and MulTrees on (keeping multiple,
shortest trees). Robustness of clades was estimated using
the bootstrap (Felsenstein, 1985) with 5,000 replicates
with simple sequence addition, TBR branch swapping
and MulTrees on.
Bayesian analyses were conducted with MrBayes
version 3.01 (Huelsenbeck & Ronquist, 2001) using four
Markov chains simultaneously started from random
trees. Modeltest 3.06 (Posada & Crandall, 1998, 2001)
was used to select the optimal substitution model (GTR,
general time reversible model). One million cycles were
performed, sampling a tree at every 100 generations. Trees
that preceded the stabilization of the likelihood value (the
burn-in) were excluded, and the remaining trees were used
to construct a majority rule consensus in PAUP (version
4.0b10; Swofford, 2002). The percentages on this tree are
the Bayesian posterior probabilities.
Maximum likelihood (ML) analyses were performed
with PAUP*4.0b10 (Swofford, 2002). The substitution
model employed in the analyses was the same as for the
Bayesian analyses.
RESULTS
Structure, size and composition of ITS.
Length
of the entire ITS region, including ITS1, 5.8S rDNA and
ITS2, varied among Melioideae accessions from 627 to
664 bp. ITS1 ranged in length from 233 to 273 bp, 5.8S
rDNA from 156 to 172 bp, and ITS2 from 214 to 238 bp.
The mean GC ratios of Melioideae taxa for the sequences
of ITS1, 5.8S and ITS2 were 66%, 55% and 66%, respec-
tively. The complete set of statistics for all datasets is
summarized in Tables 1 and 2.
Phylogeny estimation based on ITS.
The aligned
ITS matrix consisted of 794 characters (Table 1). For the
entire ITS matrix, 499 (63 %) positions were variable and
403 (51 %) were potentially parsimony informative. The
parsimony search produced three most parsimonious trees
of 2,421 steps with consistency index (CI) = 0.38 and re-
tention index (RI) = 0.54 for the entire ITS matrix (Fig.
1). Bayesian results derived from the entire ITS matrix
are shown in Figure 2. The broad phylogenetic patterns
are similar to the MP analysis: Aglaieae are monophyletic
(51% bootstrap percentage, BP; 97% posterior probability,
PP), Guareae are paraphyletic (Figs. 1, 2). Turraeeae are
paraphyletic and appear in a clade with representatives of
Trichilieae (53% BP; 94 PP; Fig. 2). Members of the lat-
ter also appear in other parts of the tree. Sandoriceae are
monophyletic (100 BP; 100 PP; Figs. 1, 2), as are Melieae
(87 BB; 100 PP; Figs. 1, 2). Maximum likelihood results
reflect the same broad patterns (tree not shown).
Phylogeny estimation based on rbcL.
The
aligned rbcL matrix consisted of 1,387 characters (Table
1). For the rbcL matrix, 186 (13%) positions were vari-
able and 97 (7%) were potentially parsimony informative.
The parsimony search produced 7,199 most parsimonious
trees of 293 steps with CI = 0.59 and RI = 0.82 (Table 1).
Bayesian tree topology derived from the rbcL matrix is
Table 1. Statistics for the maximum parsimony analyses of
the internal transcribed spacer (ITS) of nuclear ribosomal
DNA (nrDNA), defined as the unit containing the ITS1 spac-
er, 5.8S rRNA gene and ITS2 spacer, and of plastid rbcL.
Dataset ITS rbcL
No. of all accessions/of Melioideae accessions 55/51 37/33
No. of characters included 794 1,387
No. of variable sites 499 186
No. of informative characters 403 97
Length of shortest tree (no. of steps) 2,421 293
Number of shortest trees 3 7,199
Consistency index 0.38 0.59
Retention index 0.54 0.82
Table 2. Characterization of ITS in Melioideae and outgroup taxa.
Length Length (bp) Mean GC ratio (%)
Region (no. characters) Melioideae Outgroup Melioideae Outgroup
Entire ITS 794 627–664 636–650 63 69
ITS1 338 233–273 247–257 66 73
5.8S 214 156–172 164 55 55
ITS2 242 214–238 225–228 66 74
101
Muellner & al. • Tribes and generic relationships in MelioideaeTA XON 57 (1) • February 2008: 98–108
identical to the MP results (Fig. 3), with one exception:
Aglaia and Lansium formed a clade supported by 51%
in the Bayesian majority rule consensus tree. Posterior
probabilities are plotted on the MP tree (Fig. 3). Again,
Aglaieae are monophyletic (74 PP; Fig. 3) and Guareae
paraphyletic (Fig. 3). With the exception of Munronia,
all other representatives of Turraeeae are members of a
monophyletic group (98 BP; 71 PP; Fig. 3). All members
15
16
16
10
13
18
15
16
11
9
7
8
17
18
6
5
2
7
1
11
25
5
22
16
10
6
26
16
9
19
18
10
5
8
23
4
13
13
26
32
28
6
20
16
21
19
3
9
58
10
48
32
7
59
52
50
31
21
26
34
59
18
17
10
19
27
14
14
11
54
100
25
61
29
14
12
13
32
35
42
58
18
1
4
10
40
13
13
45
43
7
70
13
63
73
29
16
21
15
31
32
17
18
24
35
29
38
98
100
99
99
53
100
100
100
54
100
64
98
60
100
55
80
85
96
66
55
96
99
69
62
53 100
100
100
87
97
100
87
76
51
Aphanamixis
borneensis
(5)
Aphanamixis
polystachya
(5)
Sphaerosacme
decandra
(5)
Cabralea
canjerana
(6)
Guarea
glabra
(6)
Ruagea
pubescens
(6)
Turraeanthus
sp.
(6)
Heckeldora
staudtii
(6)
Dysoxylum
gaudichaudianum
(6)
Chisocheton
macrophyllus
(6)
Synoum
glandulosum
(6)
Anthocarapa
nitidula
(6)
Pseudocarapa
nitidula
(6)
Vavaea
amicorum
(3)
Turraea
sericea
(1)
Humbertioturraea
sp.
(1)
Calodecaryia
crassifol
ia
(1)
Naregamia
alata
(1)
Pterorhachis
zenkeri
(4)
Nymania
capensis
(1)
Owenia
vernicosa
(4)
Malleastrum
mandenense
(4)
Ekebergia
capensis
(4)
Cipadessa
baccifera
(4)
Pseudoclausena
chrysogyne
(4)
Munronia
pinnata
(1)
Lepidotrichilia
volkensii
(4)
Quivisianthe papinae
Sandoricum koetjape
(7)
Sandoricum borneense
(7)
Azadirachta indica
(2)
Melia azedarach
(2)
Walsura tubulata
(4)
Cedrela odorata
Toona sp.
Khaya anthotheca
Swietenia macrophylla
Reinward
tiodendron
kinabaluense
(5)
Reinwardtiodendron
kostermansii
(5)
Reinwardtiodendron
humilis
(5)
Reinwardtiodendron
cinereum
(5)
Lansium
domesticum
(5)
Lansium
membranaceum
(5)
Aglaia australiensis
(5)
Aglaia
cucullata
(5)
Aglaia lawii
(5)
Aglaia teysmanniana
(5)
Aglaia archboldiana (5)
Aglaia vitiensis
(5)
Aglaia samoensis
(5)
Aglaia sapindina
(5)
Aglaia odorata
(5)
Aglaieae (5)
Guareeae (6)
Turraeeae + Trichilieae
(1) (4)
Sandoriceae (7)
Melieae(2)
Cedreleae
Swietenieae
Outgroup
Aglaia
sect. Aglaia
Aglaia
sect. Amoora
Aglaia
sect. Neoaglaia
Vavaeeae (3)
Trichilia
prieureana
(4)
Trichilia
emetica
(4)
Turraea
heterophylla
(1)
Fig. 1. One of the three most parsimonious trees obtained from the maximum parsimony analysis of the ITS nrDNA dataset
of 55 Meliaceae accessions. Tribal names and numbers after Pennington & Styles (1975). Numbers above branches are es-
timated branch lengths (DELTRAN optimization), numbers below branches are bootstrap percentages (5,000 replicates);
in italics. The arrow indicates a group not present in the strict consensus tree.
102
TAXON 57 (1) • February 2008: 98–108Muellner & al. • Tribes and generic relationships in Melioideae
of Turraeeae appear in a clade with representatives of
Trichilieae (67 BP; 100 PP; Fig. 3). Again, members of the
latter appear in other parts of the tree. Vavaea, Quivisian-
the and Sandoricum are interdigitated with Trichilieae.
Maximum likelihood results are almost identical to the
MP and Bayesian topologies (Fig. 4).
Maximum likelihood results based on the combined
ITS/rbcL matrix support Aglaieae as monophyletic; Guar-
eae as paraphyletic; Turraeeae as paraphyletic, appearing
in a clade with Trichilieae (Fig. 5). As for the single ITS
and rbcL analyses, members of the latter also appear in
other parts of the tree (Fig. 5).
100
98
80
56
64
58
67
50
93
92
99
100
100
100
100
90
100
97
100
100
100
90
74
100
100
92
57
94
87
100
94
82
100
100
100
84
100
100
80
100
100
100
56
100
100
100
Aphanamixis borneensis
(5)
Aphanamixis polystachya
(5)
Sphaerosacme decandra
(5)
Cabralea canjerana
(6)
Guarea glabra
(6)
Ruagea pubescens
(6)
Turraeanthus sp.
(6)
Heckeldora staudtii
(6)
Dysoxylum gaudichaudianum
(6)
Chisocheton macrophyllus
(6)
Synoum glandulosum
(6)
Anthocarapa nitidula
(6)
Pseudocarapanitidula
(6)
T
urraea sericea
(1)
Humbertioturraea
sp. (1)
Calodecaryia crassifolia
(1)
Naregamia alata
(1)
Pterorhachis zenkeri
(4)
Nymania capensis
(1)
Owenia vernicosa
(4)
Malleastrum mandenense
(4)
Ekebergia capensis
(4)
Cipadessa baccifera
(4)
Pseudoclausena chrysogyne
(4)
Lepidotrichilia volkensii
(4)
Quivisianthe papinae
Sandoricum koetjape
(7)
Sandoricum borneense
(7)
Azadirachta indica
(2)
Melia azedarach
(2)
Walsura tubulata
(4)
Cedrela odorata
Toona sp.
K
haya anthotheca
Swietenia macrophylla
Reinwardtiodendron kinabaluense
(5)
Reinwardtiodendron kostermansii
(5)
Reinwardtiodendron humilis
(5)
Reinwardtiodendron cinereum
(5)
Lansium domesticum
(5)
Lansium membranaceum
(5)
Aglaia australiensis
(5)
Aglaia cucullata
(5)
Aglaia lawii
(5)
Aglaia teysmanniana
(5)
Aglaia archboldiana (5)
Aglaia vitiensis
(5)
Aglaia samoensis
(5)
Aglaia sapindina
(5)
Aglaia odorata
(5)
Aglaieae (5) Guareeae (6)
Turraeeae + Trichilieae
(1) (4)
Sandoriceae (7)
Melieae(2)
Trichilieae (4)
Cedreleae
Swietenieae
Outgroup
Vavaea amicorum
(3)
Munronia pinnata
(1)
Vavaeeae (3)
Trichilia prieureana
(4)
Trichilia emetica
(4)
Turraea heterophylla
(1)
Fig. 2. Bayesian tree (10,000 total trees, burn-in of 500 trees) of the ITS nrDNA dataset of 55 Meliaceae accessions. Tribes
after Pennington & Styles (1975). Numbers above branches are Bayesian posterior probabilities.
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Muellner & al. • Tribes and generic relationships in MelioideaeTA XON 57 (1) • February 2008: 98–108
DISCUSSION
Tribal affiliation within Melioideae.
At a
glance, Pterorhachis Harms is distinct from all other
Meliaceae on morphological grounds and resembles
instead some members of Sapindaceae (Pennington &
Styles, 1975). Placed in Meliaceae tribe Turraeeae by
Harms (1940), a critical examination of morphology,
wood and pollen showed that it definitely belongs in
Meliaceae and is related to Trichilia L. (Pennington &
Styles, 1975). This study confirms the position of Pter-
orhachis in subfamily Melioideae and a close relation-
ship to tribes Trichilieae and Turraeeae (Figs. 1, 2).
Pennington & Styles (1975) demonstrated that sec-
ondary xylem provides good characters for subfamilial
delimitation in Meliaceae, as well as for delimitation of
tribal groups within Melioideae. They recognized two
groups of tribes within the latter: (1) Sandoriceae, Tur-
raeeae, Trichilieae (except Cipadessa) and Melieae, and
(2) Aglaieae, Guareeae (except Turraeanthus) and Va-
vaeeae. This pattern of relationship among tribes is broadly
confirmed by our study (Figs. 1–5). First, Aglaieae plus
9/96
2/67
13/
63
5/92
3/85
4/71
3/70
1
1
1
3
1
5
4
3
3
2
1
3
3
3
1
4/67
3/71
4/97
2/71
7
6
11
12
3/50
7
4
2
2
3
14
19
1
5/74
3
6
11
7
12/ 98
7
4/94
6
11
2/62
1
12
5/88
4
2
4/73
7
7
96
74
76
100
94
100
98
97
100
100
97
99
88
100
99
71
88
100
94
100
100
100
100
Aphanamixis polystachya
(5)
Cabralea canjerana
(6)
Astrotrichilia sp.
(4)
Guarea glabra
(6)
Ruagea pubescens
(6)
Heckeldora staudtii
(6)
Dysoxylum gaudichaudianum
(6)
Chisocheton macrophyllus
(6)
Synoum glandulosum
(6)
Pseudocarapanitidula
(6)
Vavaea amicorum
(3)
Turraea sericea
(1)
Humbertioturraea sp. (1)
Calodecaryia crassifolia
(1)
Naregamia alata
(1)
Nymania capensis
(1)
Owenia ver
nicosa
(4)
Malleastrum mandenense
(4)
Ekebergia capensis
(4)
Cipadessa baccifera
(4)
Munronia pinnata
(1)
Lepidotrichilia volkensii
(4)
Quivisianthe papinae
Sandoricum koetjape
(7)
Azadirachta indica
(2)
Melia azedarach
(2)
Pseudobersama mossambicensis
(4)
Walsura tubulata
(4)
Cedrela odorata
Toona sp.
Khaya anthotheca
Swietenia macrophylla
Reinwardtiodendron kinabaluense
(5)
Lansium domesticum
(5)
Aglaia elaeagnoidea (5)
Aglaieae (5)
Guareeae (6)
Turraeeae (1)
Sandoriceae (7)
Melieae (2)
Trichilieae (4)
Cedreleae
Sw ietenieae
Outgroup
Trichilia emetica
(4)
Trichilieae (4)
Trichilieae (4)
Vavaeeae (3)
Pseudoclausena chrysogyne
(4)
Fig. 3. One of the 7,199 most parsimonious trees obtained from the maximum parsimony analysis of the plastid rbcL data-
set of 37 Meliaceae accessions. Tribes after Pennington & Styles (1975). Numbers above branches are estimated branch
lengths (DELTRAN optimization), and bootstrap percentages (1,000 replicates; in italics). Numbers below branches are
Bayesian posterior probabilities (10,000 total trees, burn-in of 1,100 trees). Arrows indicate groups not present in the strict
consensus tree.
104
TAXON 57 (1) • February 2008: 98–108Muellner & al. • Tribes and generic relationships in Melioideae
Guareeae are always monophyletic. Second, Sandoriceae,
Turraeeae and Trichilieae are closely interrelated (Figs.
1–5). Vavaea is sister to the clade formed by Guareae
and Aglaieae in the MP ITS tree (Fig. 1) and is sister to
the clade uniting Aglaieae/Guareeae and most Turraeeae/
Trichilieae in the rbcL tree (Fig. 3).
Tribe Aglaieae.
Aglaieae, currently including
Aglaia Lour., Aphanamixis Blume, Lansium Correa,
Reinwardtiodendron Koord. and Sphaerosacme Wall. ex
Royle, owe their current circumscription to the work of
Pennington & Styles (1975). These five genera are re-
stricted to the Asian tropics and extend into the western
Pacific. All except Sphaerosacme, of which there is one
species, S. decandra, restricted to the Himalayas, are rep-
resented in Malesia.
The close morphological relationships of Aglaia, Lan-
sium and Reinwardtiodendron collectively with Aphana-
mixis and Sphaerosacme are reflected by our phyloge-
netic trees (Figs. 1–5; for a detailed taxonomic history
see Pennington & Styles, 1975; compare Mabberley &
al., 1995 and Muellner & al., 2005). A detailed account
on the evaluation of taxonomic concepts in the morpho-
logically variable genus Aglaia based on DNA data and
secondary metabolites was recently published by Muellner
& al. (2005).
Our ITS study includes members of all three sections
of Aglaia (sect. Aglaia, sect. Amoora, sect. Neoaglaia), all
but one species of Aphanamixis, monospecific Sphaero-
sacme and all but one species each of Lansium and
Reinwardtiodendron (we were unable to amplify these two
species). Aglaia forms a monophyletic group with Lan-
sium and Reinwardtiodendron (53 BP, Fig. 1; 99 PP, Fig.
2). Lansium and Reinwardtiodendron are monophyletic,
Aglaia is paraphyletic; the three sections of Aglaia
Aphanamixis polystachya
(5)
Cabralea canjerana
(6)
Astrotrichilia sp.
(4)
Guarea glabra
(6)
Ruagea pubescens
(6)
Heckeldora staudtii
(6)
Dysoxylum gaudichaudianum
(6)
Chisocheton macrophyllus
(6)
Synoum glandulosum
(6)
Pseudocarapa nitidula
(6)
Vavaea amicorum
(3)
Turraea sericea
(1)
Humbertioturraea
sp. (1)
Calodecaryia crassifolia
(1)
Naregamia alata
(1)
Nymania capensis
(1)
Owenia vernicosa
(4)
Malleastrum mandenense
(4)
Ekebergia capensi
s
(4)
Cipadessa baccifera
(4)
Munronia pinnata
(1)
Lepidotrichilia volkensii
(4)
Quivisianthe papinae
Sandoricum koetjape
(7)
Azadirachta indica
(2)
Melia azedarach
(2)
Pseudobersama mossambicensis
(4)
Walsura tubulata
(4)
Cedrela odorata
Toona sp.
Khaya anthotheca
Swietenia macrophylla
Reinwardtiodendron kinabaluense
(5)
Lansium domesticum
(5)
Aglaia elaeagnoidea (5)
Trichilia emetica
(4)
Pseudoclausena chrysogyne
(4)
0.005 substitutions/site
Fig. 4. Tree obtained from the maximum likelihood analy-
sis of the plastid rbcL dataset of 37 Meliaceae accessions.
Tribal numbers in brackets after species names.
Fig. 5. Tree obtained from the maximum likelihood analysis
of the combined ITS/rbcL dataset of 37 Meliaceae acces-
sions. Tribal numbers in brackets after species names.
Aphanamixis polystachya
(5)
Cabralea canjerana
(6)
Astrotrichilia sp.
(4)
Guarea glabra
(6)
Ruagea pubescens
(6)
Heckeldora staudtii
(6)
Dysoxylum gaudichaudianum
(6)
Chisocheton macrophyllus
(6)
Synoum glandulosum
(6)
Pseudocarapanitidula
(6)
Vavaea amicorum
(3)
Turraea sericea
(1)
Humbertioturraea sp. (1)
Calodecaryia crassifolia
(1)
Naregamia alata
(1)
Nymania capensis
(1)
Owenia vernicosa
(4)
Malleastrum mandenense
(4)
Ekebergia capensi
s
(4)
Cipadessa baccifera
(4)
Munronia pinnata
(1)
Lepidotrichilia volkensii
(4)
Quivisianthe papinae
Sandoricum koetjape
(7)
Azadirachta indica
(2)
Melia azedarach
(2)
Pseudobersama mossambicensis
(4)
Walsura tubulata
(4)
Cedrela odorata
Toona sp.
Khaya anthotheca
Swietenia macrophylla
Reinwardtiodendron kinabaluense
(5)
Lansium domesticum
(5)
Aglaia elaeagnoidea (5)
Trichilia emetica
(4)
Pseudoclausena chrysogyne
(4)
0.01 substitutions/site
105
Muellner & al. • Tribes and generic relationships in MelioideaeTA XON 57 (1) • February 2008: 98–108
each form monophyletic groups (Figs. 1, 2). Sphaero-
sacme is sister to Aphanamixis. Altogether, Aglaieae form
a monophyletic group (51 BP, Fig. 1; 92 PP, Fig. 2; 96 PP,
Fig. 3; Figs. 4–5).
Tribe Guareeae.
Guareeae comprise nine gen-
era, of which two, Cabralea A. Juss. and Ruagea Karst.,
are restricted to tropical America, two, Heckeldora Pierre
and Turraeanthus Baill., to Africa, three, Anthocarapa
Pierre, Chisocheton Blume and Dysoxylum Blume, to In-
domalesia and western Pacific and one, Synoum A. Juss.,
to tropical Australia.
Our analysis of ITS includes representatives of all gen-
era of Guareeae and therefore permits a detailed review of
relationships within the tribe. As a whole, Guareeae are a
paraphyletic group. Guarea and Ruagea (clade with 80 BP,
87 PP; Figs. 1, 2) are sister to Turraeanthus (Figs. 1, 2). The
relationship to Heckeldora, Chisocheton and Dysoxylum
lacks strong support; the same applies to Cabralea and
Synoum. Anthocarapa nitidula and a sample collected as
Pseudocarapa nitidula (regarded as synonym of the
latter; Mabberley & al. 1995) form a clade supported by
85 BP (Fig. 1) and 100 PP (Fig. 2). Although regarded as
a single species, the two samples exhibit a high number
of autapomorphies (26 and 34, respectively; Fig. 1), which
needs further investigation.
Tribe Vavaeeae.
Vavaeeae are a monogeneric
tribe of four species distributed from Sumatra eastwards
through Malesia to tropical Australia, Micronesia, Mela-
nesia and Polynesia. Vavaea occupies a morphologically
isolated position within Melioideae. It possesses most of
the individual morphological, anatomical and palynologi-
cal characters of the subfamily, but in a distinctive com-
bination enabling it to be easily distinguished from all
other genera. Vavaea has morphological similarities to
various tribes and genera: Turraeeae (leaves), Trichilieae
(fruit, seed, embryo), Sandoriceae (wood anatomy, pollen),
Aglaia (pollen). The ambiguous morphological relation-
ships are reflected in our phylogenetic trees: Vavaea oc-
cupies an isolated position sister to Aglaieae/Guareeae in
the MP ITS tree (Fig. 1) and is sister to the clade uniting
Aglaieae/Guareeae and most Turraeeae/Trichilieae in the
rbcL and combined trees (Figs. 3–5).
Tribe Trichilieae.
Trichilieae are a pantropical
tribe of twelve genera, Astrotrichilia (Harms) J.F. Leroy
ex T.D. Pennington & B.T. Styles, Cipadessa Blume, Eke-
bergia Sparrm., Heynea Roxb. ex Sims, Lepidotrichilia
(Harms) T.D. Pennington & B.T. Styles, Malleastrum
(Baill.) Leroy, Owenia F. Muell., Pseudobersama Verdc.,
Pseudoclausena T.P. Clark, Pterorhachis Harms, Trichilia
L. and Walsura Roxb.
The taxonomic history of Trichilieae is complex and
closely related to that of Turraeeae (reviewed in Pen-
nington & Styles, 1975). For morphological reasons,
Pennington & Styles (1975) concluded that Pterorhachis
and Cipadessa did not belong in Turraeeae, in which they
were placed by Harms (1940). A critical examination of
morphology, wood and pollen showed that Pterorhachis
is closely related to Trichilia, from which it differs prin-
cipally in having more numerous filament appendages
and from most species of Trichilia in its spheroidal pollen
grains (Pennington & Styles, 1975). Cipadessa is similar
in these same characters to Trichilieae as well, with an
hypothesized relationship to Ekebergia, and was there-
fore, like Pterorhachis, included in this tribe (Pennington
& Styles, 1975). Pseudobersama is thought to be closely
related to Trichilia (Pennington & Styles, 1975).
Our study of ITS reveals Pterorhachis as the clos-
est relative of Nymania, a member of Turraeeae (66 BP
and 84 PP; Figs. 1, 2). A close relationship of Cipadessa
to Ekebergia is confirmed by ITS (100 BP, 100 PP; Figs.
1, 2), though not by rbcL. In the analysis of rbcL, Pseudo-
bersama forms a clade with Trichilia, its closest morpho-
logical relative. As for the remaining genera of Trichilieae,
relationships based on ITS and rbcL are incongruent. Based
on our results, it is impossible to keep Trichilieae separated
from Turraeeae, Vavaeeae and Sandoriceae (Figs. 1–5). To
reach a robust and well-resolved phylogenetic appreciation
of Trichilieae, sampling of additional taxa on species level
and the collection of much more data will be necessary.
Tribe Turraeeae.
Turraeeae comprise six or
seven genera: Calodecaryia Leroy, Humbertioturraea
Leroy, Munronia Wight, Nymania S.O. Lindb., Turraea
L. including Naregamia Wight & Arn., and perhaps an
undescribed genus (Turraea breviflora” Ridley), all re-
stricted to the Old World tropics. The largest is Turraea,
which is the most widespread; the rest are small genera,
one or two restricted to Indomalesia, two to Madagascar,
one to southern Africa and one found in both India and
southern Africa (Mabberley & al., 1995).
Pennington & Styles (1975) used Turraeeae in the
introduction of their generic monograph to illustrate that
most tribes in Meliaceae can only be diagnosed by using a
combination of several differential characters (as defined
by White, 1962). They stated that members of Turraeeae
cannot be distinguished from other Meliaceae on the basis
of a single diagnostic character and that most character-
states typical of the tribe have at least a few exceptions and
also occur at least occasionally in other tribes, but always
in markedly different combinations. The overall pattern,
however, was such that all members of Turraeeae possess
many more of the tribal character-states than any excluded
species. Thus, Pennington & Styles (1975) claimed Tur-
raeeae, as well as all other tribes in the monograph, to
be objectively circumscribed, being based on gaps in the
pattern of variation.
Our investigation includes representatives of all gen-
era of Turraeeae and therefore allows a detailed review
of relationships within the tribe. In our analysis of ITS,
106
TAXON 57 (1) • February 2008: 98–108Muellner & al. • Tribes and generic relationships in Melioideae
Nymania is sister (as part of a clade with Pterorhachis) to
the “core group” of Trichilieae, formed by Turraea, Hum-
bertioturraea, Calodecaryia and Naregamia (Figs. 1, 2).
In the rbcL tree, Nymania is again sister to this core group
(Figs. 3–4). Naregamia is sister to the clade formed by
Turraea, Humbertioturraea and Calodecaryia in both the
single ITS and rbcL, and in the combined trees (Figs. 1–5).
The separation of Naregamia from these three genera is
well supported in ITS and rbcL trees (99 BP, Fig. 1; 100 PP,
Fig. 2; 71 BP, 94 PP, Fig. 3), emphasizing that Naregamia
is genetically distinguishable from Turraea. Naregamia
was reduced to synonymy with Turraea by Cheek (1996;
for a detailed discussion of characters and the status of
Naregamia and Turraea see Cheek, 1990). Cheek (1990)
stated that, as far as seed structure was concerned, Nar-
egamia could not be separated from Turraea. Previously,
Pennington & Styles (1975) had claimed Naregamia to be
easily distinguished from Turraea by combined charac-
teristics of leaves, the staminal tube and seed structure.
Our data agree with these earlier findings of Pennington
& Styles (1975); we propose to keep Naregamia separate
from Turraea. The position of Munronia remains ambigu-
ous, as expected by its morphological intermediacy be-
tween typical Turraeeae and the remainder of Melioideae
(Figs. 15). Unfortunately, we were unable to amplify
samples of Turraea breviflora collected from herbarium
specimens located in Kepong (KEP), Malay Peninsula,
and in Kew (K), U.K., due to the old age of specimens and
resulting poor quality of DNA extracts (high degradation).
The species, according to Mabberley & al. (1995) perhaps
an undescribed genus, is known only from a few localities
in the Malay Peninsula and Singapore. The fruit has never
been observed; recent collections are lacking.
As for Trichilieae, an increase of sampling on species
level and the collection of additional DNA data will be
necessary to make final decisions about a new circum-
scription of Trichilieae, especially the inclusion/exclusion
of Munronia in the tribe.
Tribe Sandoriceae.
Sandoriceae are monoge-
neric with five species, all but one (S. koetjape) restricted
to western Malesia (Mabberley & al., 1995). Pennington
& Styles (1975) claimed Sandoricum to be a morpho-
logically distinct genus, without a close relationship to
Dysoxylum as proposed by Harms (1940) or to Guareeae.
Sandoricum is at once identifiable by trifoliate leaves,
the ribbed staminal tube, characteristic style-head with
divided stigma and indehiscent drupaceous fruit, presum-
ably the reason Pennington & Styles (1975) placed the
genus in its own tribe.
Our data confirm that Sandoricum has no close rela-
tionship to either Dysoxylum or Guareeae (Figs. 1–5). In
our analysis of ITS, the two species of Sandoricum form
a strongly supported clade (100 BP, Fig. 1; 100 PP, Fig.
2) and are characterized by a relatively high number of
autapomorphies (29, Fig. 1). In the rbcL trees, Sandori-
cum is sister to Ekebergia and Quivisianthe (Figs. 3–4)
and again characterized by a relatively high number of
autapomorphies (11, Fig. 3).
Tribe Melieae.
Melieae comprise two genera,
Melia L. (one to possibly three species) and Azadirachta
A. Juss. (two species), in the wild state restricted to the
Old World Tropics. Melia and Azadirachta are similar
morphologically (Pennington & Styles, 1975). Both gen-
era share a number of anatomical characters not recorded
elsewhere in Meliaceae (e.g., clusters of minute vessels
with spiral wall thickening). Our single and combined
analyses of ITS and rbcL confirm monophyly of Melieae
(Figs. 1–5). In the ITS MP and Bayesian analyses, Melieae
are sister to all other Melioideae (Figs. 1, 2). The same is
true for the combined analysis (Fig. 5). In the analyses of
rbcL, Melieae are sister to Owenia (98 BP, 100 PP, Fig. 3;
Fig. 4), and this clade is sister to all other Melioideae.
Quivisianthe (Quivisianthoideae).
Although
treated in a monogeneric subfamily by Pennington & Styles
(1975), the authors mentioned in their generic monograph
that the genus is similar in its floral structure to some
genera in Trichilieae and that the complete staminal tube
without appendages and with the anthers or antherodes
inserted on the margin is similar to that of Ekebergia. Our
ITS and rbcL data confirm the position of Quivisianthe
in Melioideae (Figs. 15). In the rbcL tree, Quivisianthe
exhibits a close relationship to Ekebergia (clade with 74
BP, 100 PP; Fig. 3), whereas for ITS it appears as sister to
Walsura (Figs. 1, 2). In the combined Bayesian (tree not
shown) and ML analyses (Fig. 5), Quivisianthe occupies
an isolated position, in the MP analysis the genus appears
as sister to Walsura (tree not shown).
Concluding remarks.
DNA data of Melioideae
and related genera contribute to a better understanding
of the intricate systematic relationships of this group of
trees that constitute an important component of moist
tropical forests world-wide. This study is the first to
assess circumscription of Melioideae and the com-
ponent tribes in detail with data independent of mor-
phology. Maximum parsimony, maximum likelihood
and Bayesian analyses of nuclear ITS, compared with
analyses based on plastid rbcL, confirm monophyly for
Aglaieae, Sandoriceae and Melieae, an isolated position
for Vavaeeae, the position of Pterorhachis and Quivisi-
anthe in Melioideae, and close relations between Tur-
raeeae and Trichilieae. Trichilieae are the most complex
clade. Anthocarapa and Pseudocarapa, regarded as syno-
nym of the latter, form a clade, but exhibit each a high
number of autapomorphies, which needs further inves-
tigation. We propose to keep Naregamia separate from
Turraea because the two are not exclusively related. These
taxonomic decisions are based on DNA data as well as
morphological variation.
107
Muellner & al. • Tribes and generic relationships in MelioideaeTA XON 57 (1) • February 2008: 98–108
ACKNOWLEDGEMENTS
The authors thank Terry D. Pennington (Royal Botanic
Gardens, Kew) for his critical reading of an earlier draft of
the manuscript, and two reviewers for their helpful comments.
Financial support for this study was provided by the Austrian
Science Fund to RS (FWF grant no. P14150-BOT), an EU Marie
Curie Fellowship to ANM (project no. MEIF-CT-2003–502194)
and the Senckenberg Research Institute.
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TAXON 57 (1) • February 2008: 98–108Muellner & al. • Tribes and generic relationships in Melioideae
Appendix. Vouchers, origin and GenBank accession numbers* of the material used in the study.
SUBFAMILY, Tribe, Species, Collector number and location of herbarium voucher, Origin, GenBank accession numbers
MELIOIDEAE, Turraeeae, Calodecaryia crassifolia Leroy, Croat 31521 (K), Madagascar, DQ861631, AY128216; Humbertio-
turraea sp. (H. labatii Lescot ined.), Bardot-Vaucoulon 160 (K), Madagascar, DQ861632, DQ238058; Munronia pinnata (Wall.)
Theob., Samuel 6 (WU), Sri Lanka, DQ861604, AY128236; Naregamia alata Wight & Arn., Kanodia 89603 (K), India, DQ861629,
DQ238059; Nymania capensis Lindb., Chase 270 (NCU), South Africa, DQ861633, AY128238; Turraea sericea Sm., Civeyrel
1336 (K), Madagascar, DQ861630, AY128245; Turraea heterophylla Sm., Küppers 2212 (FR), West Africa, EF136578; Melieae,
Azadirachta indica A. Juss., Samuel 5 (WU), Sri Lanka, AY695594, AY128215; Melia azedarach L., Chase 2867 (K), K Living
Collection 1953-37801 [donation from KYGH], AY695595, AY128234; Vavaeeae, Vavaea amicorum Benth., Katik & al. 74722 (K),
Papua New Guinea, DQ861610, DQ238066/67; Trichilieae, Astrotrichilia sp., Richard 25 (K), Madagascar, DQ2388060, Cipadessa
baccifera Miq., Chase 1310 (K), Indonesia (Bogor III.B.90), DQ861627, AY128224; Ekebergia capensis Sparrm., MG 246 (Cynthia
Morton), South Africa, DQ861623, AY128228; Lepidotrichilia volkensii (rke) J.-F. Leroy ex B.T. Styles & F. White, Hughes
189 (K), Tanzania, DQ861620, DQ238061; Malleastrum mandenense Leroy, Cheek & al. 3-17-5 (K), Madagascar, DQ861626,
DQ238062; Owenia vernicosa F. Muell., Evans M3071, Australia, DQ861622, DQ238063; Pseudobersama mosambicensis (Sim)
Verdc., Bidgood, Abdallah & Vollesen 1426 (K), Tanzania, DQ238064; Pseudoclausena chrysogyne (Miq.) T.P. Clark, Muellner 2052
(FR), Malaysia (FRIM Arboretum), DQ861602, DQ238065; Pterorhachis zenkeri Harms, Breteler 2741 (K), Cameroon, DQ861628;
Trichilia emetica Vahl, Chase 552 (K), K Living Collection 1984-1568, AY128244; Trichilia emetica Vahl, Sieglstetter 15 (FR),
West Africa, EF136577; Trichilia prieureana A. Juss., Neumann 1518 (FR), West Africa, EF136576; Walsura tubulata Hiern, Chase
1314 (K), Indonesia (Bogor VIII.B.127), DQ861625, AY128246; Aglaieae, Aglaia archboldiana A.C. Smith, Greger 696 (WU),
Fiji, AY695524; Aglaia elaeagnoidea Benth., Samuel 4 (WU), Sri Lanka, AY128209; Aglaia odorata Lour, Greger 903 (WU),
Thailand, AY695552; Aglaia samoensis A. Gray, Greger 752 (WU), Samoa, AY695557; Aglaia sapindina (F. von Muell.) Harms,
Greger 669 (WU), Australia, AY695558; Aglaia vitiensis A.C. Smith, Greger 691 (WU), Fiji, AY695569; Aglaia lawii (Wight) C.J.
Saldanha, Greger 573 (WU), Thailand, AY695573; Aglaia teysmanniana (Miq.) Miq., Greger 704 (WU), Thailand, AY695539;
Aglaia australiensis Pannell, Greger 662 (WU), Australia, AY695571; Aglaia cucullata (Roxb.) Pellegrin, Brunei Museum s.n. (K),
Brunei, AY695572; Lansium domesticum Correa, Chase 2113 (K), Indonesia (Bogor, III.B.100), AY695586, AY128232; Lansium
cf. membranaceum (Kosterm.) Mabb., Pannell 1934 (FHO), Sumatra, DQ861611; Reinwardtiodendron cinereum (Hiern) Mabb.,
F.R.I. (Forest Res. Inst.) 26877 (K), Malaysia (Perak), AY695588; Reinwardtiodendron humile (Hassk.) Mabb., Trichon VT 641
(FHO), Sumatra, DQ861612; Reinwardtiodendron kinabaluense (Kosterm.) Mabb., Lamb ALFB 112/87 (K), Malaysia (Borneo),
AY695589, DQ238054; Reinwardtiodendron kostermansii (Prijanto) Mabb., Kostermans 19215 (K), Indonesia (W Sumbawa),
DQ861634; Aphanamixis borneensis Harms, Beaman 8208 (K), Malaysia (Borneo), AY695583; Aphanamixis polystachya (Wall.)
R.N. Parker, Samuel 14 (WU), Sri Lanka, AY695584; Aphanamixis polystachya (Wall.) R.N. Parker, Chase 2109 (K), Indonesia
(Bogor III.C.68a), AY128213; Sphaerosacme decandra (Wal.) T.D. Penn., Williams & Stainton 8533 (K), Ecuador, AY695590;
Guareeae, Anthocarapa nitidula (Benth.) T.D. Penn., Chanel 1110 (K), Melanesia, DQ861615; “Pseudocarapanitidula (Benth.)
T.D. Penn., Chase 3313 (K), Australia, DQ861616, DQ238056; Cabralea canjerana (Vell.) Mart., Pennington 17067 (K), Peru,
DQ861617, DQ238055; Chisocheton macrophyllus King, Chase 1309 (K), Indonesia (Bogor III.F.30a), DQ861613, AY128221;
Dysoxylum gaudichaudianum (A. Juss.) Miq., Chase 1312 (K), Indonesia (Bogor III.F.90), DQ861619, AY128227; Guarea glabra
Vahl, Chase 336 (NCU), U.S.A., AY695591, AY128229; Heckeldora staudtii (Harms) Staner, Chase 3311 (K), Cameroon, AY695592,
AY128230; Ruagea pubescens Karst., Pennington & Frere 13761 (K), Ecuador, AY695593, DQ238057; Synoum glandulosum
(Sm.) A. Juss., Schodde 5101 (K), Australia, DQ861618, AY128242; Turraeanthus sp., Carvalho 4348-1 (K), Equat. Guinea,
DQ861614; Sandoriceae, Sandoricum koetjape (Burm. f.) Merr., Muellner 2050 (FR), Thailand, DQ861600, DQ238068; Sando-
ricum borneense Miq., Chase 1313 (K), Indonesia (Bogor, III.B.92), DQ861601; Quivisianthe papinae Baill., Phillipson 1650 (K),
Madagascar, DQ861605, AY128239; SWIETENIOIDEAE, Cedreleae, Cedrela odorata L., Chase 2112 (K), Indonesia (Bogor
III.B.2), DQ861606, AY128220; Toona sp., Terrazas s.n. (K), Australia, DQ861607, AY128243; Swietenieae, Khaya anthotheca
C. DC., Chase 2859 (K), K Living Collection 1967-35601 (source plant: Amherst College, Massachusetts), DQ861608, AY128231;
Swietenia macrophylla King, Chase 250 (NCU), U.S.A., DQ861609, AY128241.
*All sequences are deposited in GenBank; new sequences are deposited under the accession numbers DQ861600–DQ861602,
DQ861604DQ861620, DQ861622–DQ861623, DQ861625DQ861634 and EF136576EF136578 (http://www.ncbi.nlm.nih
.gov/).
... Kribs (1930) suggested that Swietenioideae be raised to the rank of family (as Swieteniaceae) because the genera form a distinct homogeneous group in terms of anatomical and morphological characters. Seven tribes were recognized in Melioideae, defined by morphological, anatomical and palynological characters (Pennington & Styles, 1975;Muellner et al., 2008). South African indigenous species of the family belong to Melioideae, with the exception of Entandrophragma caudatum (Sprague) Sprague, which is a member of Swietenioideae. ...
... Evolutionary pathways for wood anatomical features were identified by mapping distinctive characters on a subsample of the majority rule consensus tree recovered from the parsimony and Bayesian analyses of a data set of nuclear ITS rDNA sequences (Muellner et al., 2008). The new data and wood anatomical information for other genera of Meliaceae (Kribs, 1930;Panshin, 1933;Kromhout, 1975;Pennington & Styles 1975;Gasson & Cheek, 1992;InsideWood, 2004onwards) were analysed. ...
... Scale bars: A, D = 20 µm; B, C, E, F = 10 µm. by phylogenetic relationships between these genera (Muellner et al., 2008;Muellner-Riehl et al., 2016). Like other Meliaceae, these species share exclusively simple perforation plates and alternate (mostly minute to small) intervessel pits; they also lack the crystals in marginal ray cells that is a characteristic trait for the subfamily Melioideae (Kribs, 1930;Panshin, 1933;Metcalfe & Chalk, 1950;Pennington & Styles, 1975;InsideWood, 2004onwards;Wheeler, 2011). ...
Article
Wood structure in seven South African species of Ekebergia, Nymania, Trichilia and Turraea (Meliaceae) was studied and compared with data for other genera of the subfamily Melioideae to elucidate phylogenetic relationships and pathways of trait evolution in this group and to clarify the ecological significance of some wood characters. Non-septate fibres, the presence of crystals in axial parenchyma and relatively wide (> triseriate) heterocellular rays are the ancestral conditions for Melioideae. A loss of crystals confirms the monophyly of the clade embracing tribe Turraeeae and Pterorhachis. Uniseriate rays are synapomorphic for the Turraeeae+Trichilieae clade with secondary gains of wider rays in the Nymania+Pterorhachis lineage and in some species of Turraea and Trichilia. A close relationship between Nymania and Pterorhachis was also confirmed by their similarity in having small intervessel pits. Trichilia is distinctive by its homocellular rays made of square and upright cells. The close affinity between Ekebergia and Quivisianthe is confirmed by their similar composition of rays that consist only of procumbent cells. Nymania capensis and Turraea obtusifolia share narrower (< 50 µm) and more numerous (> 70 per mm2) vessel lumina than other species; these are adaptive features for their habitat.
... Simaroubaceae is a relatively small family (Table 1) currently formed almost only by members of the former subfamily Simarouboideae of Engler (1931), which included five other subfamilies; four of these have been excluded from Sapindales, while Kirkioideae was raised as Kirkiaceae (Clayton 2011). The Meliaceae is currently divided in two subfamilies: the early diverging Cedreloideae, and Melioideae, which is the most diversified (Koenen et al. 2015;Muellner et al. 2008). ...
Article
Sapindales is a monophyletic order within the malvid clade of rosids. It represents an interesting group to address questions on floral structure and evolution due to a wide variation in reproductive traits. This review covers a detailed overview of gynoecium features, as well as a new structural study based on Trichilia pallens (Meliaceae), to provide characters to support systematic relationships and to recognize patterns of variations in gynoecium features in Sapindales. Several unique and shared characteristics are identified. Anacrostylous and basistylous carpels may have evolved multiple times in Sapindales, while ventrally bulging carpels are found in pseudomonomerous Anacardiaceae. Different from previous studies, similar gynoecium features, including degree of syncarpy, ontogenetic patterns, and PTTT structure, favors a closer phylogenetic proximity between Rutaceae and Simaroubaceae, or Rutaceae and Meliaceae. An apomorphic tendency for the order is that the floral apex is integrated in the syncarpous or apocarpous gynoecium, but with different length and shape among families. Nitrariaceae shares similar stigmatic features and PTTT structure with many Sapindaceae. As the current position of both families in Sapindales is uncertain, floral features should be investigated more extensively in future studies. Two different types of gynophore were identified in the order: either derived from intercalary growth below the gynoecium as a floral internode, or by extension of the base of the ovary locules as part of the gySapindales is a monophyletic order within the malvid clade of rosids. It represents an interesting group to address questions on floral structure and evolution due to a wide variation in reproductive traits. This review covers a detailed overview of gynoecium features, as well as a new structural study based on Trichilia pallens (Meliaceae), to provide characters to support systematic relationships and to recognize patterns of variations in gynoecium features in Sapindales. Several unique and shared characteristics are identified. Anacrostylous and basistylous carpels may have evolved multiple times in Sapindales, while ventrally bulging carpels are found in pseudomonomerous Anacardiaceae. Different from previous studies, similar gynoecium features, including degree of syncarpy, ontogenetic patterns, and PTTT structure, favors a closer phylogenetic proximity between Rutaceae and Simaroubaceae, or Rutaceae and Meliaceae. An apomorphic tendency for the order is that the floral apex is integrated in the syncarpous or apocarpous gynoecium, but with different length and shape among families. Nitrariaceae shares similar stigmatic features and PTTT structure with many Sapindaceae. As the current position of both families in Sapindales is uncertain, floral features should be investigated more extensively in future studies. Two different types of gynophore were identified in the order: either derived from intercalary growth below the gynoecium as a floral internode, or by extension of the base of the ovary locules as part of the gynoecium. Sapindales share a combination of gynoecial characters but variation is mostly caused by different degrees of development of the synascidiate part relative to the symplicate part of carpels, or the latter part is absent. Postgenital fusion of the upper part of the styles leads to a common stigma, while stylar lobes may be separate. Due to a wide variation in these features, a new terminology regarding fusion is proposed to describe the gynoecium of the order.noecium. Sapindales share a combination of gynoecial characters but variation is mostly caused by different degrees of development of the synascidiate part relative to the symplicate part of carpels, or the latter part is absent. Postgenital fusion of the upper part of the styles leads to a common stigma, while stylar lobes may be separate. Due to a wide variation in these features, a new terminology regarding fusion is proposed to describe the gynoecium of the order.
... Simaroubaceae is a relatively small family (Table 1) currently formed almost only by members of the former subfamily Simarouboideae of Engler (1931), which included five other subfamilies; four of these have been excluded from Sapindales, while Kirkioideae was raised as Kirkiaceae (Clayton 2011). The Meliaceae is currently divided in two subfamilies: the early diverging Cedreloideae, and Melioideae, which is the most diversified (Koenen et al. 2015;Muellner et al. 2008). ...
... Quivisianthoideae and Capuronianthoideae each contain a single monotypic genus. Phylogenomic analysis with the four subfamilies supported the inclusion of the members of the two small subfamilies, Quivisianthe and Capuronianthus, within Melioideae and Swietenioideae, respectively (Muellner et al. 2003(Muellner et al. , 2006(Muellner et al. , 2008. As discussed here, the genera are arranged in two subfamilies, Cedreloideae and Melioideae. ...