Support for an expanded family concept of Malvaceae within a recircumscribed order Malvales: A combined analysis of plastid atpB and rbcL DNA sequences

Abstract

Sequence analyses of the plastid genesatpB andrbcL support an expanded order Malvales. Within this alliance, core Malvales are clearly supported and comprise most genera that have previously been included in Sterculiaceae, Tiliaceae, Bombacaceae, and Malvaceae. Additional well supported malvalean alliances include the bixalean clade (Bixaceae, Diegodendraceae, and Cochlospermaceae), the cistalean clade (Cistaceae, Dipterocarpaceae, and Sarcolaenaceae) and Thymelaeaceae (including Gonystyloideae and Aquilarioideae). Our results indicate sister-group relationships between (1) Neuradaceae and the cistalean clade; (2) Sphaerosepalaceae and Thymelaeaceae; (3) these two clades (1 and 2); and (4) all these and an alliance comprising the bixalean clade and core Malvales, but this pattern is weakly supported by the bootstrap. The affinities of Muntingiaceae andPetenaeaare especially ambiguous, although almost certainly they are Malvaless.l.The traditional delimitation of families within core Malvales is untenable. Instead, we propose to merge Sterculiaceae, Tiliaceae and Bombacaceae with Malvaceae and subdivide this enlarged family Malvaceae into nine subfamilies based on molecular, morphological, and biogeographical data: (1) Byttnerioideae, including tribes Byttnerieae, Lasiopetaleae and Theobromeae (all of which have cucullate petals) and Hermannieae; (2) Grewioideae, including most genera of former Tiliaceae; (3) Tilioideae, monogeneric in our analysis; (4) Helicteroideae, comprising most of the taxa previously included in Helictereae, plusMansonia,Triplochiton(indicating that apocarpy evolved at least twice within Malvaceae) and possibly Durioneae; (5) Sterculioideae, defined by apetalous, apocarpous, usually unisexual flowers with androgynophores; (6) Brownlowioideae, circumscribed as in previous classifications; (7) Dombeyoideae, expanded to includeBurretiodendron,Eriolaena,Pterospermum, andSchoutenia; (8) Bombacoideae, corresponding to former Bombacaceae (without Durioneae) but including Fremontodendreae andPentaplaris; (9) Malvoideae, monophyletic but difficult to delimit from Bombacoideae, which with more data and taxon sampling than here might prove to be paraphyletic without Malvoideae.

Full text

BotanicalJoumal
oJh
Linnean
So&@
(1999),
129:
267-303.
With
4
figures
Article
ID:
bojl.
1998.0226, available
online
at
http://www.idealibrary.com
on
ID
E
b[
@
c
Support for
an
expanded family concept
of
Malvaceae within
a
recircumscribed order
Malvales:
a
combined analysis of plastid
atpB
and
rbcL
DNA
sequences
CLEMENS BAYER,'* MICHAEL
F.
FAY,' ANETTE Y. DE BRUIJN,'
VINCENT SAVOLAINEN,3 CYNTHIA M. MORTON: KLAUS KUBITZKI,'
WILLIAM
S.
ALVERSON,5
MARK
W.
CHASE'
I
Universitat Hamburg, Institut4r Alkemeine Botanik und Botanischer Garten, Ohnhorststra be
18,
22609
Hamburg, Germany
Ryal Botanic Gardens, Kew, Richmond, Surrty
W9
3DS
Consmatoire et Jardin Botaniques,
1292
Geneva
G3
IBSG, Universip ofhusanne,
I015
Department
of
Botany, Universip
fl
Reading, Reading RG6
2AS
Haluard Universip Herbaria,
22
Divinip Avenue, Cambridge,
MA
02138,
USA.
Luusanne, Switzerland
Received
April
1998; acrepkddfor publication
September
I998
Sequence analyses of the plastid genes atpB and
rbcL
support an expanded order Malvales.
Within this alliance, core Malvales are clearly supported and comprise most genera that
have previously been included in Sterculiaceae, Tiliaceae, Bombacaccae, and Malvaceae.
Additional well supported malvalean alliances include the bixalean clade (Bixaceae, Diego-
dendraceae, and Cochlospermaceae), the cistalean clade (Cistaccac, Dipterocarpaceae, and
Sarcolaenaceae) and Thymelaeaceae (including Gonystyloideae and Aquilarioideae). Our
results indicate sister-group relationships between
(I)
Neuradaceae and the cistalean clade;
(2)
Sphaerosepalaceae and Thymelaeaceae;
(3)
these
two
clades
(1
and
2);
and
(4)
all
these
and an alliance comprising the bixalean clade and core Malvales, but this pattern
is
weakly
supported by the bootstrap. The affinities of Muntingiaceae and
Pehaea
are especially
ambiguous, although almost certainly they are Malvales
s.1.
The traditional delimitation of
families within core Malvales
is
untenable. Instead, we propose to merge Sterculiaceae,
Tiliaceae and Bombacaceae with Malvaceae and subdivide this enlarged family Malvaceae
into nine subfamilies based on molecular, morphological, and biogeographical data:
(1)
Byttnerioideae, including tribes Byttnerieae, Lasiopetaleae and Theobromeae (all of which
have cucullate petals) and Hermannieae;
(2)
Grewioideae, including most genera
of
former
Tiliaceae;
(3)
Tilioideae, monogeneric in our analysis;
(4)
Helicteroideae, comprising most
of the taxa previously included in Helictereae, plus
Mansonia, Triplochiton
(indicating that
apocarpy evolved
at
least twice within Malvaceae) and possibly Durioneae;
(5)
Sterculioideae,
defined by apetalous, apocarpous, usually unisexual Rowers with androgynophores;
(6)
Brownlowioideae, circumscribed as
in
previous classifications;
(7)
Dombeyoideae, expanded
to include
Burretiodendmn,
Eriolaaa,
Rmspemum,
and
Schoutenia;
(8)
Bombacoideae, cor-
responding to former Bombacaceae (without Durioneae) but including Fremontodcndreae
*
Corresponding author. Email:
c.bayer@botanik.uni-hamburg.de
00241074/99/040267+37
$30.00/0
267
0
1999 The
Linnean
Society
of
London
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268
C.
BAYER
ETAL.
and
PeritaplanS;
(9) Malvoideae, monophyletic but difficult to delimit from Bombacoideae,
which with more data and taxon sampling than here might prove to be paraphyletic without
Malvoideae.
0
1999
The
Linnean
Society
of
London
ADDITIONAL
KEY
WORDS:-Sterculiaceae
-
Tdiaceae
-
Bombacaceae
-
Bixales
-
Cistales
-
apocarpy
-
pollen
-
molecular systematics.
CONTENTS
Introduction
.......................
268
Material and methods
...................
269
DNA extraction
....................
270
Amplification and sequencing
of
atpB and
rbcL
..........
270
Data analysis
.....................
27
1
Results
........................
272
Analysis
of
rbcL
....................
272
Analysis
of
atpB
....................
274
Combined analysis
...................
275
Discussion
.......................
277
Malvales
sm
lato
...................
277
Circumscription of core Malvales
..............
279
Subdivision of core Malvales
................
280
Conclusion
.......................
290
Acknowledgements
....................
2
90
References
.......................
290
Appendix1
.......................
296
Appendix2
.......................
299
INTRODUCTION
Order Malvales has been variously defined: narrow circumscriptions have restricted
it to Tiliaceae, Sterculiaceae, Bombacaceae, Malvaceae and Elaeocarpaceae (Cron-
quist, 1988), but many authors have included additional families such as Bixaceae,
Cistaceae, Cochlospermaceae, Diegodendraceae, Dipterocarpaceae, Dirachmaceae,
Huaceae, Peridiscaceae, Plagiopteraceae, Sarcolaenaceae, Scytopetalaceae, Sphaero-
sepalaceae and Thymelaeaceae (e.g. Dahlgren, 1983; Huber, 199
1
;
Thorne, 1992;
Takhtajan, 1997). It has become apparent that the closely related Tiliaceae, Ster-
culiaceae, Bombacaceae, and Malvaceae constitute the monophyletic core Malvales,
if
putative relatives such
as
Elaeocarpaceae, Flacourtiaceae, Muntingiaceae and
Neuradaceae are removed (Chase
et
al.,
1993, and unpubl.; Judd
&
Manchester,
1997; Fay
et
al.,
1998a; Bayer, 1999 and unpubl.; Bayer, Chase
&
Fay, 1998;
Alverson
et
al.,
1998). The expanded order Malvales includes some but not all of
the families mentioned above. Previous morphological and molecular studies support
the exclusion
of
Elaeocarpaceae, Flacourtiaceae, Huaceae, Scytopetalaceae, Di-
rachmaceae, Peridiscaceae, and Plagiopteraceae (Chase
et
al.,
1993, and unpubl.;
Appel, 1996; Morton
et
al.,
1996; 1997; Fay
d
al.,
1998a; Alverson
et
al.,
1998;
Thulin
et
al.,
1998; C. Bayer, unpubl.).
Although the component families of the expanded Malvales have been identified
in previous studies, the interrelationships between malvalean families, especially
within core Malvales, are largely unknown. This is largely a result of the problematic
delimitation of the core families, which appear to be based on tradition rather than
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MOLECULAR SYSTEMATICS
OF
MALVALES
269
characters. The limits of Malvaceae/Bombacaceae, Sterculiaceae/Tiliaceae and
Sterculiaceae/Bombacaceae
remain nebulous.
As
a
consequence, taxa such as
Fremontodendreae, Gossypieae, Hibisceae,
Corchompis,
and
Nesogordonia
have been
moved between families. Especially Tiliaceae in their traditional circumscription
(e.g. de Candolle, 1824; Bentham
&
Hooker, 1862; Bocquillon, 1866; Baillon, 1873;
von Szyszylowicz, 1885; Hutchinson, 1967) have been used for filing genera that
could not be otherwise placed. Even authors who had a narrower and more critical
concept of Tiliaceae (e.g. Burret, 1926) included aberrant genera such as
Neotessmanniu
(Bayer
et
al.,
1998). Ongoing morphological studies (C. Bayer, unpubl.) indicate that
many Tiliaceae
s.1.
such as
Burretiodendmn, Schoutenia,
and even
lilia
are more closely
related to Sterculiaceae than to the grewioid alliance, which includes the majority
of Tiliaceae. However, all such considerations remain vague because none of these
families is unambiguously defined by morphological characters.
The distribution
of
distinctive characters derived from inflorescence, flower, and
pollen morphology is only partly consistent with the traditional classifications. For
instance, spinose or spinulose pollen occurs in all four families of core Malvales
(Erdtman, 1952), and it is not known to what extent this scattered distribution is
due to common ancestry or to parallel evolution; the same applies to the occurrence
of an epicalyx (Bayer, 1999). Sterculiaceae, to mention another example, have
been subdivided into subfamilies Sterculioideae and Byttnerioideae (Thorne, 1992;
Takhtajan, 1997; or even elevated as families: Edlin, 1935) on the basis of the
apetalous, unisexual, and apocarpous flowers of Sterculioideae.
If
secondary apocarpy
has evolved only once within Sterculiaceae, genera such
as
Helicteres, Mansonia,
and
Tiplochiton
would have to be referred to Sterculioideae on the basis
of
their apocarpous
gynoecia, even though they exhibit hermaphrodite flowers with petals, which are
not found
in
the other apocarpous genera.
In view of the difficulties with the distribution of morphological characters, the
present study based on DNA sequences was undertaken
as
an additional approach
to clarifjr the interrelationships among malvalean families. We decided to analyse
two
plastid genes,
rbcL
and
atpB,
since in some cases the latter provides greater
resolution than
rbcL
(Hoot, Culham
&
Crane, 1995), and a combination of data
sets may increase support of clades (as estimated by the bootstrap, Felsenstein, 1985;
Soltis
et
a/.,
1997).
MATERIAL
AND
METHODS
As is evident from previous molecular studies (Chase
et al.,
1993; Gadek
et al.,
1996; Fay
et
al.,
1998a; Alverson
et
ul.,
1998), Malvales are related to expanded
Capparales and Sapindales, which have been used as outgroups in the present study.
To cover the major lineages within Malvales we included representatives of most
known or suspected alliances as well as some isolated taxa
of
unknown affinities;
this was restricted by the availability of suitable plant material. For most taxa, the
same samples were used to sequences both atpB and
rbcL
(Appendix
1).
On certain
occasions, however, we combined sequences of the respective genes obtained from
different DNA samples or closely related taxa in the combined data set. Full names,
authorities, sources, vouchers and database accessions are listed in Appendix
1.
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270
C.
BAYER
ETAL
DNA extraction
Leaf tissue, flowers or seeds from fresh or silica gel dried material, or leaf fragments
from herbarium specimens were used. Total genomic DNA was extracted using a
modified
2
x
CTAB method (based on Doyle
&
Doyle, 1987). Since we had difficulties
obtaining DNA even from fresh material, DNA precipitation with ethanol or
isopropanol was generally extended to about one month
at
-20°C (Fay
et
al.,
1998a). Due to the mucilage content of many samples, it was sometimes difficult
to
remove the mucilaginous supernatant after centrifugation without losing most of the
DNA. DNA was purified by ultracentrifugation on a CsC12-ethidium bromide density
gradient (1.55 g/ml) followed by dialysis. Subsequently, total DNA samples were
purified using QIAquick silica columns (Qiagen, Ltd., Crawley, U.K.) according to
the manufacturer’s protocols. We took this additional step because amplification of
atpB was generally more difficult than amplification of rbcL, which succeeded without
problems from the same total DNA samples. Following purification on QIAquick
columns, success with atpB was much more consistent; we suspect that phenolic
compounds, which are known to be inhibitors of DNA polymerases, are present,
but why such differential effects should occur is not clear.
For a few samples, especially some of those extracted from herbarium material,
the usual protocol including precipitation, gradient centrifugation and dialysis was
replaced by using QIAquick columns to purifjr the raw extract directly, after
treatment with chloroform/isoamyl alcohol (24:
1)
to remove proteins
(J.
Ronnholm,
University of Uppsala, pers. comm.). Again, due to the high mucilage content of
some samples, prolonged and repeated centrifugation of the columns was required.
Ampl$ication and sequencing
ofatpB
and
rbcL
PCR amplification of r6cL was generally performed in
two
overlapping segments,
using synthetic primers that anneal at base positions
1
and 636 (forward), and 724
(reverse) and
a
downstream ribosome control site (Olmstead
et
al.,
1992; Fay
et
al.,
1998a). In contrast, atpB was usually amplified in a single piece from position
2
(forward) to 1494 (reverse). The internal primers start at position 61
1
(forward) and
766 (reverse), respectively (Hoot
et
al.,
1995). Bovine serum albumin (1-4
O/o
of 0.4
YO
aqueous solution; Savolainen
et
al.,
1995) was added to all PCR reactions to bind
phenolic compounds. PCR products were purified using Wizard minicolumns
(Promega U.K., Ltd., Southampton, U.K.) according to the manufacturer’s protocol.
Modified dideoxy cycle sequencing with dye terminators was used to produce the
new sequences presented here (Perkin-Elmer Applied Biosystems, Inc., Warrington).
In most cases, the total reaction volume suggested by the manufacturer
(20
pl)
was
reduced
to
5 p1. Diluting the reaction products with 15 p1 water prior to precipitation
and cleaning considerably improved the quality of the first part of each sequence
by eliminating most or all of the unincorporated dye terminators. Products for both
strands were sequenced directly on an automated sequencer (ABI 377, Perkin-Elmer
Applied Biosystems, Inc.) following the manufacturer’s instructions. Individual strands
were edited and assembled using Sequence Navigator and Auto Assembler (Perkin-
Elmer Applied Biosystems, Inc.).
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MOLECULAR SYSTEMATICS
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MALVALES
27
I
Data
anabsis
For each of the three matrices
(rbcL,
atpB and combined) under equal weights
(Fitch parsimony; Fitch, 197 l), we performed 1000 replicates of random taxon-
addition with TBR (tree bisection-reconnection) branch swapping, which is the most
thorough swapping algorithm of PAUP 3.1.1 (Swofford, 1993). In these replicates,
we limited the number of trees being held at each step to ten
so
that excessive
amounts of time were not spent swapping on suboptimal island, but this method of
search could not find
all
most parsimonious trees or detect islands of equally
parsimonious trees (Maddison, 1991). We therefore used all trees collected in the
1000 replicates as starting trees for a more complete search with a tree limit of
5000. We limited this search for
r6cL
and atpB due
to
computer memory limitations,
and thus we could not determine how many trees
in
total existed at the shortest
tree-lengths found. Using five single
trees
found in separate replicates as starting
trees, we were able to find all 5000 trees, thus indicating that islands were not
present.
Following these searches under the Fitch criterion, we performed successive
approximations weighting
(SW,
Farris, 1969) to reduce or eliminate the effects of
positions that change frequently. In most cases, the effect of
SW
is
to
reduce tree
number, but not always (Fay
et
al.,
199813). Using all trees found in the Fitch search
(above), we reweighted characters using the menu command in PAUP 3.1.1 with
the following settings: a base weight of 1000 and best fit for each character based
on the rescaled consistency index (RC). Using the consistency
(CI)
or the retention
index
(RI)
has no effect on the topologies produced with these matrices. Rounds of
search followed by re-weighting were performed until branch lengths were the same
in
two
consecutive searches. Each round consisted of ten replicates of random taxon-
addition with TBR swapping and a tree limit of 50 trees.
All
trees were then
swapped on to completion (up to
5000
trees) before preceeding
to
the next round
of
SW. Trees favoured by SW are never radically different from those found by
Fitch analysis (equal weights), and this is the case here (Table
1).
Internal support was evaluated with the bootstrap (Felsenstein, 1985). Use of
extensive swapping makes this process very slow,
so
we made use of
a
modified
procedure that is much faster but not much less accurate. We performed 5000
replicates of bootstrapping with nearest-neighbour interchange
("I)
swapping, but
permitting only ten trees to be held per replicate. The greatest effect here results
from group presence in the starting trees (which are the result of quick distance
calculations), but we have found that some minimal amount of swapping improves
the estimates for larger clades (which are under-estimated when only 'no swapping'
is employed). We have compared, on smaller matrices, the effects of such minimal
swapping on bootstrap percentages with those found with extensive TBR swapping,
and they are highly correlated. Thorough bootstrapping with TBR and no tree limit
is not practical for such large matrices because
it
would require several months of
analysis. If there is any effect from this faster method, it would only be an
underestimate rather than an exaggeration of support. Patterns of sequence evolution
were estimated using MacClade (Maddison
&
Maddison, 1992) from matrices
stripped to only the base positions included in the analyses. Because we believe that
the SW combined tree is the most accurate (due to higher overall levels of bootstrap
support), we assessed the evolution
of
each gene on this tree rather than on the
trees produced in the separate
rbcL
and atpB analyses.
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272 C. BAYER
ET
AL.
TABLE
I. Statistical values from our analysis
of
rhcL
and
atpB
gene sequences (CI: consistency index,
RI: retention index)
rbcL
Invariant sites 946 (67.62%)
Uniquely variable sites 144 (10.29%)
Informative sites 309 (22.09%)
Transitions 930
CI
0.42
RI 0.71
Transversions 684
CI 0.38
RI 0.57
Transition/transversion ratio 1.36
Number
of
equally parsimonious Fitch trees >5000
Fitch tree length 1619
CI
0.40
RI 0.66
Number
of
SW trees 1509
SW
tree length 434569
CI 0.72
RI 0.85
Fitch length
of
SW tree 1626
CI
0.40
RI
0.66
Steps, first position
(%
assessed on the combined tree) 375
CI
0.31
RI 0.54
Steps, second position
(%
assessed on the combined tree)
161
(9.98%)
CI
0.40
RI 0.57
Steps, third position
(%
assessed on the combined tree) 1078 (66.79%)
CI 0.43
RI 0.68
atpB
914 (63.69%)
209 (14.56%)
312 (21.74%)
1002
0.41
0.73
454
0.58
0.64
2.21
>5000
1435
0.50
0.69
>5000
492134
0.77
0.84
1438
0.50
0.69
(23.23%)
0.51
0.60
139 (9.55%)
0.59
0.52
1068 (73.35%)
0.47
0.71
combined
>5000
3066
0.44
0.66
81
912505
0.75
0.84
3070
0.44
0.66
249 (17.10%)
To
calculate the number
of
transitions and transversions observed on one
of
the
shortest combined
SW
trees
(as
well as their Cls and Rls), we used the following
step matrix to calculate the number
of
transversions at each base position:
A
c
G
T
A
1
0
1
c
1
0
G
0
1
T
1
0
1
From this number
of
transversions and their collective
CI
and RI,
we
could calculate
those
of
transitions.
RESULTS
Ana[ysis
of
rbcL
Due to the position
of
the forward
PCR
primer, we deleted the first 29 bases
of
the total 1428 bases from
our
rbcL
matrix and used 1399 characters,
of
which 453
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MOLECULAR
SYSTEMATICS
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273
A20,
I
12
j
10
v1
8
6
4
2
0
200 400
600
800
1000 1200
Site
16nn
12 14tt
10
U
I
II
atpB
I
0
200 400
600
800
Site
1000 1200
Figure
1.
Number and distribution
of
base changes in
(A)
rbcL
and
(B)
atpB
(produced by MacClade;
Maddison
&
Maddison,
1992).
These are optimized substitutions on one
of
the
81
combined
SW
trees.
were variable and 309 were potentially informative. Heuristic search under the Fitch
criterion yielded more than 5000 equally parsimonious trees of 1619 steps with a
CI of 0.40 and a RI of 0.66. Successive weighting produced 1509 trees of 434569
steps (CI 0.72, RI 0.85), which corresponds to a Fitch length of 1626 steps (CI
0.40,
RI
0.66; trees not shown). Changes in
rbcL
are not particularly clustered; the
abundance and distribution
of
substitutions are shown
in
Figure 1A. The transition/
transversion ratio was 930/684 (1.36). Although more numerous, transitions had
both a higher consistency index (CI) and retention index
(RI)
than transversions
(0.42 versus 0.38 and 0.71 versus 0.57, respectively; Table
1).
Third positions
contributed the most steps (66.79
O/o
as assessed
on
the combined tree) and had the
highest CI and RI, whereas the CI and
RI
of the first positions were lowest (Table
Malvales
s.1.
form
a
clade in
all
most parsimonious Fitch trees found, but their
monophyly is not supported by the bootstrap. There
is
strong support for core
Malvales (bootstrap values: 99
'/o
with Fitch weights, 100
O/O
with
SW),
Muntingiaceae
(97/96), Thymelaeaceae (including
Aquiluria
and
Gonysplus;
97/99) and a clade
1).
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274
C.
BAYER
ETA.
including Cistaceae, Dipterocarpaceae and Sarcolaenaceae (99/ 100).
Bixa
is
sister
to
Diegodendron
(96/97), but their sister-group relationship with Cochlospermaceae is
only weakly supported (73/85). Within core Malvales, only
a
few clades are well
supported, such as the
Dombya
alliance
(Dombya, Helmiopsiella, Eriolaena, Ruizia,
Trochetiopsis
and
Paramelhania;
loo/ loo),
Brownlowia
and
Pentace
(1
00/
loo),
Gossypium
and
nespesia
(90/93),
Hibiscus
and
Pavonia
(loo/
loo),
Helicteres
and
Triplochiton
(8
1
/
92) and
llornasia
and
Lasiopetalum
(96/ 100).
?ilia
is sister
to
all other core Malvales,
but this position is not supported by the bootstrap. There
is
some support for a
clade including
G'rewia, Colona, Microcos
and
Goethalsia,
if SW
is
applied
(-/88).
The
byttnerioid alliance (see discussion) is neither resolved nor supported.
Anahsis
ofatpB
The beginning and the end of each sequence were not reliable due
to
the
annealing positions of the PCR primers,
so
we cut the first 34 and the last 28 bases
of
the total 1497. We thus used 1435 base pairs of atpB in the analysis, of which
52
1
were variable and
3
12 were potentially informative. A single six-base deletion
was detected in the
atpB
gene of
Spamannia,
corresponding
to
AGATAG starting
at
position 156 in the
Niotiana
reference sequence (GenBank accession X6 13 19).
Insertions in the atpB sequence as compared to the
Nicotiana
reference sequence
were found in the following taxa: CTTAG starting at position 1472 in
Heliocarpus,
TAGAA starting at position 1474 in
Lavatera,
GGA starting at position 1098 in
Aquilaria.
All these were deleted from the PAUP matrix because they were all unique
to single taxa. Heuristic search under the Fitch criterion yielded more than 5000
equally parsimonious trees
of
1435 steps (CI 0.50, RI 0.69). Successive weighting
produced more than
5000
trees of 492 134 steps (CI 0.77,
RI
0.84), which corresponds
to
a
Fitch length of 1438 steps (CI 0.50,
RI
0.69; trees not shown). The abundance
and distribution of base changes are shown in Figure 1B. The transition/transversion
ratio was 1002/454 (2.21). As with
rbcL,
transitions were more numerous; their CI
was lower than those for transversions, but the RI was higher (Table
1).
Third
positions contributed the most steps (73.35
O/O
as assessed on the combined tree) and
had the lowest CI and the highest RI, whereas the second positions had the highest
CI and the lowest RI (Table
1).
Malvales
s.L.
are supported by
atpB
data (bootstrap values: 84
%
with Fitch weights,
95
O/o
with
SW).
Well supported clades within Malvales
s.L.
include Muntingiaceae
(96/96), Thymelaeaceae (including
Aquilaria
and
Gonysglus;
98/ loo), Cistaceae,
Dipterocarpaceae and Sarcolaenaceae (99/ 100) and
Bixa
with
Diegodendron
(90/97).
The sister-group relationship between
Neurada
and the remaining Malvales
is
not
supported (452). There is no support for the monophyly of
core
Malvales
(-/53).
Within core Malvales (68/53), the
Dombya
alliance (as mentioned for the
rbcL
analyses but without
Helmiopsiella,
for which
atpB
was not available) is well supported
(loo/ 100). Its sister-group relationship with a clade comprising
Pterospemzum, Schoutenia
and
Burretiodendron
(78/83) is also supported by the bootstrap (62193). Other clades
include
Abroma
and
Byttmria
(81
/88),
Lasiopetulum
and
lhomasia
(80/77)
and
Pavonia
and
Hibiscus
(60/87). Malvaceae
(Gossypium, Hibiscus, Pavonia
and
Lavatera)
are only
very weakly supported (-/69). There is some support for an enlarged
Grewia
alliance
(as above for
rbcL
plus
Apeiba, Sparrmannia
and
HeLiocarpus;
63/8
1).
The sterculioid
genera
(Sterculia, Hildegardia,
Cola)
form a weakly supported clade (53/69). The
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MOLECUIAR
SYSTEMATICS
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275
brownlowioid alliance
(Christiana,
Benya,
Brownlowia
and
Pentace)
is even more weakly
supported (-/58). The clade formed by
Christiana
and
Benya
has slightly stronger
support (56/
78).
Combined analysis
The combined matrix under the Fitch criterion yielded more than 5000 equally
parsimonious trees of 3066 steps (CI 0.44, RI 0.66), the strict consensus tree of
which (for core Malvales) is shown in Figure
2.
Successive weighting of the combined
data set produced 81 trees
of
912505 steps (CI 0.77, RI 0.84), which corresponds
to
3070 Fitch steps (CI 0.44,
RI
0.66).
A
randomly selected tree (of the 81
SW
trees)
is
shown in Figure 3 (Malvales
s.L.,
Sapindales, Capparales) and Figure 4 (core
Malvales). Branch lengths are shown above the branches (ACCTRAN optimization),
bootstrap values (equal/SW) are indicated below the branches
(to
save space in
Figures 3 and 4, we indicated only 99 if support was 99 or
100°/o;
if values for both
Fitch and
SW
were 99 or loo%, we indicated a single 99). Branches not present in
the
SW
strict consensus tree are marked with arrows. Expanded Malvales (68/58)
comprise core Malvales (Malvaceae
s.L.,
see below; 99/100), which are the sister
group to the bixalean clade (Bixaceae, Diegodendraceae, Cochlospermaceae; 85/
8
l), and these in turn are sister to a larger clade in which Thymelaeaceae (including
Gonys~lus
and
Aquilaria;
loo/
100) and Sphaerosepalaceae together are the sister
group to the cistalean clade (Cistaceae, Dipterocarpaceae, Sarcolaenaceae and
Neuradaceae). The outlier to this whole assemblage is a clade comprised of
Muntingiaceae and
Petenaea.
However, the interrelationships between the clades
mentioned, as well as the sister-group relationships between Sphaerosepalaceae/
Thymelaeaceae (-/70) and Neuradaceae and the cistalean clade (-/67), are either
unsupported or only weakly supported. The positions of Muntingiaceae and
Petenaea
are especially unstable.
Core Malvales (Malvaceae
s.1.
in Fig. 3) are strongly supported by our data.
HibzScus, Pavonia, Gossypium,
and
Luvatera,
which represent Malvaceae
S.S.
in the
combined analysis, form the only monophyletic clade (56/83) that corresponds
to
a traditionally circumscribed family (Figs 2, 4). None of other core Malvales families
is
indicated to be monophyletic: Bombacaceae are unresolved but are paraphyletic
with respect to Malvaceae, and those alliances
or
single genera usually classified
as
Tiliaceae or Sterculiaceae are interwoven (Fig.
2).
This
is
also evident from the
separate analyses of both apB and
rbcL
sequences (not shown), which yield similar
topologies
but
are generally more weakly supported. Since the commonly applied
family names are not suitable to describe most of the clades shown in Figure 4, we
refer here to the alliances and their names
as
outlined in the discussion: Bombacoideae
(without
Pentaplaris,
not supported by the bootstrap); Dombeyoideae (72/96); Ster-
culioideae (-/69); Brownlowioideae (93/94), sister to
Mortoniodendmn
(50/74); Hel-
icteroideae (74/9
l),
sister
to
Durio
(55/56); Grewioideae (70/78); and Byttnerioideae
(not supported) including
Hemzannia
with
"3eobroma
(not supported), Lasiopetaleae
(55/64) and
Abroma
with
Byttneria
(86/96). Malvoideae, Bombacoideae, Dom-
beyoideae, Sterculioideae, Brownlowioideae, Helicteroideae and
72ia
form a clade
(74/94), in which
7ilia
is
sister to the remaining
taxa
(-/57). Most other sister-group
relationships among the clades mentioned as well as those within Byttnerioideae
have no bootstrap support.
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276
C.
BAYER
ET
AL.
Gossypium
Thespesia
Lavatera
Hibiscus
Pavonia
Pentaplaris
Adansonia
Ochroma
Fremontodendron
Bombax
Matisia
Chorisia
Pachira
Dombeya
Helmiopsiella
Eriolaena
Paramelhania
Trochetiopsis
Ruizia
Burretiodendron
Pterospermum
Schoutenia
Sterculia
Hildegardia
Cola
Mortoniodendron
Christiana
Berry a
Pentace
Brownlowia
Helicteres
Triplochiton
Reevesia
Durio
Tilia
Keraudrenia
Thomasia
Lasiopetalum
Rulingia
Colona
Microcos
Goethalsia
Grewia
Heliocarpus
Apeiba
Sparrmannia
Hermannia
Theobroma
Abroma
Byttneria
Leptonychia
outgroups
]~~~-
:J
Tiliaceae
J
Bombacaceae
:J
Sterculiaceae
J
·-~-
J·~~·
:J
Tiliaceae
:J
Sterculiaceae
:J
Tiliaceae
J
Sterculiaceae
JTIJ-M
J
Sterculiaceae
:J
Bombacaceae
:J
Tiliaceae
J
""'"'""""''
Tiliaceae
Figure
2.
Core Mal vales in the strict consensus tree
of
more than 5000 equally parsimonious Fitch
trees (equal weight) obtained
by
heuristic search using the combined
rbcL
and
atpB
data set (no
atpB
data for
Helmiopsiella
and
7hespesia;
length 3066 steps,
CI
=
0.44, RI
=
0.66). Family affiliation
of
genera according
to
Brummitt
(1992).
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MOLECULAR
SYSTEMATICS
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MALVALES
Malvaceae
s.1.
7
Bixaceae
99
21
Diegodendron
3
Diegodendraceae
Cochlospermum
7
Cochlospermaceae
456
85/
81
22
-167
L
i:
99 42
Sarcolaena
Neurada
85
Helianthemum
99
39
mberaria
Koelreuteria
Rhus
Pistacia
Schinus
Reseda
99
44
73/65
56
35
99
Floerkea
Carica
72
19
86/
92 52
,
27
98/99
Petenaea
Dicraspidia
Cistaceae
1
2
7
Dipterocarpaceae
7
Sarcolaenaceae
3
Neuradaceae
7
Sphaerosepalaceae
1
"hymelaeaceae
1
7
incertae sedis
Muntingiaceae
3
Hippacastanaceae
7
Aceraceae
7
Sapindaceae
1
Anacardiaceae
I
7
Resedaceae
7
Capparaceae
Brassicaceae
7
Limnanthaceae
3
Caricaceae
3
nopaeolaceae
1
j.
Figure
3.
Malvales, Sapindales and Capparales in one of the
81
equally parsimonious trees selected
at random from heuristic search of the combined data set (no
atpB
data for
Petenma)
using successive
weighting
(SW
tree length 912505, CI
=
0.44,
RI
=
0.66; Fitch length
3070,
CI
=
0.44,
RI
=
0.66). Branch lengths are indicated above the branches (ACCTRAN optimization; note that the branch
length marked with an asterisk is not comparable
to
the others, since
atpB
data
is
lacking for
Peknaen),
numbers below the branches represent bootstrap values without/with
SW.
Bootstrap percentage of 99
or more is marked as 99; if both values are 99 or more, only a single 99 is given.
All
branches in this
portion of
the
strict consensus tree are resolved. Malvaceae
s.1.
(core Malvales) are shown in Figure
4.
DISCUSSION
Malvales
sensu lato
The content and relationships
of
Malvales
s.1.
have been discussed elsewhere (Fay
et
al.,
1998a, Bayer
et
al.,
1998, Alverson
et al.,
1998), but some differences between
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278
C.
BAYER
ET
AL.
29
Gossypium
Lavatera
Hibiscus
MALVOIDEAE
Pavonia
Pentaplaris
3
Adansonia
-/67
Chorisia
Pachira
BOMBACOIDEAE
Fremontodendron
Ochroma
Bombax
-1-
Matisia
13
Dombeya
1
-1-
Eriolaena
Paramelhania
Trochetiopsis
DOMBEYOIDEAE
Ruizia
Burretiodendron
Pterospermum
Schoutenia
-1-
Sterculia
5
Cola
STERCULIOIDEAE
2
Hildegardia
-1-
Mortoniodendron
(incertae sedis)
Christiana
Berry a
BROWNLOWIOIDEAE
Pentace
74/94
Brownlowia
Triplochiton
Helicteres
3
Reevesia
HELICTEROIDEAE
55/56
Durio
(incertae sedis)
31
Tilia
TIUOIDEAE
Colona
Microcos
-1-
Goethalsia
Grewia
GREWIOIDEAE
Heliocarpus
Apeiba
Sf!.arrmannia
33
Hermannia
99
-1-
Theobroma
3 6
Keraudrenia
-1-
Rulingia
55/64
Thomasia
BY'ITNERIOIDEAE
Lasiopetalum
14
Abroma
8
86/96 28
Byttneria
12
Leptonychia
(incertae sedis)
Figure
4.
Malvaceae
s.l.
(core Malvales) portion
of
the same single tree
as
in Fig.
3.
Branch lengths
are indicated above the branches (ACCTRAN optimization), numbers below the branches represent
bootstrap values without/with successive weighting. Bootstrap support
of
99
or
more
is
marked as 99;
if
both values are 99
or
more, only a single 99
is
given. Branches not present in the strict consensus
of
the
SW
trees are indicated by arrows; for the strict Fitch consensus tree, see Figure 2.
The
suprageneric names given
on
the right margin correspond to the preliminary classification proposed
here
(sec
text).
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MOLECULAR
SYSTEMATICS
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279
these and this study need to be addressed. Based on
rbcL
sequence data,
Rhopalocarpus
(Sphaerosepalaceae) falls either in the bixalean clade (Alverson
et
al.,
1998)
or
is
sister to Thymelaeaceae (Fay
et
al.,
1998a), although neither placement is well
supported. The latter placement
is
supported here in the combined data set, although
not strongly.
Neurada,
which agrees with many Malvales in the lysigenous mucilage
canals, exotegmic seed coat and cyclopropene acids in the seed
oil
(Huber, 1993),
is either sister to the cistalean clade (our Fig. 3; Fay
et
al.,
1998a; Alverson
et
ul.,
1998: fig.
2)
or represents the sister group of all other Malvales (Alverson
et
al.,
1998: fig. 3). Muntingiaceae belong to the cistalean clade according to rbcL analyses
(Fay
et
al.,
1998a; Alverson
et
al.,
1998), but in our combined analysis they are
(together with
Petenaea,
see below) sister to the remaining Malvales. However, this
topology is not supported by the bootstrap (Fig.
3).
These taxa require further
research to elucidate their relationships with confidence.
Petenaea,
which has not been included in previous phylogenetic studies, merits
special attention. The monotypic genus from southern Mexico, Guatemala and
Belize was originally placed in Elaeocarpaceae (Lundell, 1962). The suggestion that
Pei!enaeu
should be placed in Elaeocarpaceae was claimed to be supported by
anatomical studies, which also emphasized the differences between
Petenaea
and
Muntingia
(Kukachka, 1962; Gasson,
1
996).
Petenaea
is characterized by multicellular
simple or branched trichomes, palminerved, cordate leaves with minute stipules,
tetra- or pentamerous flowers without petals but with moniliform trichomes, re-
ceptacular glands that alternate with the stamina1 filaments, dorsifixed anthers that
open by apical slits, prolate and tricolporate pollen with microperforate tectum,
massive axile placentae with numerous ovules and baccate fruits (C. Bayer, pers.
obs.).
The structure of the ovary is especially reminiscent of Muntingiaceae, which
are close to
Petenaea
according to our results (Fig. 3). Even though this position is
not supported by the bootstrap it seems to be the least inconvenient option to treat
Petenaea
as tentatively related to Muntingiaceae.
Circumscription
of
core
Malvales
Core Malvales are well supported by our sequence data. The clade
is
usually
characterized by features such as palminerved leaves, stellate hairs, mucilage, layered
phloem with dilated rays, valvate calyces, and more or less numerous stamens.
However, these characters are not rare outside core Malvales. The few known
morphological apomorphies for Malvales
S.S.
include occurrence of a unique repeating
unit within the inflorescences (bicolor unit: Bayer, 1999), trichomatous floral nectaries
localized mainly on the adaxial side of the perianth (Knuth, 1898, 1904; Brown,
1938; Frei, 1955; Vogel, 1977) and perhaps a valvate calyx, even if this feature is
not rare outside Malvales
s.1.
The occurrence of tile cells (Chattaway, 1933;
Manchester
&
Miller, 1978) is restricted to core Malvales (and
Kaminskia,
Rham-
naceae; Schirarend, pers. comm.) but is known only from relatively few genera.
Contrary to widespread opinion (e.g. Cronquist, 1981; Judd
&
Manchester, 1997),
the occurrence of cyclopropenyl fatty acids is not restricted to core Malvales: positive
Halphen reaction and/or the detection of (dihydro-) malvalic or (dihydro-) sterculic
acids have been reported for Sarcolaenaceae and Thymelaeaceae and also for some
remote families such as Boraginaceae, Elaeocarpaceae, Leguminosae, Rhamnaceae,
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280
C.
BAYER
E’TAL.
and Sapotaceae (and even for
Gnetum;
Vickery, 1980, 198
1
;
Gaydou
&
Ramanoelina,
1983; Hosamani, 1994, 1995).
Subdiuision
of
core Malvales
As
evident from our results (Figs
2,
4) there is strong support for the polyphyly
of Tiliaceae and Sterculiaceae and no evidence for the subdivision of core Malvales
into the four traditional families Sterculiaceae, Tiliaceae, Bombacaceae and Mal-
vaceae, only the last of which is monophyletic. Other clades of the consensus tree
also correspond to previously recognized alliances, which however are usually ranked
below the family level. Even if some of them are not supported by the bootstrap or
found in the consensus tree (Figs
2,
4),
most of them can be circumscribed by
morphological characters and roughly correspond to some of the traditionally
accepted suprageneric taxa. These clades are here considered as subfamilies of a
single family Malvaceae that is expanded to comprise all core Malvales. The name
Malvaceae Juss. (1789: 271)
is
preferred over Tiliaceae
Juss.
(1789: 289) because
the former has already been used in a similar broader sense by earlier botanists
(e.g. Jussieu, 1789; Baillon, 1873; van Tieghem, 1884; for comments see Masters,
1869; Schumann, 1895; Judd, Sanders
&
Donoghue, 1994; Judd
&
Manchester,
1997).
Certainly, there will be some objections to the fusion of the established families
Tiliaceae, Sterculiaceae, Bombacaceae, and Malvaceae. However, in view of our
data and others (Judd
&
Manchester, 1997), there seems to be
no
advantage to
the maintenance of the traditionally accepted families by simply changing their
circumscriptions. For instance, representatives of former Tiliaceae are scattered
among Sterculiaceae. To achieve a more natural delimitation of Tiliaceae, all
‘tiliaceous’ genera except Grewioideae (the largest clade
of
Tiliaceae, see below)
would have to be transferred to Sterculiaceae. Since
7ilia
would also have to be
removed, the remaining genera would have to be named Grewiaceae, not Tiliaceae.
Based
on
molecular as well as on morphological data it
is,
therefore, not possible
to maintain both Sterculiaceae and Tiliaceae in their broader delimitation. If, in
turn, Tiliaceae were expanded to include Sterculiaceae, and Bombacaceae were
sunk into Malvaceae, then the
two
remaining core families of Malvales would be
difficult
to
delimit by morphological characters, and the dombeyoid group especially
would occupy an intermediate position. In addition to the fact that Tiliaceae (incl.
Sterculiaceae) would be paraphyletic with respect to Malvaceae (incl. Bombacaceae),
there
is
no
molecular evidence in favour of a deep split between these
two
families.
If
it
is admitted that neither a subdivision of core Malvales into four families nor
an expansion of both Tiliaceae and Malvaceae are supported by available data,
then two possibilities remain: the clades found in our trees can be treated either
as
separate families or as infrafmilial taxa of a single family, Malvaceae. To us
it
would seem inappropriate to rank these clades as families, some of which would
have to be formally described as new. It is true that there are
no
objective criteria
or
formal obstacles against treating the clades within core Malvales as families, but
for practical reason we feel that any increase in the number of small families should
be generally avoided if possible. Furthermore, the morphological differences as well
as the plastid gene sequence divergence within Malvaceae
s.1.
are not larger than
in other families. The monophyly of Malvaceae
s.1.
is
well established, whereas the
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MOLECULAR
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28
I
suprageneric taxonomy within this group obviously requires far more research. For
now, ambiguously placed genera can simply be treated as taxa incertae sedis within
Malvaceae, whereas splitting core Malvales into numerous smaller families would
leave these genera without clear family affiliation, which is also impractical and
undesirable.
The emerging suprageneric alliances are treated here as subfamilies, which has
the advantage that some of the former tribes (especially those within former
Malvaceae) may be maintained in their commonly used sense, even if certain changes
in their circumscription may be necessary. In view of the tentative character of the
classification proposed here it seems favourable to use only names that are already
available, which is true for all subfamilies listed below. Previous classifications made
little use of the subfamily rank,
so
this category allows
us
to circumscribe the major
lineages within core Malvales without changing the commonly used names any
more than is required. This is desirable since the circumscriptions of these entities
have to be drastically narrowed (e.g. Tilioideae) or broadened (e.g. Dombeyoideae)
to achieve presumably natural groups with roughly comparable ranges of variation.
Except for Malvoideae, Bombacoideae, and Durioneae, for which only a few
representatives are listed, the taxonomic position of every genus according to some
previous classifications (Jussieu,
1
789; Baillon, 1873; Schumann, 1895; Hutchinson,
1967) as well as our circumscriptions here are given in Appendix
2.
The placement
of those genera, which are not included in
our
molecular analyses, is based on
morphological characters (C. Bayer, unpubl.). Distinctive characters of the sub-
families, some of which are likely to be synapomorphies, are mentioned in the
following paragraphs and summarized in Table
2.
Byttnerioideae Burnett
Byttnerioideae include genera that represent tribes Byttnerieae, Lasiopetaleae,
Theobromeae and Hermannieae (see below). Byttnerioideae can be circumscribed
by their peculiar cucullate (‘hooded’) petals (Schumann, 1886; Leinfellner, 1960).
However, this character is absent from Hermannieae, which might be interpreted
as the result of
a
secondary transformation within Byttnerioideae. As far as our
molecular data are concerned, this clade represents the most problematic alliance
within core Malvales. The assumption that Byttnerioideae are monophyletic
is
neither supported nor strongly rejected by our molecular data: Byttnerioideae appear
to be paraphyletic with respect to Grewioideae
in
all most-parsimonious trees (both
Fitch and
SW),
but this topology is not supported by the bootstrap. Although Figure
4
indicates that Grewioideae are monophyletic but embedded within Byttnerioideae,
we suspect a sister-group relationship between them. This relationship
is
only
two
steps less parsimonious with these data (as determined with MacClade and a
constraint experiment in PAUP). In view of the morphological differences between
these entities, we treat them as separate subfamilies. Of the tribes mentioned above,
only Lasiopetaleae are supported. Based on morphological characters, Byttnerioideae
could be subdivided into the four tribes discussed below. Although the combined
rbcL/atpB matrix does not identift the first two, it does not strongly refute their
existence. The topology that we obtained lacks
a
clear pattern because of the only
modest level of divergence. Hence, we suspect that with more information these
four clades will emerge. Although we presently lack evidence for these tribes’
monophyly, use of the names is not precluded and serves a useful exploratory
purpose.
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tG
cc
tG
TASLE
2.
Summary characteristics of the subfamilies of Malvaceae
s.1.
as recognized in
our
treatment; most distinctive characters
or
potential apornorphies
underlined (for sources see text)
Subfamily Inflorescences
Byttnerioideae flowers in many- to 3(-2)-
flowered bicolor units, more
rarely solitary with epicalyx
(many Lasiopetaleae), often
in sympdi
3-flowered (epicalyx e.g.
in
Luehea)
anthocladia,
condensed sympodia, or
panicles, sometimes terminal
Grewioideae bicolor units usually many-to
Tdioideae bicolor units usually many-flowered,
axillary,
axis
with
wing-like bract
(Xlia)
Helicteroideae bicolor units sometimes
reduced to flower pairs with
4
bracts, sometimes
arranged in anthocladia;
rarely panicles of flowers
with
or
without epicalyx
in many-flowered bicolor
units
Brownlowioideae probably at least sometimes
Sterculioideae
mostb
panuuhk,
axillary,
rarely condensed and
cauliflorous;
epicaJvx
absent
Flowers Pollen other features
~~ ~
pclals
curullate
(except Hermannieae)
to
reduced; stamens epipetalous, fused
to clusters
or
solitary;
episepalous
staminodia present or reduced;
ovary
5-1-locular
ncctarics,
ifpresent,
mostJv
on
petalr
or
andmgynophore;
stamens
ariringfmrn
altmipelolotu primalia
orjimn
nngwall
primonfia, distinct,
numerous,
some occasionally
sterile,
but not
resembling byttnerioid staminodia
stam
nmtu,
distinct
their
primordia and
(if
present)
staminodia
epipefulous
sometimes zygomorphic; often
gamosepalous;
petals
ojkn
wiul
laieral
conslrittions;
andmgynophore
usually
present;
staminodio
present; sometimes
apocarpous
gamosepalous; sometimes apetalous
and/or unisexual;
sfnmorr
nwnemtu,
fie,
thecue
dimgent
at
base
and
touching
each
0.h
on
lop
oj
connectiw
often apocarpous
gamosepalous;
apelalour;
usual&
unisexual;
andmgynophore
present,
staminodia
absent;
apocatpotu
usually 3-colporate to
pororate, sometimes
operculate; reticulate to
perforate or
occasionally spinulous
pmk,
3-colporate;
usually micro-perforate,
often with
suprategillary reticulum
+
oblate; (brevi-)
colporate, finely
reticulate
+
oblate; 3
(-5)-
angdapermrate;
brevicolpate, sometimes
with vemcae or tiny
spinules
5
oblate;
breviaperturate; often
finely reticulate
spheroidal to prolate;
tricolporate;
suprategillary reticulate,
often micro-perforate
pantropical; mostly
small trees or shrubs
pantropical, trees,
shrubs, rarely herbs
n
2
trees; northern
hemisphere, mainly
from temperate
sometimes with
extrafloral nectary on
inflorescence
ramifications
m
ia
regions
b
predominantly
palaeotropical, trees,
rarely large shrubs;
occasionally lepidote
pantropical, trees;
leaves sometimes
digitate or uniforliolate;
fruits follicles or nuts
continued
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TABLE
2.
continued
Subfamily Inflorescences Flowers Pollen
Dombeyoideae
Jowm
axilhty
on
open
stamens in bundles usually separated by suboblate to spheroidal;
shoo&,
often solitary
or
in staminodia, sometimes numerous, often 3-porate,
few-flowered cymes; free
or
forming a tube occasionally
epicalyx usually present polyaperturate;
spinose
Bombacoideae flowers solitary
dary
or
variously arranged, rarely
paniculate; sometimes in
anthocladia; epicalyx present
Malvoideae flowers usually with
epicalyx, in axillary
condensed sympodia or
solitary, rarely in anthocladia
gamosepalous, stamens (sometimes
very) numerous, filaments more or less
fused, sometimes forming phalanges
or
tubes,
anthers di-, tetra-,
or
polysporangiate
gamosepalous,
stam
+_
numerous,
forming
a
tube,
anthers always
dirporangiate,
number of carpels often
increased
spheroidal to oblate;
usually 3-(col)porate;
often reticulate, rarely
spinulose
often large and more
or
less spheroidal, 3- to
polyaperturate, mostly
spinose
other features
3
0
F
m
n
mainly Madagascar
and Pacific islands;
mostly shrubs or
sometimes winge,ed;
cobledom
unralb
F
3
bjfid
2
mainly tropical
5
America and Africa;
=!
tall to small trees;
v,
leaves
o@
d@ta&
0
often
chiropterophilous
5
r
cosmopolitan,
<
temperate to tropical;
F
herbs
or
shrubs, rarely
trees, fruits rarely
capsular
or
baccate
herbs; seeds
P
n
1
1\3
P
w
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284
C.
BAYER
ETAL.
(
1)
Byttnerieae
(Byttneria, Ayenia, Ryhya
and
Megatritheca)
obviously represent a
natural entity. The flowers of Byttnerieae are characterized by a whorl of single
antepetalous stamens and, more specifically, their peculiar clawed petals, which
Leinfellner
(1
960) regarded as the most complicated in the angiosperms (Cristobal,
1960, 1976).
Abroma,
which is sister to
Byttneria
according to our analysis, has cucullate
petals with a much broader base, and the stamens are not solitary but in bundles.
Judging from these characters, which are typical of Theobromeae (see below), it is
not clear why
Abroma
should be more closely related to
Byttneria
than to
%obroma,
as our cladograms indicate.
(2)
Theobromeae include
Theobroma, Herrania, Guazuma, Abroma, Scaphopetalum,
Kleinhouia
and
Leptonychia.
These genera share petals with a broadly based cucullus.
The distal petal appendix is laminar in
Abroma, Guazuma, Herrania
and most
Theobroma
species but
is
lacking in
Scaphopetalum, Leptonychia
and
Theobroma
sect.
Zlmatocarpus
(Cuatrecasas, 1964). The androecium includes staminodia, which are usually con-
spicuous, and alternisepalous bundles of two or more stamens that are produced
through secondary increase
of
primordia (e.g. Payer, 1857; Baillon, 186
1
/
1862,
1870; van Heel, 1966; Bayer
&
Hoppe, 1990). It is quite obvious that the neotropical
genera
Herrania
and
Guazuma
are closely related
to
Theobroma.
The palaeotropical
genera
Abmma
and
Scaphopetalum,
and possibly also
Leptonychia,
appear to
fit
well into
this alliance, even
if
Corner
(1
976) regarded the
last
as a misfit within Sterculiaceae.
Nevertheless, there
is
no molecular support for a placement
of
Abroma
and
Leptonychia
within Theobromeae and especially the position of
Leptonychia
(here treated as
incertae sedis) remains unclear.
(3)
Lasiopetaleae include a well delimited core group that is confined to Australia
and comprises
Thomasia, Hannafardia, Lysiosepalum, Lusiopetalum
and
Guichenotia.
Their
flowers are mostly arranged in bracteose monochasia and have an epicalyx (Classen,
1988; Bayer
&
Kubitzki, 1996). Further characters are the reduced or absent petals
and staminodia, the occurrence
of
anthers opening with short slits or pores, often
less than five carpels, tubular stigmas and adaptions
to
myrmecochory (Gay,
182
1
;
Schumann, 1886; Jenny, 1985). In addition to this core group, Lasiopetaleae are
generally considered to include genera such as
Kiraudrenia
and
Smkgia.
However, the
separation
of
such a broadly circumscribed Lasiopetaleae from other Byttnerioideae
has always been somewhat arbitrary. There is a morphological continuum between
the flowers of Theobromeae and Lasiopetaleae, and some of the ‘intermediate’
genera here placed in Lasiopetaleae have previously been included in Theobromeae.
We cannot see any obvious reason to include the traditionally accepted
Kiraudrenia
and
Seringia
in Lasiopetaleae if the similar genera
Rulingia
and
Commersonia
are
excluded (Jenny, 1985; Bayer
&
Kubitzki, 1996). It is more likely that these four
genera are closely related to each other and belong to a slightly expanded tribe
Lasiopetaleae, which is represented by
hiopetalum, Thomasia, Rulingia
and
Keraudrenia
in our analysis (Fig.
4).
This clade is present but only weakly supported in all most
parsimonious trees produced by the combined matrix.
Lasiopetaleae extend from Australia to Madagascar and tropical Asia. Their
inflorescences are arranged in anthocladia, and the flowers have an epicalyx or are
united in many-flowered units, in which the first, sterile bract is displaced on the
main axis (Bayer
&
Kubitzki, 1996; C. Bayer, pers. obs.). Their relatively small
albeit cucullate petals link them with Theobromeae.
As
in Byttnerieae and in contrast
to Theobromeae, the androecium
of
Lasiopetaleae includes
only
five fertile stamens.
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MOLECULAR SYSTEMATICS
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MALVALES
285
(4)
Hermannieae
(Hermannia, Melochia, Dicarpidium
and
Waltheria)
are united by the
presence of five stamens and reduced or absent staminodia. Since we sampled only
a single species
of
this tribe, we can only speculate about its monophyly. Our data
indicate that Hermannieae are embedded within Byttnerioideae. Accordingly, one
could postulate the loss of the cucullate condition of the petals within this lineage.
In Hermannieae, flower pairs surrounded by four bracts prevail, and these are often
arranged in sympodia (Bayer, 1994). Pollen is usually spheroidal to prolate; spinulose
grains are restricted
to
the short-styled flowers of heterostylous
Waltheria
and
Melochia
species (Kohler, 1973; M. Jenny, pers. comm.). Anatomically, Hermannieae appear
to be homogeneous and similar to other Byttnerioideae (Dumont, 1887).
Grewioideae Hochr.
Grewioideae, which comprise Burret’s
(1
926) Sparmanniinae and Grewiinae plus
Tetraliceae, are strongly supported by our DNA data. If there is any consistency in
former Tiliaceae apart from Brownlowioideae, it
is
found in this subfamily, which
includes the vast majority of ‘tiliaceous’ genera, but not
Zlia
itself. Their floral
nectaries, if present, are located at the ventral base of the petals and rarely on
adjacent tissue such as the androgynophore. Staminodia equivalent to those of
Byttnerioideae are lacking. The fact that the stamens are free and indeterminate in
number, but usually more numerous than in most former Sterculiaceae, constitutes
the traditional character used
to
discriminate between Tiliaceae and Sterculiaceae.
These traits have also been cited as support for an alleged primitive position of
Tiliaceae (Edlin, 1935), even if
it
was known that the increased number of stamens
is due to a ‘dtdoublement’ and
is
therefore secondary (Ronse Decraene
&
Smets,
1993). Unlike other Malvaceae, stamens usually arise from alternipetalous primordia
or from
a
ringwall-shaped primordium (Payer, 1857; Celakovskjr, 1875; Hirmer,
1917; van Heel, 1966; Kortum, unpubl.;
C.
Bayer, pers. obs.). Two whorls of
androecial primordia are only rarely found
(Mollia:
W.
Kortum, unpubl.). Pollen of
Grewioideae is more or less prolate, its exine usually micro-perforate and often
bearing a suprategdlary reticulum.
It
appears to occur throughout the tribe; somewhat
similar, albeit finer sculptured, prolate grains are found in Lasiopetaleae (Erdtman,
1952; Sharma, 1969; Presting, Straka
&
Friedrich, 1983; M. Jenny, pen. comm.).
Tilioideae Arn.
Zlia
occupies an isolated position in our analaysis. Judged from morphological
and molecular data,
Zlia
appears
to
stand outside the clade comprising Malvoideae,
Bombacoideae, Dombeyoideae, Brownlowioideae, Sterculioideae, and Hel-
icteroideae. The remaining genera included in Hutchinson’s
(1
967) Tilieae
(Duboscia,
Muntingia, Brachypodandra, Schoutenia)
are only remotely related:
Schoutenia
is much
better placed in expanded Dombeyoideae rather than close to
Zliu,
as indicated by
molecular data as well as the presence of an epicalyx and spinose pollen.
Duboscia
and
Brachypodandra
were not included in this study; the former should be palced in
Grewioideae, and the latter is
a
synonym of
khca
(Dipterocarpaceae; Ashton, 1982).
Muntingia
is not a member of core Malvales and, with
Dicraspidia
and
Neotessmannia,
forms a distinct family, Muntingiaceae (Fig. 3; Bayer
et
al.,
1998).
Zliu
is by no means typical of what was formerly called Tiliaceae. In contrast
to
most genera of former Tiliaceae, the genus exhibits generalized malvalean characters,
such as the presence of sepal nectaries and alternisepalous androecial primordia.
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286
C.
BAYER
E7AL
The peculiar sympodial shoot and conspicuous wing-like bract of the inflorescence
(Hall
&
Swain, 1971; Manchester, 1994; Bayer, 1994) apparently represent
aut-
apomorphies. The high chromosome numbers of
i'ilia
(x=41; Fedorov, 1969) are
certainly an indication of polyploid origin, and it is likely that the genus represents
an early temperate offshoot of Malvaceae
s.L.
(for distribution of
i'ilia,
see Tang
&
Zhuge, 1996).
A
genus not included in our study that might prove to be sister to
i'ilia
is
Craigia
(Judd
&
Manchester, 1997). On the other hand, Zhuge (1989) suggested close
affinities between
Maxwellia
and
Craigia,
both of which he considered to be ster-
culiaceous. From a palynological comparison between
CrazgZa
and few other genera,
Long, He
&
Hsue (1985) concluded that
Craigia
agrees better with Sterculiaceae
than with Tiliaceae. In fact, the pollen of
Craigia
is tilioid, thus resembling the pollen
of
Mortoniodendron,
Brownlowioideae, certain Helicteroideae, Bombacoideae, and of
course
i'ilia
(Erdtman, 1952; Sharma, 1969; Nilsson
&
Robyns, 1986; Ying, Zhang
&
Boufford, 1993; M. Jenny, unpubl.). This character seems to be the decisive one
in
Judd
&
Manchester's (1997) assumption of a sister-group relationship between
i'ilia
and
Craigia.
Flower structure, however, might provide more specific characters in favour of a
relationship between
Craigia
and
i'ilia.
The flowers
of
Craigia
have been misinterpreted
as apetalous (Smith
&
Evans, 1921; Ying
et
al.,
1993), which might have led
Hutchinson (1967) to place the genus in Lasiopetaleae. Alternating with the sepals,
five clustered structures are found, in each of which four fused stamens are enclosed
by an outer and an inner organ. The outer organ
is
obviously homologous to the
petals of other Malvaceae. The inner one corresponds to a staminode that most
probably developed from the epipetalous androecial primordium, whereas the
episepalous sector remains empty. Therefore the inner staminodia do not correspond
to
the staminodia of other Malvaceae; those
of
both these taxa are from the inner
androecial whorl and arise from the episepalous sectors
(C.
Bayer
&
M. Jenny,
unpubl.). However,
a
similar arrangement with staminodia that represent the central
members of epipetalous androecial clusters are found in several
Zlia
species (Payer
1857; Schumann, 1890;
C.
Bayer, pers. obs.). In view
of
this rare character
Craigia
certainly merits further attention to clarify the sister-group relationships of
lilia.
Helicteroideae (Schott
&
Endl.) Meisn.
Helicteroideae are well supported by our data. They include the genera of
Helictereae
sensu
Hutchinson (1967) except for
Pterospennum,
which is here transferred
to Dombeyoideae, and
Heinhovia,
which is referrable to Byttnerioideae according to
ndhF
data (Alverson
et
al.,
in press). Within Helicteroideae,
Neoregnellia
is obviously
related to
Helicteres.
As
to
the other genera included in Helictereae by Hutchinson
(1967), the position of
Reevesia
in this clade is supported by our molecular data; our
sampling did not include
Unger;l.
In addition to the generally accepted Helictereae,
we also include
Tiplochiton
and
Mansonia. Tiplochiton
was described by Schumann
(1
900)
as representing a new family. The genus exhibits a peculiar combination of
characters of both Sterculioideae (secondary apocarpy, androgynophore) and many
cucullate Byttnerioideae (presence
of
petals and staminodia). These characters,
however, are met within Helicteroideae, into which
Tiplochiton
falls in our analyses.
Mansonia,
which has not been included in the molecular study,
is
morphologically
similar and probably closely related to
Tiplochiton
(see Prain, 1905; Mildbraed, 192
1
;
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MOLECULAR SYSTEMATICS
OF
MALVALES
287
Schulze-Motel, 1964; but also Emberger, 1960).
Mansonia
and
Helicteres
share the
occurrence of unique glands on the inflorescence ramifications (Fahn, 1979;
C.
Bayer, pers. obs.). Pollen of
Tiplochiton, Mansonia,
and the remaining Helicteroideae
is quite similar. The exine is often microperforate and occasionally spinulose
(Neorepllia, Helicteres, Tiplochiton:
Erdtman, 1952; M. Jenny, pers. comm.). The petals
of some Helicteroideae have been described as being cucullate (Schumann, 1886;
Leinfellner, 1960); they often exhibit lateral constrictions that are reminiscent of the
petals of the cucullate Byttnerioideae.
Durioneae
(Durio,
Neesziz, Coelostegia, Kostmnansia, Cullenia, Boschia),
which are gen-
erally considered
to
represent
a
tribe of Bombacaceae, appear to be related
to
Helictereae according to our data. They differ from Bombacoideae
(see
below) in
characters such as their pinnately nerved leaves, lepidote indumentum, more
or
less
fused epicalyx, distinctive muricate to spinose fruit, usually arillate seeds with thick
and flat cotyledons, special pollen type with mostly smooth microperforate exine,
considerably lower chromosome numbers
(n
=
14, di- or tetraploid), vegetative
anatomy, and exclusively Asian distribution (Dumont, 1887; Masters, 1875;
Bak-
huizen van den Brink, 1924; Nilsson
&
Robyns, 1986; Krutzsch, 1989; Baum
&
Oginuma, 1994). These differences indicate that this homogeneous alliance has been
generally misplaced in Bombacaceae. However, an inclusion in Helicteroideae is
neither unambiguously evident from these sequence data nor corroborated by
morphological characters. Therefore the systematic position of Durioneae remains
puzzling, and we consider them incertae sedis here.
Brownlowioideae Burret
Our molecular data strongly support Brownlowioideae
sensu
Burret
(1
926), who
remarked that it is
so
different from other Tiliaceae that it might even be raised
to
family rank. Its members are characterized by fused sepals and a special arrangement
of staminal thecae, which are divergent at the base and touching each other on the
top of the connective. Unlike Sterculioideae, which also possess fused sepals, the
pollen of Brownlowioideae corresponds to the Zlia-type (Erdtman, 1952; Sharma,
1969). Some Brownlowioideae are described as apocarpous or have at least free
carpels in fruit, which is also reminiscent of Sterculioideae. However, due to a lack
of suitable material for ontogenetic studies, it is not known whether true secondary
apocarpy exists in Brownlowioideae (Kubitzki, 1995).
The position of
Mortoniodendmn
within Brownlowioideae is only weakly supported
by the
SW
bootstrap. Based on morphology, there
is
no obvious justification for
including
Mortoniodendmn
in this clade. Neither the typical anthers nor the fused
calyx of Brownlowioideae are present, and the adate seed
is
as uncommon in this
group as in the remaining former Tiliaceae. Agreement with Brownlowioideae can
be found in the tilioid pollen (Erdtman, 1952; Graham, 1979), which is, however,
more coarsely reticulate (G. El-Ghazaly and K. Kubitzki, pers. obs.).
Sterculioideae Burnett
The clade representing Sterculioideae is weakly supported by the bootstrap
(SW
only) but is readily characterized by the usually unisexual and always apetalous,
apocarpous flowers with androgynophores. In addition
to
Hutchinson’s
(1
967)
Sterculieae, this subfamily also includes
Hildegardia
and
Heritiera
(Tarrietieae
sensu
Hutchinson, 1967). The remaining genera
of
Hutchinson’s (1967) Tarrietieae,
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288
C.
BAYER
ETAL.
Mansonia
and
T~filochiton,
differ in their hermaphrodite flowers with petals and
staminodia and the more or less oblate pollen with short apertures (Erdtman, 1952;
M. Jenny, pers. comm.) and are transferred here to Helicteroideae (see above). The
wood anatomy
of
Sterculioideae has been described as unique within Malvales and
treated as an apomorphy (Chattaway, 1932, 1937; Taylor, 1989). This alliance has
been considered as a primitive tribe or subfamily
of
Sterculiaceae (e.g. Brizicky,
1966). Nonetheless, apetaly, unisexuality of flowers and, less widely known, apocarpy
of Sterculioideae are secondary and by no means primitive (Endress, Jenny
&
Fallen,
1983; Jenny, 1985, 1988). These features, the presence of axillary paniculate
inflorescences, androgynophores, absence of staminodia and an epicalyx can be
regarded as advanced character states of this clade, although these traits also occur
scattered in other taxa. This
also
indicates that secondary apocarpy evolved at least
twice within core Malvales.
Dombeyoideae Beilschm.
Dombeyoideae are strongly supported by our molecular data (both with Fitch
and
SW).
Most genera of the subfamily belong to a monophyletic core group
that corresponds to Hutchinson’s
(1
967) Dombeyeae with addition of
Eriolaena,
Helmiopsiella,
and obviously also
Helmiopsis
and
Corchompsis
(no molecular data). This
alliance is morphologically homogeneous and unambiguously supported by the
bootstrap. They also resemble Malvoideae in certain respects
(de
Candolle, 1823;
Erdtman, 1952; Heslop-Harrison
&
Shivanna, 1977; Jenny, 1985, 1988; Barnett,
1987,
1988; Bayer, 1994).
The core group
of
Dombeyoideae as outlined above is centred in Madagascar
and Pacific islands, extending to Africa (some
Dombya
and
Melhania
species and
Hurmsia
incl.
Aethiocurpa),
St. Helena
(Tochetiopsis),
SE Asia (Cronk, 1990).
As
indicated
by our data, there are
at
least there more Asian genera that share palynological
and inflorescence characters with Dombeyoideae and should be included in this
subfamily.
Plemspermum,
which was misplaced in Helictereae (Dumont, 1887; Schu-
mann, 1886; Zebe, 19 15; Schulze-Motel, 1964; Jenny, 1985; Tang, 1992; Bayer,
1994) or separated as Pterospermeae Wu
&
Tang (Tang, 1992), has a seed wing
of
the same type as
Helmiopsis
and
Helmiopsiella
(Barnett, 1988). However,
F’tuospermum
lacks
the bifid cotyledons (Mohana Rao, 1976), the apomorphy of Dombeyeae
S.S.
(Barnett, 1988), and appropriately branches
off
at
a lower node of the cladogram.
The same is true for
Schouteniu,
which was formerly included in Tiliaceae-Tilieae,
and
Burretiodendron
(Tiliaceae-Enteleeae according to Hutchinson, 1967). However,
it is not known if this
is
true for all species recognized by Zhuge
(1
990), who included
Excentrodendron
H.T. Chang
&
R.H. Miao, since
Burretiodendmn
s.1.
appears to be
palynologically heterogeneous (Tang
&
Gao, 1993). The species investigated in the
present study,
B.
esquirolii
(LCv.) Rehder, has the spinose pollen
of
Dombeyoideae.
As a rough rule, this character seems to prevail in the ‘advanced’ subfamilies outlined
here and, for instance, helped to assign genera of uncertain position to Dombeyoideae.
However, spin(u1)ose pollen must not be taken as the only criterion for an inclusion
in this subfamily, since spines, spinules or similar structures apparently evolved
independently in other taxa (e.g. Byttnerieae:
Ayenia;
heterostylous Hermannieae:
see above; Helicteroideae:
Helicteres
p.p.; Erdtman, 1952; M. Jenny, pers. comm.).
Bombacoideae Burnett
The clade representing Bombacoideae (and Malvoideae) in our study is largely
resolved as monophyletic, but weakly or unsupported. Bombacoideae comprise most
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MOLECULAR SYSTEMATICS
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289
genera that formerly have been referred to Bombacaceae. In contrast to previous
classifications, we exclude Durioneae from this alliance but include Fre-
montodendreae
(Frmontodendmn
and
Chirunthodendmn).
The latter have been been
placed in Sterculiaceae by most authors, although bombacaceous affinities have
been generally admitted (Erdtman, 1952; Metcalfe
&
Chalk, 1950). Our data favour
the latter placement, even if
Frmontodendron
has a relatively low chromosome number
(n
=
20) as compared with the general
n
=
43-46 typical of other Bombacoideae.
However, Baum
&
Oginuma’s (1994) karyological review did not include rep-
resentatives of the
Matisiu
alliance; counts for
Chirunthodendm
have not been reported.
Another genus that, contrary to the placement in Tiliaceae-Brownlowieae pro-
posed by Williams
&
Standley
(1
952), could belong
to
Bombacoideae, is
Pentuphris.
This is supported by features such as the basally fused, slightly imbricate calyx that
is penetrated by the contorted petals before anthesis, and the presence of a staminal
column with five phalanges of monothecal anthers (C. Bayer, pers. obs.). Pollen of
Pentuplurk
resembles Nilsson
&
Robyns’
(1
986)
Rhodognuphulopsis
type (C. Bayer, pers.
obs.).
According to our cladograms (Figs 2,
4),
Pentupluris
is sister to Malvoideae.
However, this position is not supported by the bootstrap, and only three additional
steps (as assessed with MacClade) are required to shift the genus into Bombacoideae.
Except for the uncertain position of
Pentupluris
and apart from Durioneae (see
Helicteroideae), the monophyly of Bombacoideae is not refuted by our data (Figs
2,4). Therefore, we tentatively maintain former Bombacaceae as a distinct subfamily,
even if we are aware of the fact that the lack of unambiguously discriminating
characters and future evidence for paraphyly may lead to sinking
it
into Malvoideae
(Judd
et
al.,
1994).
Malvoideae Burnett
Our molecular data provide only weak to moderate support for a monophyletic
clade Malvoideae that corresponds to former Malvaceae in the circumscription
accepted by most authors, thus including Hibisceae and Gossypieae. The dehiscent
fruits of the latter tribes are probably plesiomorphic, and Edlin
(1
935) transferred
them to Bombacaceae, many of which have capsules. In contrast, our analyses
confirm Hutchinson’s (1967: 538) comment that “Malvaceae without the great genus
Hibiscus
would be like a horse without
a
tail” and support the original placement
(see La Duke
&
Doebley, 1995).
There appears to be no single morphological character discriminating Bom-
bacoideae from Malvoideae. Malvoideae are rarely arborescent and usually have
lower chromosome numbers. The free portions of their staminal filaments are
relatively short, monothecal anthers are found throughout, and pollen is almost
always spinose and often pantoporate (Bakhuizen van den Brink, 1924; Erdtman,
1952; Robyns, 1963; Fryxell, 1968; Christensen, 1986; Nilsson
&
Robyns, 1986;
Baum
&
Oginuma, 1994). Nevertheless, these and other characters fall within the
range found in Bombacoideae. A character that has been claimed clearly to
discriminate between these taxa, the persistence of the nucleolus during mitosis
(Baker
&
Baker, 1968), is neither known for a sufficient number of species nor can
it be regarded
as
a convenient character to distinguish the two former families.
However, even if there are exceptions (e.g.
Camptostmon),
the vast majority of genera
can be easily referred
to
one of the respective groups by applying the traditional
combination of characters.
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290
C. BAYER
ETAL.
The topology within the clade comprising Malvoideae, Bombacoideae, Dom-
beyoideae, Brownlowioideae, and Sterculioideae, all in the extended sense outlined
here, is not supported by the bootstrap. Morphologically, Malvoideae resemble both
Bombacoideae and Dombeyoideae more than the remaining subfamilies. Malvoideae
and Dombeyoideae share inflorescence and pollen features that are rare in Bom-
bacoideae (Erdtman, 1952; Christensen, 1986; Nilsson
&
Robyns, 1986; Bayer,
1994). On the other hand some similarities between Bombacoideae and Malvoideae
(e.g. stamina1 tube with monothecal anthers) are
so
striking that it cannot be excluded
that the latter represent an offshoot within the bombacoid clade.
CONCLUSION
Previous workers rarely questioned the traditional family borders within core
Malvales but instead erected highly structured infrafamiliar classifications. Some
earlier authors such as Schumann, who were familiar with the broad range
of
Malvales
groups, recognized inconsistencies in character distribution (e.g. the occurrence
of spinose pollen in
Ptemspemzum;
Schumann, 1886). Nevertheless, the available
information may have been insufficient for attempting a revised family cir-
cumscription, and authors working only on a single family did not perceive the
problems of higher order classification and simply followed tradition. Our new
molecular data provide
a
basis for an revised subdivision
of
core Malvales that is
more consistent with the distribution of morphological characters. Therefore we are
convinced that the classification proposed here will provide an improved basis for
future work
in
Malvales, but we
by
no means consider this as a final solution to
these longstanding problems.
ACKNOWLEDGEMENTS
We would like to thank our colleagues at Kew for help in the Jodrell Laboratory,
F.
R.
Blattner for some DNA samples, D. A. Baum and
T.
Terrazas for the
permission to use their sequence data and
0.
Appel and
L.
J.
Dorr for helpful
comments on the manuscript. Travel support for the first author was kindly provided
by the Deutsche Forschungsgemeinschaft (Ku 174/
14-1).
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APPENDIX
I
Sources
of
plant
material
(family
affiliation
following
Brummitt,
1992,
except
for
Muntingiaceae)
Family Species Accession/Voucher Reference
for
a@B Reference
for
rbcL
Aceraceae
Anacardiaceae
Bixaceae
Bornbacaceae
Brassicaceae
Capparaceae
Caricaceae
Cistaceae
Cochlospermaceae
Diegodendraceae
Dipterocarpaceae
Hippocastanaceae
Limnanthaceae
Malvaceae
Acer
saccharum
L.
fitacia
wa
L.
Rhur
mix
L.
&him
mlk
L.
Bixa
orcllana
L.
Adanronia
rubmstjpa
Jum.
&
H. Penier
Bmnbnr buonopozme
P. Beauv.
Bmnbnr
ceiba
L.
Choriria
spcciosa
A. St.-Hd.
DUG
zibethinur
Murray
hria
zibethinu
Murray
Matisia cordata
Hurnb.
&
Bonpl.
Ochm
j!ydlc
(Cav. ex
Lam.)
Urb.
Pachira
aquatics
Aubl.
Brmsica
car@eslric
L.
Megacarpaen
po&andra
Benth.
S-a
pinnata
(Pursh) Britton
Stanlga
pinnata
(Pursh) Britton
Capparis
harlata
Jacq.
Capparis
Spinosa
L.
Calica
papya
L
Carica
papya
L.
Cktm
mlii
Coste
&
Soulit
Helianhwn
grand$lorum
DC.
Tuberaria
guftata
Gross
Cochlospennum
in-dium
Mddbr.
Dugodendmn
hmbertii
Capwon
Anisoptma
ma+&
Korth.
Aesculus
pavia
Castigl.
Fhrkea
pmserpinuoides
Willd.
Gasppiam
mbinsonii
F.
Muell.
Gossypium
hirsutm
L.
Chase 106, NCU
Terrazas
s.n.,
CHAPA
Terrazas
s.n.,
CHAPA
Anderson 13601, MICH
Chase 243, NCU
Chase 3043, K
Alverson
s.n.,
WIS
Chase 3049, K
Chase 3188, K
Alvenon 2180,
WIS
Chase 3039, K
Kubitzki, Bayer
&
Appel 21, HBG
Chase 244, NCU
Chase 3189,
K
unknown
Chase 565,
K
Price
sm.,
IND
Chase 2748, K
Chase 275
1,
K
WIS
Botanical Garden
Chase 2508,
K
Chase 524, K
Chase 525, K
Chase 1075, K
Fay
s.n.,
K
Capuron 23034, K
Chase 2486,
K
Chase 503,
K
Reznicek 8609, MICH
Wendel
s.n.,
ISC
Chase 3014, K
ntis
30-315,
WIS
Bakker
et
al.,
1998; AF035893
unpublished
Bakker
et
al.,
1998; AF035912
Bakker
et
al.,
1998; AF035914
Bakker
et
al.,
1998; AF035897
this
paper,
A5233050
this paper, A523305
I
this
paper, A5233052
this paper, A5233053
this paper, A5233054
Bakker
el
al.,
1998; AF0359
10
this paper, A5233056
unpublished
unpublished
Bakker
et
al.,
1998; AF035900
Bakker
el
al.,
1998; AFO3590
1
Bakker
el
al.,
1998; AF035902
Bakker
et
al.,
1998; AF035907
this paper, A5233059
this
paper, A5233060
this
paper, A5233061
Bakker
et
al.,
1998; AF035918
Bakker
el
al.,
1998; AF035894
Bakker
et
al.,
1998; AF035904
this paper, A5233063
Albert, Williams
&
Chase, 1992;
LO1
Terrazas, unpublished
Terrazas, unpublished
Chase
ct
al.,
1993; U39270
Fay
et
al.,
1998a; Y 15 139
this
paper, A52331
15
Chase
et
al.,
1993; AF022118
this paper, A52331 16
Alverson
ef
d.,
1998; AF022119
this paper, A5233
1
1
7
this paper, A5233
1
18
this paper, A52331 19
Olmstead
el
al.,
1992
Chase
et al.,
1993; M95753
Rodman
ef al.,
1993; M95754
Rodman
et al.,
1993; M95671
Fay
ef
al.,
1998a; Y15140
Fay
et
al.,
1998a;
Y15141
this paper, AJ233 120
Fay
ef
al.,
1998a; Y15143
Fay
et
al.,
1998a; Y 15 138
Fay
et
al.,
1998a; Y
15
144
Gadek
et
al.,
1996; U39277
Chase
el
al.,
1993; L12679
Chase
et
al.,
1993; L13186
88
I
n
-e
E
continued
Downloaded from https://academic.oup.com/botlinnean/article-abstract/129/4/267/2557306
by guest
on 15 May 2018

APPENDIX
1
continued
Family Species Accession/Voucher Reference
for
atpB
Reference for
rbcL
Malvaceae
Muntingiaceae
Neuradaceae
Resedaceae
Sapindaceae
Sarcolaenaceae
Sphaerosepalaceae
Sterculiaceae
HibLTCU.pLlnduunsiF
(Skottsb.)
0.
Deg.
Lavatcra
acmiolia
Cav.
Pnuonia
multy¶ora
A.St.-Hil.
77mpecsia populnca
(L.)
Sol. ex CorrZa
Dicrnrptdia
donncll-smithii
Standl.
Muntingia
calabura
L.
Nard
pmcumbm L.
huh
alba
L.
huh
alba
L.
Koelmrtnin
paniculata
Lawn.
Rhqbalocarpuc
sp.
Abmma
august0
&.)
1.f.
Bytbreria
aculeata
(Jacq.) Jacq.
Bybfilips
Mart. ex
K.
Schum.
Cola
nitida
(Vent.) Schott
&
Endl.
Dombya
sp.
EtiOh
spedubilic
Planch. ex H0ok.f.
Fmnonlodendron
mexicanwn
Fmntodmdmn
caliiomimm
(TOIT.)
Cov.
X
mwitanum
Davidson
Hehtms barumrir
Jacq.
Helmiopsiclh
madagaccarimsir
Ar6nes
Hm~nnin
emdioides
Kuntze
Hddeganiia bartoi
(Mast.) Kosterm.
&audmin
henanifofin
J.
Gay
Lasqbetalum
sp.
Leptqchia
pallida
K. Schum.
Parmulania
decayam
Arenes
PUmspermum celebincm
Miq.
Reeiuh
thyrsoidca
Lindl.
&
I.
Deg.
sanoh
sp.
Chase 3045, K
Chase 3035, K
Chase 323, NCU
Wendel
sm.,
ISC
Pennington, Owen
&
Zamora
Chase 346, NCU
Collenette 8-93, K
Chase 3017, K
Price s.n.,
IND
Chase 115, NCU
Chase 903, K
Chase 906, K
Chase 3081, K
Alverson
s.n.,
WIS
Chase 3228,
K
Chase 3190, K
Chase 273,NCU
Kubitzki
&
Appel
102,
HBG
Thorne 547 17, RSA
Chase 3037, K
Chase 3048, K
Capuron 18625, K
Chase 3046, K
Chase 3187, K
Chase 2194, K
Chase 2195, K
Cable 4571,
K
Chase 3038, K
Chase 2142, K
Chase 3185, K
13583, K
this
paper, A5233064
this paper, A5233065
Bakker
et
al.,
1998; AF035916
this paper, A5233067
Bakker
el
al.,
1998; AF035908
this paper, A5233069
unpublished
unpublished
this paper, A5233070
this
paper, A5233071
this paper, A5233072
this paper, A5233073
this paper, A5233074
this paper, A5233075
this paper, A5233076
this paper, A5233077
this paper, A5233078
this paper, A5233080
this paper, A5233081
this paper, A5233082
this paper, A5233083
this paper, A5233084
this paper, A5233085
this paper, AJ2331 14
this paper, A5233086
this paper, AJ233 12 1
this paper, A5233122
this
paper, A5233123
Albert
et
al.,
1992; LO1961
Fay
el
al.,
1998a; Y 15 145
Fay
et
al.,
1998a; Y15146
Morgan,
Soltis
&
Robertson, 1994; U06814
Rodman
et
al.,
1993; M95756
Gadek
et
al.,
1996, U39283
5
?
3
r
8
ga
Fay
d
al.,
1998a; Y 15 147
Fay
ct
al.,
1998a; Y 15 148
this paper, A5012208
Alverson
et
al.,
1998; AF022 123
this paper, AJ2331 24
$
=!
this
paper, AJ233 123
0
this paper, A5233126
21
F
5
this
paper, AJ233 129
E
Alverson
et al.,
1998; AF22 124 Davidson
this paper, A5233127
this paper, A5233130
this paper, A5233131
this paper, A5233132
this paper, A52331 33
this
paper, AJ233 134
this paper, AJ233 135
this paper, AJ233 136
this paper, A5233137
continued
14
s
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by guest
on 15 May 2018

lj
11
APPENDIX
1
continued
03
Family Species Accession/Voucher Reference
for
alpB
Sterculiaceae
Ruizia
cardata
Cav. Chase 3227$ K
Rulingin
sp. Chase 2 196, K
Stmulia
apetala
(Jacq.) G. Karst. Chase 352,
NCU
&ohmma
cacao
L. Solheim BUF296,
WIS
&obmma
cacao
L.
Chase 3016, K
7;hommia
solanacea
J.
Gay Chase 3186, K
Tiiplochiton
zambesiocw
hlilne-Redhead
Cubr
36100,
B
Tmhtiopsis
erylllmxylon
(G. Font.) Marais Chase 3040, K
Thymelaeaceae
Aquzlaria
beccariana
Tiegh. Chase 1380, K
Dais
cotin$~lia
L. Chase 1381, K
Gony~!vlus
mmphvllus
(.Miq.) Airy Shaw Chase 1382, K
Phaleria
chermrideano
(Bailey)
C.T.
White Conti 106,
WIS
Phahia
capita&
Jack Chase 1383, K
Thymeha
hirsuta
End. Chase 1882, K
ha
jaminr
(Turcz.)
Burret Chase 2143, K
Bmwnlowia
rlata
Roxb. Chase
2144,
K
Bumudmn
esquimlii
(Lkv.)
Rehder Beusekom
et
al.,
3852, K
Chrirlinna
afncana
DC.
Luke 2916, K
ColanaJoribunda
Craih Kuhitzki
&
Appel 104, HBG
Coehlsia
meiantha
Burret Richards 5873, K
Gaia
occidentalis
L.
Chase 3042,
K
Helwcarpus
&anus
L.
Kubitzki, Bayer
&
Appel
1
I,
HBG
hfkmcos
ladstipulata
(Ridl.) Burret
Coode
7923, K
i\fo&niodendmn
unisop~llum
(Stand.) Thomsen 74. K
Pmke
pobantha
Hassk. Chase 2147,
K
PentaplariS
domteae
L.O.
Williams
&
Standl.Hammel 17697, K
Petmaea
cardata
Lundell Pennington
&
MacQueen 13427, K
Schoutenia
glomerata
King Kubitzki
&
Appel 108, HBG
Spamnannia
ricinocai$a
(Eckl.
&
Zeyh.)Chase 3229, K
Kuntze
'lilia
ampricama
L.
7ih
plappl#os
Scop.
Tmpaeolum
tricolor
Sweet
Tiliaceae
Apeiba
tibourbou
Aubl. Kubitzki, Bayer
&
Appel
I,
HBG
Standl.
&
Steyerm.
Alverson s.n.,
U'IS
Chase 3018, K
Chase 2518, K
'Iropaeolaccae
Tmpaeohm
rnajus
L.
Chase 11 3,
NCU
this paper, A5233087
this paper, A5233088
this paper, A5233089
this paper, A5233090
this paper, A5233091
this paper, A5233092
this paper, A5233093
this paper, A5233079
this paper, A5233094
this paper, A5233095
this paper, A5233096
this paper, A5233097
this paper, A5233098
Bakker
et
al.,
1998; AF035896
Bakker
et
al.,
1998; AF035898
this paper, A5233101
this paper, A3233102
this paper, A5233103
this paper, A5233104
this paper, AJ233105
this
paper, AJ233
I06
this paper, A5233107
this paper, .4J233108
this paper, A5233 109
this paper, A52331 10
this paper, AJ2331
1
1
this paper, AJ233
I
12
this paper, AJ2331 13
Bakker
et
al.,
1998; 4F035917
Reference
for
rbcL
this paper, A5233138
this paper, A52331 39
this paper, AJ233
140
Chase
et
al.,
1993; AF022125
this paper, A5233141
this paper, AJ233 142
this paper, A5233143
Fay
et
al.,
1998a;
Y
15
149
this paper, A5233
144
Fay
et
al.,
1998a;
Y
15
150
Conti, Litt
&
Sytsma, 1996; U26332
n
Fay
et
al.,
1998a;
Y
15
15
1
?
this paper, AJ233 145
2
this paper, A5233146
P
this paper, A5233147
h
this paper, A5233148
2
P
this paper, A5233149
this paper, AJ233
150
this paper, A5233151
this paper, AJ233 I52
this paper, A5233153
this paper, AJ233
I54
this paper, AJ233155
this paper, AJ233 I56
this paper, AJ233157
this
paper, AJ233
I58
this paper, A5233 I59
this paper, A5233128
Chaw
et
al.,
1993: AF022 127
Price
&
Palmrr, 1993; L14706
Downloaded from https://academic.oup.com/botlinnean/article-abstract/129/4/267/2557306
by guest
on 15 May 2018

Genus
Hemuu2nia
Waltheria
Melochia
Dicarpidium
Ray-&
MegatrilheGa
Bytmnia
AJOlia
Rulingia
Commcrsonia
Keraudmia
sningia
&petalum
Thomacia
Hannafaniia
Lysisepalum
Guichenolia
Manuellia
Ht7laniQ
7heobmma
Guaauna
Abmma
finhouia
Scaphopetalum
Leptonychia
Glossoshon
APPENDIX
2
Placement
of
core Malvales genera
in
previous classifications
and
in
the present treatment
Jussieu
(1
789)
Tiliaceae
dubiae
Malvaceae
-
Malvaceae
Malvaceae
Baillon
(1
873)
Malvaceae-Hermannieae
Malvaceae-Buennerieae
Malvaceae-LasiopetaJeae
Malvaceae-Buettnerieae
MalvaceaeHelictereae
Malvaceae-
Buettnerieae
Schumann (1895)
Malvaceae-Hermannieae
~
Sterculiaceae-
Biittnerieae-
Biittnerinae
Sterculiaceae-Lasiopetaleae
-
(sub
7heobmma)
Sterculiaceae-
Biinnerieae-
Theobrominae
Sterculiaceae-Helictereae
Sterculiaceae-
Biittnerieae
Theobrominae
Hutchinson (1967)
Sterculiaceae-Hermannieae
Sterculiaceae- Byttnerieae
Sterculiaceae-Lasiopeialeae
Sterculiaceae-Theobromeae
Sterculiaceae-Helictereteae
Sterculiaceae-
Theobromeae
this paper (Malvaceae-)
Bptnerioideae
5
m
d
d
E
0
=E
incertae sedis
(Byttnerioideae?)
N
W
continued
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APPENDIX
2
continued
Baillon (1873)
Genus Schumann
(1
895)
Gocrhnlria
Psnulocorchom
Tdiaceae-Tilieae
Entclza
Conh
Spamnannia
Chpptrtania
Duboscia
Dwpliltcia
Hydmgaster
V*
Mollia
Lulua
T%hospmum
crauia
Mkos
colona
Elcuthcms!ylil
Luchcopsir
Zlralir
Dzplophrackun
Erinocargus
Tiimfetta
Heliocmpus
Aptiba
G!yphma
An&tnua@s
Elin
Craigia
Tiliaceae-Tilieae
Jussieu
(1
789)
Tiliaceae-Tdieae
Tiliaceae verae
TiaceaeTdieae/Grwieae
Tiliaceae-Grewieae
~
Tiliaceae verae
(sub
Gmh)
-
Tdiaceae verae
Tiliaceae verae
~
Tiliaceae-Tilieae
1
TiliaceaeTiieae
Tiliaceae-Grewieae
(sub
G&)
(sub
Gmoia)
Tdiaceae-Tdieae
Tiliaceae-Tdieae
I-
-
Hutchinson (1967)
Flacourtiaceae
Tiliaceae-
Pseudocorchoreae
Tiliaceae-
Enteleeae
Tiliaceae-
Spamnanieae
Tiliaceae-Tilieae
Tiliceae-
Desplatzieae
Tiliceae
Imeheeae
Tiliaceae-Lueheeae/Grewieae
Tiliacea4rewieae
(sub
G&)
Tdiaceae-Triumfetteae
Tdiaceae-Apeiheae
Tiiaceae-Tilieae
Sterculiaceae-
hiopetaleae
W
0 0
this paper (Malvaceae-)
Grewioideae
n
Tilioideae
incertae sedis
riioideae?)
continued
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APPENDIX
2
conaiuud
~
this
paper (Malvaceae-)
Helicteroideae
Genus Jussieu
(1
789)
Baillon (1873) Hutchinson (1967)
Schumann (1895)
Sterculiaceae-Tarrietieae
Sterculiaceae-Helictereteae
Malvaceae-Helictereae
Sterculiaceae-Helictereae
Malvaceae
~
Malvaceae-Bombaceae Bombacaceae-Durioneae Bombacaceae-Durioneae
5
Brownlowioideae
E;;
incertae sedis
(Helicteroideae?)
Tdiaceae-Diplodisceae
Tiliaceae-Brownlowieae
Tiliaceae-Brownlowieae
Tdiaceae-Brownlowieae
Tiliaceae-Benyeae
2
I
incertae sedis
Sterculioideae
E
v,
Tiliaceae-Enteleeae
Sterculiaceae-Sterculieae
Sterculiaceae-Stercdieae
(sub
Fimizna)
Malvaceae-Sterculieae
Malvaceae
-
Sterculiaceae-Tarrietieae
Malvaceae-Sterculieae
continued
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APPENDIX
2
cunhd
Genus
Helmiopsitlla
HelmwpSiS
Erioloena
Dombya
hlelhania
Rurrj,
Pmlspetes
Astiria
Tmchetia
Cheimloena
Ha-
Paraabmbya
Parmlhania
Tiheh@SiS
Conhampsis
Ptemsp
mum
SChoUtmia
Bumtibdendmn
Sinea
.hisogurdonia
Jussieu
(1
789)
Malvaceae
Baillon (1873)
~
Malvaceae-Helictereae
Malvaceae-Dombeyeae
Malvaceae-Helictereae
Tiliaceae-Tilieae
Schumann
(1
895) Hutchinson (1967)
Sterculiaceae-
Sterculiaceae-Eriolaeneae Sterculiaceae-Eriolaeneae
Sterculiaceae-
Helrniopsideac
~~
this
paper (Malvaceae-)
Dombeyoideae
n
2
m
P
h
41
b
rc
incertae
sedis
(Dornbeyoideae?)
continued
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MOLECULAR
SYSTEMATICS
OF
MALVALES
303
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