J 1095-8339 2012 01235 X PDF

bs_bs_banner
Botanical Journal of the Linnean Society, 2012, 169, 540. With 1 figure
A new subfamilial and tribal classification of the

pantropical flowering plant family Annonaceae
informed by molecular phylogenetics
LARS W. CHATROU1*, MICHAEL D. PIRIE2, ROY H. J. ERKENS3,4,
THOMAS L. P. COUVREUR5, KURT M. NEUBIG6, J. RICHARD ABBOTT7,
JOHAN B. MOLS8, JAN W. MAAS3, RICHARD M. K. SAUNDERS9 and
MARK W. CHASE10
1
Wageningen University, Biosystematics Group, Droevendaalsesteeg 1, 6708 PB Wageningen, the

Netherlands
2
Department of Biochemistry, University of Stellenbosch, Stellenbosch, Private Bag X1, Matieland
7602, South Africa
3
Utrecht University, Institute of Environmental Biology, Ecology and Biodiversity Group, Padualaan
8, 3584 CH, Utrecht, the Netherlands
4
Maastricht Science Programme, Maastricht University, Kapoenstraat 2, 6211 KL Maastricht, the
Netherlands
5
Institut de Recherche pour le Dveloppement (IRD), UMR DIA-DE, DYNADIV Research Group, 911,
avenue Agropolis, BP 64501, F-34394 Montpellier cedex 5, France
6
Florida Museum of Natural History, University of Florida, PO Box 117800, Gainesville, FL
32611-7800, USA
7
Missouri Botanical Garden, PO Box 299, St. Louis, MO 63166-0299, USA
8
Netherlands Centre for Biodiversity, Naturalis (section NHN), Leiden University, Einsteinweg 2,
2333 CC Leiden, the Netherlands
9
School of Biological Sciences, The University of Hong Kong, Pokfulam Road, Hong Kong, China
10
Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3DS, UK
Received 14 October 2011; revised 11 December 2011; accepted for publication 24 January 2012
The pantropical flowering plant family Annonaceae is the most species-rich family of Magnoliales. Despite
long-standing interest in the systematics of Annonaceae, no authoritative classification has yet been published in
the light of recent molecular phylogenetic analyses. Here, using the largest, most representative, molecular dataset
compiled on Annonaceae to date, we present, for the first time, a robust family-wide phylogenetic tree and
subsequent classification. We used a supermatrix of up to eight plastid markers sequenced from 193 ingroup and
seven outgroup species. Some of the relationships at lower taxonomic levels are poorly resolved, but deeper nodes
generally receive high support. Annonaceae comprises four major clades, which are here given the taxonomic rank
of subfamily. The description of Annonoideae is amended, and three new subfamilies are described: Anaxagoreoideae, Ambavioideae and Malmeoideae. In Annonoideae, seven tribes are recognized, one of which, Duguetieae, is
described as new. In Malmeoideae, seven tribes are recognized, six of which are newly described: Dendrokingstonieae, Fenerivieae, Maasieae, Malmeeae, Monocarpieae and Piptostigmateae. This new subfamilial and tribal
classification is discussed against the background of previous classifications and characters to recognize subfamilies
are reviewed. 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2012, 169, 540.
ADDITIONAL KEYWORDS: plastid markers subfamilies supermatrix tribes.
*Corresponding author. E-mail: lars.chatrou@wur.nl

2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2012, 169, 540
L. W. CHATROU ET AL.
INTRODUCTION
Inventories of tropical forests on all continents invariably list Annonaceae as one of the most diverse plant
families (Phillips & Miller, 2002). In terms of species
richness and abundance of individuals, Annonaceae
contributes significantly to the diversity of trees in
Neotropical forests (e.g. Gentry, 1988; Valencia,
Balslev & Paz Y Mio, 1994) and lianas and trees in
rain forests of the Old World (e.g. van Gemerden
et al., 2003; Slik et al., 2003; Tchouto et al., 2006).
Around 2400 species in 108 genera are currently
recognized in the family (Rainer & Chatrou, 2006),
> 300 of which have been described in taxonomic
papers, monographs and regional or continental floras
since the start of the international Annonaceae
project almost 30 years ago (Maas, 1983; Chatrou,
1999). In parallel with renewed taxonomic efforts,
recent years have seen increasingly detailed studies
of the phylogenetics of Annonaceae (e.g. Doyle &
Le Thomas, 1994, 1996; Mols et al., 2004; Pirie
et al., 2006; Couvreur et al., 2008; Erkens, Maas &
Couvreur, 2009). The polyphyly of notorious dustbin
genera, such as Polyalthia Blume, has been demonstrated (Mols et al., 2004; Saunders, Su & Xue, 2011),
and even easily recognizable genera in morphological
terms have been shown to be nonmonophyletic
(Chatrou, Koek-Noorman & Maas, 2000; Erkens
et al., 2007; Chatrou et al., 2009; Couvreur et al.,
2009). On the basis of these results, some generic
circumscriptions have been realigned following the
primary principle of monophyly (Chatrou et al., 2000;
Su et al., 2005; Rainer, 2007; Erkens & Maas, 2008;
Mols et al., 2008; Nakkuntod et al., 2009; Su, Chaowasku & Saunders, 2010; Surveswaran et al., 2010;
Xue et al., 2011).
Given the large numbers of species in Annonaceae,
a useful and stable infrafamilial classification is necessary to aid communication and information
retrieval. Although a number of formal or informal
classifications have been proposed (e.g. Baillon, 1868;
Hutchinson, 1923; Fries, 1959; Walker, 1971; van
Heusden, 1992; van Setten & Koek-Noorman, 1992),
none has yet proved to be stable in the face of increasing knowledge of the diversity of the family. These
classifications were based on different sources of data,
such as floral morphology (van Heusden, 1992), fruit
and seed morphology (van Setten & Koek-Noorman,
1992) and palynology (Walker, 1971). In each case, the
data were interpreted intuitively, resulting in often
contradictory conclusions/classifications. The classification of Fries (1959), primarily based on floral
characters, remains perhaps the most widely used.
However, with few exceptions, his tribes and informal groups of genera are neither characterized by
unequivocal (combinations of) characters nor demon-
strably monophyletic. To quote from a recent monographic work: Systems of informal classifications [in
Annonaceae] have proliferated to the point that
classification of the family into smaller units is in
disarray (Johnson & Murray, 1995: 249).
The phylogenetic reconstruction in Annonaceae was
initiated with cladistic analyses of macromorphological and palynological characters (Doyle & Le Thomas,
1994, 1996, 1997). Although indicating the earliest
diverging position of Anaxagorea A.St.-Hil., such
characters showed high levels of homoplasy and
limited phylogenetic utility compared with subsequent studies employing DNA sequence data (Doyle,
Bygrave & Le Thomas, 2000; Mols et al., 2004; Richardson et al., 2004; Pirie et al., 2006; Couvreur et al.,
2008, 2011). To date, a new formal classification based
on molecular phylogenetic work has been postponed
because of limitations in taxon representation and
phylogenetic resolution. Clades are currently referred
to by informal names relating to aspects of their
molecular evolution [e.g. long branch clade (LBC) and
short branch clade (SBC) sensu Richardson et al.,
2004, in reference to the differing levels of genetic
divergence between the two major clades identified in
the early molecular phylogenetic studies]. These
names are neither comprehensive in scope nor usefully memorable. Improvements in generic classification have thus yet to be matched by an improved
higher level classification.
A robust and maximally representative hypothesis
of relationships between clades in this important
angiosperm family is clearly warranted. In this
article, we present a phylogenetic analysis of Annonaceae inferred from multiple plastid DNA loci, representing 94 of the 108 currently recognized genera and
marking an important improvement in both the representation of taxa (at the generic level) and phylogenetic resolution in Annonaceae compared with
previous efforts (e.g. Richardson et al., 2004; Couvreur et al., 2011). We place this analysis in the
context of previous infrafamilial classifications, evaluate the monophyly of the groupings identified and
discuss the relative utility of various morphological
characters for the diagnosis of groups in Annonaceae.
The rank at which monophyletic groups might be
classified remains a more or less subjective decision;
we discuss the potential classifications that might be
adopted given a number of secondary criteria, such as
diagnosability and size of the groups. Finally, based
on the results, we formally describe four subfamilies
and 12 tribes. The subfamilies are Anaxagoreoideae
(corresponding to the genus Anaxagorea), Ambavioideae (corresponding to the ambavioid clade of Doyle
& Le Thomas, 1994, 1996), Annonoideae (corresponding to the LBC of Richardson et al., 2004, and the
inaperturate clade of Doyle & Le Thomas, 1994, 1996)
ANNONACEAE PHYLOGENETICS AND CLASSIFICATION

and Malmeoideae (corresponding to the SBC of
Richardson et al., 2004, and the malmeoid/
piptostigmoid/miliusoid clade of Doyle & Le Thomas,
1994, 1996). Seven tribes are recognized in Annonoideae, of which Duguetieae is described as new, and
seven tribes are recognized in Malmeoideae, of which
six are newly described, namely Dendrokingstonieae,
Fenerivieae, Maasieae, Malmeeae, Monocarpieae and
Piptostigmateae.
MATERIAL AND METHODS

TAXON SAMPLING
Most genera sampled were represented by two
species. Exceptions were monotypic genera (with just
single samples) and genera that have previously
been demonstrated to be para- or polyphyletic, for
which each segregate clade was represented by two
samples. We selected taxa to bracket the crown node
of each clade, if known. Of the 108 currently recognized genera (Rainer & Chatrou, 2006), 94 were represented, five of which were sampled for the first
time, i.e. they were not represented in Richardson
et al. (2004), who sampled 79 genera, Pirie et al.
(2006), who increased sampling for the SBC, Couvreur et al. (2008), who increased sampling for the
LBC, and Couvreur et al. (2011), who added another
few unsampled genera (Table 1). Subsequent to
analyses performed for this article, the genera Anomianthus Zoll., Balonga Le Thomas, Cyathostemma
Griff., Dasoclema J.Sinclair, Ellipeia Hook.f. &
Thomson, Ellipeiopsis R.E.Fr. and Rauwenhoffia
Scheff. have been brought into synonymy with
Uvaria L. (Zhou, Su & Saunders, 2009; Zhou et al.,
2010). With the exception of Balonga and Dasoclema
(which are not sampled), these former genera are
thus still represented individually. A list of currently
recognized genera of Annonaceae is presented in
Table 2, with the numbers of recognized species,
representation of species in previous phylogenetic
studies (i.e. evidence for monophyly) and representation in this study.
CHARACTER
SAMPLING
We used previously published plus unpublished

sequence data from up to eight plastid loci: protein
coding rbcL, matK and ndhF genes plus an intron,
trnL, and spacer regions trnT-L, trnL-F, trnS-G,
atpB-rbcL and psbA-trnH. Total genomic DNA was
extracted following a protocol adapted from the cetyltrimethylammonium bromide (CTAB) method (Doyle
& Doyle, 1987), as described in Erkens et al. (2008).
Conditions for the polymerase chain reactions (PCRs)
and primers for the plastid markers were standard,
and are identical to Pirie et al. (2006) and Erkens
et al. (2008). PCR products were purified using

QIAquick PCR purification kits (Qiagen) and
sequenced with the PCR primers.
The relative importance for the phylogenetic accuracy of sampling either characters or taxa has been
discussed extensively (Graybeal, 1998; Mitchell,
Mitter & Regier, 2000; Cummings & Meyer, 2005;
Rokas & Carroll, 2005). We adopted a sampling strategy that addressed both issues at once, specifically by
following a supermatrix approach in which missing
data are tolerated (Philippe et al., 2004; Wiens, 2005,
2006; Pirie et al., 2008). In this way, we focused
sequencing effort on the resolution of relationships
between the major clades of Annonaceae, which is of
particular relevance to classification in the family. For
all 200 taxa, rbcL, the trnL intron and trnL-F spacer
were sampled. After phylogenetic analyses of these
three markers (results not shown), 56 species were
selected, paying particular attention to the inclusion
of early diverging species in clades at all levels. These
56 species were selected as placeholders to be
sampled for additional characters using the remaining six markers. All data (both taxa and characters)
were subsequently combined in a single supermatrix,
i.e. a data matrix including incompletely sampled
taxa.
DNA sequences were aligned manually using
PAUP* version 4.10b (Swofford, 2000) and MacClade
(Maddison & Maddison, 2000) following the guidelines in Kelchner (2000). Characters in regions for
which alignment was ambiguous were excluded from
the analyses. Microsatellites were also excluded, as
these regions are variable within species (Kelchner &
Clark, 1997; Provan, Powell & Hollingsworth, 2001;
personal observations on species for which the same
spacer region from different accessions was
sequenced). Gaps in the alignment shared by two or
more taxa were coded as a single binary character
(presence/absence) according to the simple indel
coding method of Simmons & Ochoterena (2000).
Single-nucleotide indels where verified once more
against the tracer files to ensure that they were not
sequence editing artefacts. Nucleotide characters
included in these indels were excluded from the
analyses, with a few exceptions when insertions in
clades contained parsimony informative variation at
the nucleotide level. Two short sequences, of 15 positions in psbA-trnH and of 12 positions in the trnT-L
spacer, appeared to represent inversions. Around half
of the species exhibited the reverse-complement
sequence of the other half and transitions between
the motifs appeared to be frequent, with different
motifs apparent in closely related species (as reported
in Pirie et al., 2006). We aligned one motif with the
reverse complement of the other and, as the informative base changes that were revealed displayed little
Annona herzogii (R.E.Fr.)

H.Rainer
Annickia chlorantha (Oliv.)

Setten & Maas
Annickia pilosa (Exell)
Setten & Maas
Annona glabra L.
Anaxagorea silvatica R.E.Fr.
Anaxagorea phaeocarpa
Mart.
Maas, P.J.M.
8836 (U)
Sosef, M.S.M.
1877 (WAG)
Sosef, M.S.M.
1803 (WAG)
Chatrou, L.W.
467 (U)
Chatrou, L.W.
162 (U)
Chatrou, L.W.
279 (U)
Chatrou, L.W.
278 (U)
Keler, P.J.A.
3116 (L)
Van Balgooy,
M. 5141 (L)
Rabevohitra,
R. 2035
(MO)
Maas, P.J.M.
8592 (U)
Liriodendron chinense
Sargent
Magnolia kobus DC.
Alphonsea boniana Finet &

Gagnep.
Alphonsea elliptica Hook.f.
& Thomson
Ambavia gerrardii (Baill.)
Le Thomas
Chatrou, L.W.
s.n. (U)
Mixed origin
Eupomatia bennettii
F.Muell.
Galbulimima belgraveana
(F.Muell.) Sprague
Degeneria vitiensis
L.W.Bailey & A.C.Sm./
D. roseiflora J.M.Mill.
Coelocaryon preussii Warb.
AY743450
AY841596
Gabon
Cultivated in UUBG,
origin Florida
Peru
AY841656
AY841594
AY743439
Gabon
Brazil
AY238952
JQ513886
Madagascar
Ecuador
AY318966
Indonesia
DQ125062
DQ125050
AY743488
AY841393
AY743477
AY238960
AY743438
AY318965
L12646
AY841593
JQ437547
AY743475
matK
DQ861790
L12643
AY743437
AY841592
rbcL
Cultivated in UUBG,
origin China
Cultivated in UUBG,
origin Japan
Vietnam
Cultivated in UUBG,
origin Australia
Origin unknown
Origin unknown
Cultivated in UUBG, of
Neotropical origin
Gabon
Persea americana Mill.
UUBG
87GR00058
Wieringa, J.J.
3640 (WAG)
Mixed origin
Country
Species
Table 1. Collections and GenBank numbers
EF179308
EF179281
AY841402
AY841401
EF179280
EF179279
JQ437546
JQ437545
ndhF
JQ742023
JQ742022
AY841572
AY841571
DQ861644
DQ861643
JQ742021
trnTL
AY841734
AY841673
AY743469
AY841671
AY231284
(intron)
AY238944
(spacer)
AY743458
JQ513889
AY319078
AY319077
AY743457
AY220415
(intron)
AY220362
(spacer)
AY841670
AY220414
(intron)
AY220361
(spacer)
DQ861842
AY743456
AY841669
trnLF
DQ125132
DQ125116
AY841444
AY841442
AY841427
AY841426
AY841424
JQ513882
psbA-trnH
EF179273
EF179246
AY841371
AY841370
AY578140
EF179244
JQ513883
atpB-rbcL
EF179350
EF179323
AY841551
AY841550
EF179322
EF179321
JQ513885
trnSG
8
UUBG
84GR00275
Chatrou, L.W.
54 (U)
Keler, P.J.A.
3199 (L)
Cymbopetalum brasiliense
(Vell.) Benth. ex Baill.
Cymbopetalum torulosum
G.E.Schatz
Dasymaschalon macrocalyx
Finet & Gagnep.
Bocageopsis pleiosperma
Maas
Asteranthe asterias (S.

Moore) Engl. & Diels
Bocageopsis multiflora
(Mart.) R.E.Fr.
Asimina triloba (L.) Dunal
Asimina angustifolia
A.Gray
Asimina rugelii B.L.Rob.
Cananga odorata (Lam.)

Hook.f & Thomson
Cleistopholis glauca Pierre
ex Engl. & Diels
Cremastosperma brevipes
(DC.) R.E.Fr.
Cremastosperma
cauliflorum R.E.Fr.
Cyathocalyx martabanicus
Hook.f. & Thomson
Chatrou, L.W.
468 (U)
Cheek, M.
7896 (K)
UUBG
94GR01614
(U)
Wieringa, J.J.
4018 (WAG)
Weerasooriya,
A. s.n. (U)
J. R. Abbott
22361
(FLAS)
Chatrou, L.W.
276 (U)
Robertson, A.
7548 (WAG)
Jansen-Jacobs,
M.J. 5789
(U)
Miralha,
J.M.S. 300
(U)
Chatrou, L.W.
93 (U)
Wieringa, J.J.
3278 (WAG)
Scharf, U. 76
(U)
Chatrou, L.W.
224 (U)
Mols, J.B. 11
(L)
Artabotrys sp.
Artabotrys hexapetalus (L.f.)

Bhandari
Anonidium sp.
Annona muricata L.
AY743542
DQ125054
DQ125055
AY743527
AY743519
AY841605
AY841608
AY743442
AY841610
French Guiana
Peru
Cultivated in Kebun
Raya Bogor,
Indonesia
Cultivated in UUBG,
originating from
Brazil
Costa Rica
Thailand
EF179277
AY743550
AY841395
AY841603
AY841394
Gabon
AY841601
Brazil
AY841602
AY841600
Guyana
AY743479
DQ125053
DQ125052
AY238962
DQ125051
AY743478
Costa Rica
EU169757
AY743441
JQ513887
USA
Cultivated in UUBG,
origin USA
Kenya
DQ124939
AY841599
AY238953
AY841598
AY743440
USA
Gabon
Cultivated in UUBG,
origin India
Cultivated in UUBG,
of Neotropical origin
Cameroon
EF179290
EF179289
EF179288
AY841406
AY841405
AY841404
AY841403
EF179287
EF179286
EF179285
EF179284
EF179283
EF179282
JQ742029
DQ861646
JQ742028
AY841574
AY841573
JQ742027
JQ742026
JQ742025
DQ861649
JQ742024
DQ861648
AY841688
AY743461
AY841686
AY841683
AY743565
AY743573
AY841681
AY841680
AY841679
AY841678
EU169757
AY743460
GQ139881
AY841677
AY231286
(intron)
AY238946
(spacer)
AY841676
AY841675
AY743459
EF179313
DQ125121
DQ125120
AY841448
AY841447
AY841432
AY841431
AY841430
DQ125119
DQ125118
AY841429
DQ125117
AY841428
EF179255
EF179254
EF179253
AY841375
AY841374
AY841373
AY841372
EF179252
EF179251
EF179250
EF179249
EF179248
EF179247
EF179332
EF179331
EF179330
AY841553
AY841552
AY841549
AY841548
EF179329
EF179328
EF179327
EF179326
EF179325
EF179324
Fissistigma glaucescens
(Hance) Merr.
Fissistigma uonicum (Dunn)
Merr.
Fitzalania heteropetala
(F.Muell.) F.Muell.
Enicosanthum
membranifolium
J.Sinclair
Enicosanthum paradoxum
Becc.
Ephedranthus boliviensis
Chatrou & Pirie
Ephedranthus sp.
Disepalum pulchrum (King)

J.Sinclair
Disepalum platipetalum
Merr.
Drepananthus biovulatus
(Boerl.) Survesw. &
R.M.K.Saunders
Duguetia hadrantha (Diels)
R.E.Fr.
Duguetia staudtii (Engl. &
Diels) Chatrou
Desmos elegans (Thwaites)

Saff.
Dielsiothamnus divaricatus
(Diels) R.E.Fr.
Desmos chinensis Lour.
Keler, P.J.A.
2746 (L)
Chatrou, L.W.
301 (U)
Maas, P.J.M.
8826 (U)
Law, C.L
00/07b (L)
Law, C.L
00/05 (L)
Forster, P.I.F.
8326 (K)
Chatrou, L.W.
181 (U)
van Andel,
T.R. 3290
(U)
Keler, P.J.A.
3198 (L)
AY841617
AY318977
Hong Kong
Australia
AY841616
Brazil
AY743444
AY841614
Bolivia
Hong Kong
AY318975
AY318974
Thailand
Indonesia
AY738178
Cameroon
HM173779
Indonesia
AY738161
AY841612
Indonesia
Peru
JQ513888
EU169781
Tanzania
Malaysia
HQ214067
JQ762414
Sri Lanka
Hong Kong
AY319060
AY319059
Costa Rica
Costa Rica
AY743443
Thailand
Keler, P.J.A.
3201 (L)
Chatrou, L.W.
85 (U)
Chatrou, L.W.
94 (U)
C.-C. Pang
N2 (HKU)
Kostermans
24761 (L)
Johnson, D.M.
1903
(OWU)
Chan, R. 192
(FLAS)
Takeuchi
18201 (L)
Wong 46009
(L)
Dasymaschalon sootepense
Craib
Desmopsis microcarpa
R.E.Fr.
Desmopsis schippii Standl.
rbcL
Country
Species
Table 1. Continued
AY841396
AY740558
AY740541
matK
AY841407
EF179294
EF179293
ndhF
AY841575
JQ742030
DQ861650
trnTL
AY319089
AY841695
AY743463
AY841694
AY841692
AY319087
AY319086
AY740590
AY740573
HM173751
AY841690
GQ139909
EU169759
HQ214069
JQ762415
AY319174
AY319173
AY743462
trnLF
AY318977
AY743444
AY841463
DQ125124
DQ125123
psbA-trnH
AY841376
EF179259
EF179258
atpB-rbcL
AY841554
EF179336
EF179335
trnSG
10
Letestudoxa bella Pellegr.
Isolona cooperi Hutch. &

Dalziel ex G.P.Cooper &
Record
Klarobelia inundata
Chatrou
Klarobelia stipitata Chatrou
Hornschuchia citriodora
D.M.Johnson
Isolona campanulata Engl.
& Diels
Guatteria pudica N.Zamora

& Maas
Haplostichanthus
longirostris (Scheff.)
Heusden
Hexalobus crispiflorus A.
Rich.
Hexalobus salicifolius Engl.
Greenwayodendron
suaveolens (Engl. & Diels)
Verdc.
Guatteria anomala R.E.Fr.
Greenwayodendron oliveri
(Engl.) Verdc.
Goniothalamus griffithii
Hook.f. & Thomson
Goniothalamus tapis Miq.
Fusaea longifolia (Aubl.)

Saff.
Fusaea peruviana R.E.Fr.
Friesodielsia desmoides
(Craib) Steenis
Friesodielsia sp.
AY740962
Mexico
AY743452
AY841628
UUBG, originating
from Ivory Coast
Peru
Costa Rica
UUBG
84GR00382
Chatrou, L.W.
205 (U)
Chatrou, L.W.
113 (U)
Wieringa, J.J.
2797 (WAG)
Gabon
AY238954
UUBG, of tropical
African origin
AY841629
AY841626
AY841625
EU169783
Gabon
Brazil
EU169782
Gabon
AY318979
AY841524
Kenya
Papua New Guinea
AY743451
Ghana
AY740994
AY841622
Thailand
Costa Rica
AY743446
AY743445
Peru
Thailand
AY841620
AY841619
Gabon
Peru
AY841618
Thailand
Sosef, M.S.M.
2287 (WAG)
Sosef, M.S.M.
2376 (WAG)
Maas, P.J.M.
8828 (U)
UUBG
86GR00240
Ishiki, M.
2233 (U)
Chatrou, L.W.
107 (U)
Takeuchi
15656 (L)
Keler, P.J.A.
3189 (L)
Wieringa, J.J.
3605 (WAG)
Chatrou, L.W.
175 (U)
Chatrou, L.W.
179 (U)
Keler, P.J.A.
3188 (L)
Keler, P.J.A.
3193 (L)
Jongkind,
C.C.H. 1795
(WAG)
Semsei 2376
(K)
DQ125059
AY743490
AY238963
AY740945
AY740913
AY743489
DQ125058
AY743484
AY743483
EF179302
AY841409
EU169715
JQ769093
EF179298
AY841408
EF179297
EF179296
EF179295
DQ861653.
AY841577
JQ742033
DQ861663
DQ861657
AY841576
JQ742032
JQ742031
DQ861652
AY841707
AY841706
AY743471
AY231287
(intron)
AY238947
(spacer)
AY841704
AY841703
EU169761
EU169760
AY319091
AY741043
AY741011
AY841538
AY743470
AY841700
AY743465
AY743464
AY841698
AY841697
AY841696
DQ125128
AY841469
DQ125127
DQ125197
AY841437
AY841465
DQ125126
DQ125125
AY841436
EF179267
AY841378
EF179266
JQ513884
EF179263
AY841377
EF179262
EF179261
EF179260
EF179344
AY841556
EU169806
FJ842397
EF179340
AY841555
EF179339
EF179338
EF179337
11
Miliusa horsfieldii (Benn.)

Pierre
Meiogyne stenopetala
(F.Muell.) Heusden
Meiogyne virgata (Blume)
Miq.
Mezzettia parviflora Becc.
Meiogyne sp.
Meiogyne cylindrocarpa
(Burck) Heusden
Marsypopetalum littorale
(Blume) B.Xue &
R.M.K.Saunders
Marsypopetalum pallidum
(Blume) Kurz
Meiocarpidium lepidotum
(Oliv.) Engl. & Diels
Malmea sp.
Maasia glauca (Hassk.)

Mols, Keler & Rogstad
Maasia sumatrana (Miq.)
Malmea dielsiana R.E.Fr.
Lettowianthus stellatus
Diels
Maasia discolor (Diels)
Keler, P.J.A.
3192 (L)
Breteler, F.
13947
(WAG)
Ridsdale, C.E.
DV-M1-1930
(L)
Rainer, H.
1593 (WU)
Jessup, L.W.
706 (K)
Keler, P.J.A.
2751 (L)
Okada 3388
(L)
Mols, J.B. 1
(L)
Chatrou, L.W.
8 (U)
Rastini 153
(L)
AY318981
Malaysia
AY318983
Indonesia
AY318986
AY318982
Indonesia
Indonesia
AY318971
Australia
AY841623
EU169776
Gabon
Mexico
AY318980
Thailand
AY319026
Indonesia
AY238955
Peru
AY841527
AY319039
Malaysia
Peru
AY319023
AY319021
Papua New Guinea
Indonesia
EU169775
Kenya
AY841630
Gabon
Letestudoxa glabrifolia
Chatrou & Repetur
Breteler, F.J.
12858
(WAG)
Robertson, A.
7505 (WAG)
Takeuchi &
Ama 16394
(L)
Mols, J.B. 20
(L)
SAN 143918
(SAN)
Chatrou, L.W.
122 (U)
rbcL
Country
Species
Table 1. Continued
EU169687
AY841397
AY238964
AY518873
AY518872
matK
AY841411
AY841410
AY841418
AY841416
ndhF
AY841579
AY841578
AY841586
AY841584
trnTL
AY319098
AY319095
AY319094
AY319083
AY841701
AY319093
EU169754
AY319092
AY319140
AY231288
(intron)
AY238948
(spacer)
AY841541
AY319153
AY319137
AY319135
EU169753
AY841708
trnLF
EU169731
AY841475
AY841473
AY841503
AY841500
psbA-trnH
AY841380
AY841379
AY841387
AY841385
atpB-rbcL
EU169798
AY841558
AY841557
AY841565
AY841563
trnSG
12
Neo-uvaria parallelivenia
(Boerl.) H.Okada &
K.Ueda
Onychopetalum periquino
(Rusby) D.M.Johnson &
N.A.Murray
Neostenanthera
myristicifolia (Oliv.) Exell
Neo-uvaria acuminatissima
(Miq.) Airy Shaw
Monodora myristica
(Gaertn.) Dunal
Mosannona costaricensis
(R.E.Fr.) Chatrou
Mosannona papillosa
Chatrou
Mwasumbia alba Couvreur
& D.M.Johnson
Monodora crispata Engl.
Monocyclanthus vegnei
Keay
Monocarpia euneura Miq.
Monanthotaxis whytei
(Stapf) Verdc.
Monanthotaxis sp.
Mitrephora polypyrena
(Blume) Miq.
Mitrephora teysmannii
Scheff.
Mkilua fragrans Verdc.
Mischogyne michelioides
Exell
Mitrella kentii (Blume) Miq.
Miliusa mollis Pierre
Pholsena 1756
(L)
Bamps, P.
4459 (WAG)
Gardette, E.
2239 (K)
Mols, J.B. 7
(L)
Keler, P.J.A.
3226 (L)
Chatrou, L.W.
474 (U)
UUBG
84GR00388
Wieringa, J.J.
3833 (WAG)
Slik, J.W.F.
20022931
(L)
Jongkind,
C.C.H. 6992
(WAG)
UUBG
E64GR00066
UUBG
E84GR00389
Chatrou, L.W.
90 (U)
Pitman, N.
s.n. (U)
Couvreur,
T.L.P. 85
(WAG)
Wieringa, J.J.
3566 (WAG)
Ridsdale, C.E.
DV-SR-4671
(L)
Keler, P.J.A.
sub IV-H-73
(L)
Chatrou, L.W.
425 (U)
EU169765
Liberia
AY318999
AY319000
AY319065
Malaysia
Indonesia
Bolivia
EU747680
Tanzania
AY743448
AY743514
Ecuador
Gabon
AY743503
AY743510
AY518876
AY743486
EU169700
AY743447
Cultivated in UUBG,
origin Ivory Coast
Cultivated in UUBG,
origin Ivory Coast
Costa Rica
AY841637
AY318998
Indonesia
AY518865
AY841636
DQ125060
EF179278
AY841634
AY841635
AY318996
Thailand
Cultivated in UUBG,
origin Kenya
Cultivated in UUBG,
origin Nigeria
Gabon
AY318997
AY841633
Malaysia
Indonesia
EU169786
AY318989
Angola
Thailand
AY841414
EF179306
AY841413
EU169721
AY841412
EF179304
EF179303
AY841582
JQ742036
AY841581
JQ742035
AY841580
JQ742034
DQ861647
AY319179
AY319113
AY319112
AY743467
EU747674
AY743500
AY743496
AY743466
AY841715
EU169787
AY319111
AY841713
AY841713
AY841712
AY319109
AY319110
AY841711
EU169764
AY319101
AY841485
DQ125130
AY841479
DQ125129
AY841477
EF179315
DQ861696
AY841383
EF179271
AY841382
EF179270
AY841381
EF179269
EF179268
AY841561
EF179348
AY841560
EU169812
AY841559
EF179346
EF179345
13
Platymitra macrocarpa
Boerl.
Phaeanthus ebracteolatus
(C.Presl.) Merr.
Piptostigma mortehani De
Wild.
Piptostigma pilosum Oliv.
Oxandra venezuelana
R.E.Fr.
Oxandra xylopioides Diels
Oxandra macrophylla
R.E.Fr.
Oxandra polyantha R.E.Fr.
Oxandra longipetala R.E.Fr.
Oxandra asbeckii (Pulle)

R.E.Fr.
Orophea polycarpa A.DC.
AY841648
Cameroon
AY319013
AY743454
Gabon
Indonesia
AY319012
AY841646
Peru
Papua New Guinea
AY841645
AY841643
Peru
Costa Rica
AY841642
AY841641
Peru
Costa Rica
AY841639
Guyana
AY319008
Thailand
AY319010
AY319006
Thailand
Thailand
AY841632
AY319004
Indonesia
Indonesia
EU169789
Kenya
Robertson, A.
7547 (WAG)
Keler, P.J.A.
2953 (L)
Keler, P.J.A.
1605 (L)
Chalermglin
440403
(TISTR)
Chalermglin
440416-1
(TISTR)
Keler, P.J.A.
3234 (L)
University of
Guyana,
course
Neotrop.
Botany
UG-NB-55
(U)
Chatrou, L.W.
114 (U)
Chatrou, L.W.
204 (U)
Chatrou, L.W.
215 (U)
Chatrou, L.W.
120 (U)
Chatrou, L.W.
165 (U)
Utteridge, T.
17 (KL)
Wieringa, J.J.
2779 (WAG)
Wieringa, J.J.
2030 (WAG)
Okada 3457
(L)
Ophrypetalum odoratum
Diels
Orophea celebica (Blume)
Miq.
Orophea creaghii (Ridl.)
Leonarda & Keler
Orophea enterocarpa
Maingay ex Hook.f. &
Thomson
Orophea kerrii Keler
rbcL
Country
Species
Table 1. Continued
AY743492
matK
AY841415
ndhF
AY841583
trnTL
AY319127
AY841726
AY743473
AY319125
AY841724
AY841723
AY841721
AY841720
AY841719
AY841717
AY319123
AY319121
AY319119
AY841710
AY319117
EU169767
trnLF
AY841498
psbA-trnH
AY841384
atpB-rbcL
AY841562
trnSG
14
Polyalthia obliqua Hook.f.

& Thomson
Polyalthia pendula Capuron
ex G.E.Schatz & Le
Thomas
Polyalthia rumphii (Blume
ex Hensch.) Merr.
Polyalthia cf. longifolia

(Sonn.) Thwaites
Polyalthia longipes (Miq.)
Koord. & Valet.
Polyalthia longifolia (Sonn.)

Thwaites
Polyalthia debilis (Pierre)

Finet & Gagnep.
Polyalthia flagellaris (Becc.)
Airy Shaw
Polyalthia cf. glabra
(Hook.f. & Thomson)
J.Sinclair
Polyalthia lateriflora
(Blume) King
Polyalthia congesta (Ridl.)

J.Sinclair
Polyalthia cerasoides
(Roxb.) Benth. & Hook.f.
ex Beddome
Polyalthia cinnamomea
Hook.f. & Thomson
Polyalthia cauliflora Hook.f.

& Thomson
Polyalthia celebica Miq.
Polyalthia borneensis Merr.
AY319019
Malaysia
Van Balgooy,
M. 5654 (L)
AY319031
AY319030
Madagascar
Indonesia
AY319029
AY319028
Malaysia
Indonesia
AY319025
Indonesia
AY319027
AY319024
Indonesia
Hort. Bot.
Bog.
XII-B-VII-37
(L)
Johnson, D.M.
1965
(OWU)
Mols, J.B. 14
(L)
Ridsdale, C.E.
DV-M2-11443
(L)
Ambriansyah
1694 (L)
Rabevohitra
2386 (K)
Tanzania
AY319032
Indonesia
AY319022
AY319018
Malaysia
Brunei
AY319017
Thailand
AY319020
AY319016
Indonesia
Thailand
AY319015
AY319014
Singapore
Malaysia
Rastini 224
(L)
Ridsdale, C.E.
DV-SR-7921
(L)
Keler, P.J.A.
3114 (L)
Mols, J.B. 9
(L)
Chalermglin
440214-4
(L)
Ridsdale, C.E.
DV-M1-347
(L)
Ridsdale, C.E.
DV-S-5105
(L)
Keler, P.J.A.
3228 (L)
Duling 38 (K)
AY319145
AY319144
AY319143
AY319142
AY319139
AY319141
AY319138
AY319146
AY319136
AY319134
AY319133
AY319132
AY319131
AY319130
AY319129
AY319128
15
Popowia pisocarpa (Blume)

Endl.
Porcelia steinbachii (Diels)
R.E.Fr.
Pseudartabotrys letestui
Pellegr.
Pseudephedranthus fragrans
(R.E.Fr.) Aristeg.
Pseudomalmea diclina
(R.E.Fr.) Chatrou
Popowia odoardi Diels
Polyceratocarpus
microtrichus (Engl. &
Diels) Ghesq. ex Pellegr.
Polyceratocarpus pellegrinii
Le Thomas
Polyalthia xanthopetala
Merr.
Polyalthia viridis Craib
Polyalthia stenopetala
(Hook.f. & Thomson)
Finet & Gagnep.
Polyalthia stuhlmannii
(Engl.) Verdc.
Polyalthia subcordata
Blume (Blume)
Polyalthia suberosa (Roxb.)
Thwaites
de Wilde
J.J.E. 8718
(WAG)
Ridsdale, C.E.
DV-SR-7422
(L)
Van Balgooy,
M. 5683 (L)
UUBG
99GR00210
Wieringa, J.J.
3273 (WAG)
Maas, P.J.M.
6878 (U)
Chatrou, L.W.
211 (U)
Chalermglin
440214-3
(L)
Ridsdale, C.E.
DV-S-5107
(L)
Bos, J.J. 6684
(WAG)
Gravendeel,
B. 678 (L)
UUBG
83GR00317
AY319068
Peru
AY841398
AY841651
Venezuela
DQ125061
AY319043
Malaysia
AY841650
EU747684
Cameroon
EU747683
Cameroon
AY841649
AY319041
Malaysia
Cultivated in UUBG,
origin Bolivia
Gabon
AY319040
Thailand
AY238965
AY319044
AY238956
Cultivated in UUBG,
origin India
matK
Indonesia
AY319037
AY319035
Kenya
Indonesia
AY319034
Thailand
AY319033
Indonesia
Polyalthia sclerophylla
Hook.f. & Thomson
Hort. Bot.
Bog.
XX-D-82 (L)
Chalermglin
440302
(TISTR)
Luke 1424 (K)
rbcL
Country
Species
Table 1. Continued
AY841419
EF179307
AY841417
ndhF
AY841587
AY841585
trnTL
AY319128
AY841729
AY841728
AY841727
AY319158
AY319157
EU747678
EU747677
AY319155
AY231289
(intron)
AY238949
(spacer)
AY319154
AY319151
AY319149
AY319148
AY319147
trnLF
AY841506
DQ125131
AY841502
psbA-trnH
AY841388
EF179272
AY841386
atpB-rbcL
AY841566
EF179349
AY841564
trnSG
16
Stelechocarpus burahol
(Blume) Hook.f. &
Thomson
Stelechocarpus cauliflorus
(Scheff.) J.Sinclair
Sanrafaelia ruffonammari
Verdc.
Sapranthus microcarpus
(Donn.Sm.) R.E.Fr.
Sapranthus viridiflorus
G.E.Schatz
Sphaerocoryne gracilis (Oliv.
ex Engl. & Diels) Verdc.
Sphaerocoryne sp.
Pseudoxandra polyphleba
(Diels) R.E.Fr.
Pseudoxandra
spiritus-sancti Maas
Pseuduvaria megalopus
(K.Schum.) Y.C.F.Su &
Mols
Pseuduvaria pamattonis
(Miq.) Y.C.F.Su &
R.M.K.Saunders
Pseuduvaria phuyensis
(R.M.K.Saunders,
Y.C.F.Su & Chalermglin)
Y.C.F.Su &
R.M.K.Saunders
Pseuduvaria rugosa (Blume)
Merr.
Ruizodendron ovale (Ruiz &
Pav.) R.E.Fr.
Sageraea lanceolata Miq.
Pseudomalmea sp.
Hort. Bot.
Bog.
XV-A-196
(L)
Keler, P.J.A.
.3209 (L)
Maas, P.J.M.
8600 (U)
Ridsdale, C.E.
DV-M2-1692
(L)
Kayombo
3027 (MO)
Maas, P.J.M.
8457 (U)
Chatrou, L.W.
55 (U)
Robertson, A.
7554 (WAG)
Chalermglin
440214-2
(L)
Mols, J.B. 13
(L)
Slik, J.W.F.
20022911
(L)
Keler, P.J.A.
3221 (L)
Idarraga, A.
13 (U)
Maas, P.J.M.
8227 (U)
Maas, P.J.M.
8833 (U)
Takeuchi
15599 (L)
EU169790
AY319052
AY319051
EU169755
AY319071
AY319053
AY319054
Tanzania
Honduras
Costa Rica
Kenya
Thailand
Indonesia
Indonesia
AY319050
Malaysia
AY319001
Thailand
AY841657
AY319049
Indonesia
Ecuador
AY319011
Papua New Guinea
AY319048
AY841533
Brazil
Thailand
AY841654
AY841652
Peru
Colombia
AY743493
HQ214070
AY841399
JQ769091
AY841422
AY841421
JQ769092
AY841590
AY841589
JQ742037
AY319168
AY319167
AY319185
EU169777
AY319165
AY319166
EU169768
AY319164
AY841735
AY319162
AY319114
AY319163
AY319124
AY841547
AY841732
AY841730
AY841515
AY841514
AY319048
AY319001
AY319049
AY319011
AY841513
AY841512
AY841391
AY841390
AY841569
AY841568
17
Uvaria cherrevensis (Pierre

ex Finet & Gagnep.)
L.L.Zhou, Y.C.F. Su &
R.M.K. Saunders
Uvaria clementis (Merr.)
Attanayake, I.M.Turner &
R.M.K.Saunders
Uvaria cuneifolia (Hook.f. &
Thomson) L.L.Zhou,
Y.C.F.Su & R.M.K.
Saunders
Uvaria dulcis Dunal
Uvaria chamae P.Beauv.
Unonopsis stipitata Diels
Trigynaea duckei (R.E.Fr.)

R.E.Fr.
Trigynaea lanceipetala
D.M.Johnson &
N.A.Murray
Trivalvaria macrophylla
(Blume) Miq.
Unonopsis pittieri Saff.
Tridimeris sp.
Tetrameranthus laomae
D.R.Simpson
Toussaintia orientalis Verdc.
AY841661
Costa Rica
Thailand
Indonesia
Thailand
Mohtar
S48169 (L)
Maxwell, J.F.
88509 (L)
Cultivated in UUBG,
origin Togo
Thailand
FJ743815
FJ743822
FJ743823
AY841606
AY841400
AY743487
matK
AY841663
AY841662
AY319056
Indonesia
Peru
AY743449
Peru
Keler, P.J.A.
3211 (L)
Chase, M.W.
1207 (K)
Chatrou, L.W.
68 (U)
Chatrou, L.W.
253 (U)
Chatrou, L.W.
482 (U)
Maxwell
90625 (L)
AY841660
Peru
AY319055
EU169778
Tanzania
Mexico
AY841659
Peru
AY841658
AY319070
Costa Rica
Brazil
AY319069
Costa Rica
Chatrou, L.W.
67 (U)
Chatrou, L.W.
100 (U)
Stevenson,
D.W. 1002
(U)
Pipoly, J.
13407 (U)
Johnson, D.M.
(OWU)
Schatz, G.E.
1198 (K)
Chatrou, L.W.
129 (U)
Chatrou, L.W.
234 (U)
Stenanona costaricensis
R.E.Fr.
Stenanona panamensis
Standl.
Tetrameranthus duckei
R.E.Fr.
rbcL
Country
Species
Table 1. Continued
AY841423
EF179309
ndhF
AY841591
JQ742038
trnTL
FJ743849
FJ743857
FJ743853
FJ743858
AY841741
AY841740
AY841739
AY319170
AY743468
AY841738
AY319169
EU169756
AY841737
AY841736
AY319184
AY319183
trnLF
AY841519
psbA-trnH
AY841392
EF179274
atpB-rbcL
AY841570
EF179351
trnSG
18
Woodiellantha sp.
Xylopia ferruginea (Hook.f.
& Thomson) Hook.f. &
Thomson
Xylopia hypolampra Mildbr.
& Diels
Xylopia peruviana R.E.Fr.
Uvariopsis vanderystii
Robyns & Ghesq.
Uvariopsis tripetala
(Baker.f.) G.E.Schatz
Uvariodendron molundense
(Diels) R.E.Fr.
Uvariopsis korupensis
Gereau & Kenfack
Saunders
07/3 (HKU)
Uvaria siamensis (Scheff.)

L.L.Zhou, Y.C.F.Su &
R.M.K.Saunders
Uvariastrum insculptum
(Engl. & Diels) Sprague
& Hutch.
Uvariastrum pynaertii De
Wild.
Uvariodendron kirkii Verdc.
Jongkind,
C.C.H. 4707
(WAG)
Wieringa, J.J.
2620 (WAG)
Robertson, A.
7550 (WAG)
Sosef, M.S.M.
2219 (WAG)
Richardson,
J.E. 212
(WAG)
Sosef, M.S.M.
2241 (WAG)
Jongkind,
C.C.H. 4356
(WAG)
Lugas 311 (K)
Slik, J.W.F.
2002-S 558
(L)
Wieringa, J.J.
3748 (WAG)
Chatrou, L.W.
483 (U)
Saunders
05/1 (HKU)
Chalermglin
440402-2
(TISTR)
UUBG
84GR00334
Uvaria grandiflora Roxb. ex

Hornem.
Uvaria griffithii L.L.Zhou,
Y.C.F.Su &
R.M.K.Saunders
Uvaria lucida Benth. subsp.
virens (N.E.Br.) Verdc.
EU169793
Kenya
AY841665
AY841666
AY841668
AY238958
Gabon
Cultivated in UUBG,
origin Peru
EU169780
Ivory Coast
Malaysia
Indonesia
EU169773
Gabon
EU169796
EU169792
Gabon
Gabon
EU169791
EU169794
FJ743824
Cultivated in Hong
Kong Botanic
Gardens
Ivory Coast
Gabon
AY238966
AY238957
Cultivated in UUBG,
origin West African
AY238967
DQ125063
FJ743820
Thailand
FJ743836
Thailand
EF179312
EF179311
EF179310
DQ861654
JQ742040
JQ742039
AY231291
(intron)
AY238951
(spacer)
AY841746
AY841743
AY841744
EU169758
EU169795
EU169774
EU169772
EU169771
EU169770
EU169769
AY231290
(intron)
AY238950
(spacer)
FJ743859
FJ743855
FJ743870
DQ125134
DQ125133
AY841440
EF179276
EF179275
EF179353
EF179352
19
20
Table 2. Currently recognized genera of Annonaceae, number of species and number of species sampled in phylogenetic
analyses, demonstrating (lack of) monophyly. Unless indicated otherwise, studies that demonstrate monophyly are given,
including the sampling size. A dash indicates either a lack of presence altogether in any phylogenetic study or the presence
of a single species only. Genera followed by an asterisk were not included in the phylogenetic analyses presented in this
paper
Genus
No. of
recognized
species
Evidence for
monophyly:
no. of species
sampled and
reference
Afroguatteria*
Alphonsea
Ambavia
Anaxagorea
Annickia
Annona
Anonidium
Artabotrys
Asimina
Asteranthe
Bocagea*
Bocageopsis
Boutiquea*
Cananga
Cardiopetalum*
Cleistochlamys*
Cleistopholis
Cremastosperma
Cyathocalyx
Cymbopetalum
Dasymaschalon
Dendrokingstonia*
Desmopsis
Desmos
Diclinanona*
Dielsiothamnus
Disepalum
Drepananthus
Duckeanthus*
Duguetia
Enicosanthum
Ephedranthus*
Exellia
Fenerivia*
Fissistigma
Fitzalania
Friesodielsia
Froesiodendron*
Fusaea
Gilbertiella
Goniothalamus
Greenwayodendron
Guatteria
Haplostichanthus
Hexalobus
Hornschuchia
Isolona
Klarobelia
Letestudoxa
Lettowianthus
Maasia
Malmea
Marsypopetalum
Meiocarpidium
2
25
2
30
8
162
4
102
7
3
2
4
1
2
3
1
4
29
7
27
21
2
14
26
3
1
9
26
1
93
18
6
1
10
48
2
51
3
2
1
134
2
210
11
5
10
20
12
3
1
6
6
6
1
4g
25n
3j,d
22b
25q
2j
2p
19i
7p
3k
22r
2a
2g (unresolved)
7r
8m
15p
32i
4g (unresolved)
3j
10l
2k
2a
5r
2k
20h
2j
145f
2c
14e
6j, 2a
2k
5l
4j
5t
Genus
No. of
recognized
species
Evidence for
monophyly:
no. of species
sampled and
reference
Meiogyne
Melodorum*
Mezzettia
Miliusa
Mischogyne
Mitrella
Mitrephora
Mkilua
Monanthotaxis
Monocarpia
Monocyclanthus
Monodora
Mosannona
Mwasumbia
Neostenanthera
Neo-uvaria
Onychopetalum
Ophrypetalum
Orophea
Oxandra
Phaeanthus
Phoenicanthus*
Piptostigma
Platymitra
Polyalthia
Polyceratocarpus
Popowia
Porcelia
Pseudartabotrys
Pseudephedranthus*
Pseudomalmea
Pseudoxandra
Pseuduvaria
Pyramidanthe*
Ruizodendron
Sageraea
Sanrafaelia
Sapranthus
Schefferomitra*
Sphaerocoryne
Stelechocarpus
Stenanona
Tetrameranthus
Toussaintia
Tridimeris
Trigynaea
Trivalvaria
Unonopsis
Uvaria
Uvariastrum
Uvariodendron
Uvariopsis
Woodiellantha
Xylopia
15
10
3
50
2
8
47
1
56
1
1
16
14
1
4
5
2
1
50
28
9
2
14
2
135
8
26
7
1
1
4
23
57
1
1
9
1
6
1
3
3
14
6
4
1
12
4
48
187
8
15
16
1
157
4a (paraphyletic)
9g
14s
2k,r
2a
13e
7i
2a, g
9g
11d (polyphyletic)
2a, g
4d
2a
26l (polyphyletic)
4d
3g
6j
54o
4a
2g
2u
3a
2g
2k
2k
2a, t
3j
59u
2c
2c
2c
4k
T. Chaowasku et al. (unpubl. data).

Chatrou et al. (2009).
c
Couvreur et al. (2008).
d
Couvreur et al. (2009).
e
Couvreur (2009).
f
Erkens et al. (2007).
g
Mols et al. (2004).
Nakkuntod et al. (2009).

Pirie et al. (2005).
j
Pirie et al. (2006).
k
Richardson et al. (2004).
l
Saunders, Su & Xue (2011).
m
R. M. K. Saunders (unpubl. data).
n
Scharaschkin & Doyle (2005).
Su & Saunders (2009).

Surveswaran et al. (2010).
q
Thongpairoj (2008).
r
Wang (2009).
s
Weerasooriya & Saunders (2010).
t
Xue et al. (2011).
u
Zhou et al. (2012).

or no homoplasy, we assumed them to be effectively
homologous and included them in the analyses (following Pirie et al., 2006).
PHYLOGENETIC
ANALYSES
As plastid DNA is inherited as a unit, individual

markers were not analysed separately to look for
incongruence; we excluded a paralogous second copy
of the trnL-F region from these analyses (Pirie et al.,
2007). For the combined analyses, a supermatrix
approach was adopted, i.e. including all taxa, even
where data were not available for particular markers,
which were coded as missing.
Parsimony analysis
Analyses were performed using PAUP* version 4.10b
(Swofford, 2000) with the heuristic search option, tree
bisectionreconnection (TBR) branch swapping, the
accelerated transformation (ACCTRAN) criterion and
the multiple parsimonious trees (MULPARS) option
invoked. Character states were specified as unordered
and equally weighted (Fitch parsimony; Fitch, 1971).
Alignment gaps were treated as missing data, but
larger indels were coded as above. The search strategy consisted of 10 000 replicates of random addition
sequence, saving 25 trees per replicate. To ensure
that the tree island with the globally shortest tree
had been visited, we performed a parsimony ratchet
(Nixon, 1999) search as implemented in PAUPRat
(Sikes & Lewis, 2001), with 1000 ratchet iterations,
perturbing 25% of the characters in each round. The
robustness of the phylogenetic relationships was
assessed by nonparametric bootstrapping of the data.
Following Mller (2005), the number of bootstrap
replicates was set at a high level (50 000), whereas
the thoroughness of searches and computing time per
bootstrap replicate were minimized by limiting the
number of random addition sequence replicates to
one, saving a single tree. When evaluating the
results, we used the following descriptions of support
by bootstrap values: 5074% represents weak
support, 7584% moderate support and 85100%
strong support.
Maximum likelihood (ML) analysis
In recent years, ML algorithms have become more
efficient, allowing for fast and accurate estimation of
ML trees and even bootstrapping, which is especially
useful for large datasets (Guindon & Gascuel, 2003;
Stamatakis, 2006; Zwickl, 2006; Morrison, 2007). For
this study, we used the RAxML web-server program
available at the CIPRES portal in San Diego, CA,
USA (http://www.phylo.org/portal2), which implements an efficient and rapid heuristic bootstrap in
RAxML (Stamatakis, Hoover & Rougemont, 2008).
21
For each analysis, the maximum likelihood search

and estimate proportion of invariable sites boxes
were selected, with a total of 1000 bootstrap replicates performed. The dataset was not partitioned, as
the number of missing data per marker (excluding
trnL-F and rbcL) resulted in aberrant results. Indel
characters were necessarily excluded from the analyses, resulting in a total of 7657 included characters.
Bayesian inference
Bayesian analysis was performed on the combined
dataset using MrBayes 3.2 (Huelsenbeck et al., 2001;
Ronquist & Huelsenbeck, 2003). We used the 56 completely sampled species to identify the best partitioning of the data, employing the Bayes factor criterion
(2ln Bayes factor > 10; Kass & Raftery, 1995; Sinsheimer, Lake & Little, 1996) following Brandley,
Schmitz & Reeder (2005). Bayes factors were calculated as the ratio of the harmonic means of each
partitioning strategy, which are produced by MrBayes
in the output from the sump command. We tested the
following partitioning strategies: 1, combined protein
coding (coding) regions/combined intron and spacer
(noncoding) regions/combined binary coded indel
characters (indels) (three partitions); 2, codon positions for the three coding regions (rbcL, matK, ndhF)
separately/noncoding/indels (11 partitions); 3, nucleotide and indel characters for each marker separately
(14 partitions). Values of the 2ln Bayes factor were all
between 0 and 1, showing no preference for any of the
partitioning strategies. This being the case, the data
were partitioned according to strategy 1. This relatively simple strategy represents an attempt to best
reflect differences between markers whilst maximizing the proportion of topology relative to substitution
parameter change proposals in the Markov Chain
Monte Carlo (MCMC) chains. Both rates and substitution models were allowed to vary across partitions.
Priors for the number of parameters in the DNA
substitution models were applied to each partition [as
determined using ModelTest 3.06 (Posada & Crandall,
1998), with the topology in each case derived from a
randomly selected most parsimonious tree]. In each
case, this corresponded to models with NST = 6,
gamma distributed rates and proportion of invariable
sites. Runs were set to continue indefinitely, and the
outputs were tested periodically for convergence
through both visual inspection of cumulative clade
posterior probabilities (PPs) (using AWTY; Nylander
et al., 2008) and according to effective sample sizes
(ESS) calculated using Tracer 1.4 (Rambaut & Drummond, 2007).
RESULTS
A small number of our sequencing attempts were
unsuccessful, e.g. in the case of trnT-L for Cananga
22
Table 3. Characteristics of individual markers, which have been assessed using all data available for each locus, i.e. 193
sequences for rbcL and trnL-F and 5961 sequences for the remaining loci. Outgroup taxa were excluded from the
calculations. Consistency index (CI) includes all (i.e. variable and invariant) nucleotide characters
Marker
Number of
characters
in aligned
matrix
Number of
potentially
parsimony
informative
characters (%)
Number
of indel
characters
CI
RI
Model
selected by
MrModeltest
rbcL
matK
ndhF
atpB-rbcL
trnT-L
trnL intron
trnL-F
psbA-trnH
trnS-G
1376
831
1956
747
673
520
377
433
744
284
247
715
206
225
197
214
209
241
0
1
4
27
0
23
32
24
19
0.40
0.61
0.50
0.70
0.68
0.60
0.56
0.54
0.70
0.80
0.70
0.70
0.82
0.73
0.83
0.84
0.69
0.81
GTR + I + G
GTR + G
GTR + I + G
GTR + G
GTR + G
GTR + G
GTR + G
GTR + G
GTR + G
(20.6)
(29.7)
(36.6)
(27.6)
(33.4)
(37.9)
(56.8)
(48.3)
(32.4)
RI, retention index.
odorata (Lam.) Hook.f. & Thomson, Meiocarpidium

lepidotum (Oliv.) Engl. & Diels and Cleistopholis
glauca Pierre ex Engl. & Diels, psbA-trnH and trnS-G
for Pseudoxandra polyphleba (Diels) R.E.Fr. and
Ruizodendron ovale (Ruiz & Pav.) R.E.Fr. and ndhF
for Meiocarpidium lepidotum. The database contained a total of 7787 characters after alignment and
exclusion of ambiguous regions of the alignment.
Table 3 shows the number of positions in the aligned
data matrix and the number of indel characters per
marker.
The heuristic search resulted in 20 960 most parsimonious trees with a tree length of 9806 steps, an
overall consistency index (Kluge & Farris, 1969) of
0.55 and an overall retention index (RI; Farris, 1989)
of 0.77. The ratchet search did not find shorter trees.
The total number of potentially parsimony informative characters was 2729 (35.0%). The greatest
number of parsimony informative characters was for
ndhF (715) and then atpb-rbcL (206); psbA-trnH (209)
had the least (Table 3). The final ML optimization
likelihood was -67 480.27. The two MrBayes runs
were terminated after ten million generations, having
reached the same likelihood plateau after c. 350 000
generations, which were discarded as burn-in. Analysis of the tree output using AWTY (Nylander et al.,
2008) showed that the clade PPs of the two runs were
consistent with each other, and clade PPs of each run
had reached values that no longer changed with additional generations. The effective sampling size of all
parameters of the combined output, minus burn-in,
as estimated using Tracer (Rambaut & Drummond,
2007), exceeded 200.
PHYLOGENETIC
RELATIONSHIPS
The monophyly of Annonaceae (clade A; Fig. 1A) and

the sister group relationship between Anaxagorea
and the remaining Annonaceae (clade B; Fig. 1A) are
maximally supported in all three analyses. Clade C
(Fig. 1) is weakly supported in the parsimony analyses [parsimony bootstrap percentage (PBP), 66],
mainly because of a degree of uncertainty in the
position of Meiocarpidium Engl. & Diels. Both parametric analyses, however, assign high support [ML
bootstrap percentage (MBP), 97; Bayesian PP, 0.95]
to this node. The rest of the strongly supported relationships in clade C are the same among all three
analyses.
The monophyly of the remainder of Annonaceae,
representing > 97% of the species diversity of the
family, is well supported in all analyses (clade D; PBP,
99; MBP, 100; PP, 1.00; Fig. 1A). The sister clades E
and F receive maximum support in all three analyses.
Most of the relationships in Annonoideae, clade E,
receive strong support (maximum parsimony, ML and
Bayesian; Fig. 1B). Bocageeae (clade G) receives
maximum support (maximum parsimony, ML and
Bayesian), as does the sister relationship between
Bocageeae and the remaining Annonoideae (clade H).
The latter splits into five strongly supported, speciesrich clades, the relationships of which, however, are
mostly unresolved: Xylopia L./Artabotrys R.Br. (clade
I: c. 250 species; PBP, 97; MBP, 100; PP, 1.00); Duguetia A.St.-Hil., Fusaea (Baill.) Saff., Letestudoxa
Pellegr. and Pseudartabotrys Pellegr. (clade J: c. 100
species; PBP, 100; MBP, 100; PP, 1.00); Guatteria Ruiz
& Pav. (clade K: c. 250 species; PBP, 100; MBP, 100;

A
Persea americana
Coelocaryon preussii
Galbulimima belgraveana
Degeneria vitiensis
Liriodendron chinense
Magnolia kobus
Eupomatia bennettii
Anaxagorea phaeocarpa
Anaxagorea silvatica
Meiocarpidium lepidotum
Lettowianthus stellatus
Drepananthus biovulatus
Cananga odorata
Cyathocalyx martabanicus
Tetrameranthus duckei
Tetrameranthus laomae
Mezzettia parviflora
Ambavia gerrardii
Cleistopholis glauca
C
A
Annonoideae, node E (Figure 1B)

D
10 changes
Malmeoideae, node F (Figure 1C)
all support values BS 85%/PP 0.95
23
(Fig. 1C) across all methods. The first dichotomy in

Malmeoideae divides five African genera (clade T;
PBP, 74; MBP, 88; PP, 0.97) from the remaining
Malmeoideae (clade U; maximally supported). The
latter comprises three major clades: V, including c.
175 Neotropical species (PBP, 85; MBP, 95; PP, 1.00);
W, comprising the genus Maasia Mols, Keler &
Rogstad; and X (PBP, 99; MBP, 100; PP, 1.00), in
which the Asian genus Monocarpia Miq. is sister to
the rest of the c. 525 species (PBP, 71; MBP, 78; PP,
1.00), mainly distributed in Asia, with four genera
endemic to Central America [Desmopsis Saff.,
Sapranthus Seem., Stenanona Standl. and Tridimeris
Baill. (35 species in total) plus a small number of
species of Polyalthia from Madagascar (e.g. P. pendula Capuron ex G.E.Schatz & Le Thomas) and
eastern Africa (e.g. P. stuhlmannii (Engl.) Verdc.].
Overall resolution in this clade is poor in all three
analyses, but, nevertheless, the nonmonophyly of
Polyalthia, with c. 135 currently recognized species, is
indicated.
two support values BS 85%/PP 0.95

one support value BS 85%/PP 0.95
Figure 1. Phylogram showing one of many most

parsimonious tree topologies, with support [maximum
parsimony bootstrap (BS) percentages, maximum
likelihood BS percentages and Bayesian posterior
probabilities (PP) indicated in the key]. A, Phylogenetic
relationships among the outgroup taxa and species of
Anaxagoreoideae and Ambavioideae. B, Phylogenetic
relationships in Annonoideae. C, Phylogenetic relationships in Malmeoideae.
PP, 1.00); Annona L., Anonidium Engl. & Diels,

Asimina Adans., Disepalum Hook.f., Goniothalamus
(Blume) Hook.f. & Thomson and Neostenanthera
Exell (clade M; PBP, 100; MBP, 100; PP, 1.00); and a
clade containing Palaeotropical species only (clade N:
c. 600 species; PBP, 100; MBP, 100; PP, 1.00). Clade M
is sister to clade N (PBP, 100; MBP, 100; PP, 1.00).
Clade N consists of three maximally supported clades:
clade O, including two monotypic African genera
Ophrypetalum Diels and Sanrafaelia Verdc.; clade P,
including c. 80 African tree species; and clade Q,
including c. 475 Palaeotropical climbing species. A
small number of more shallow nodes in the tree are
much more strongly supported by Bayesian PPs compared with the results of the maximum parsimony
and ML analyses. For example, the sister group relationship between Toussaintia Boutique and a clade
containing Friesodielsia Steenis and Monanthotaxis
Baill. (clade R; PBP, 62; MBP, 78; PP, 1.00) and the
monophyly of a clade of five African genera (clade
S; PBP, 62; MBP, 85; PP, 1.00).
Resolution and support in Malmeoideae (clade F)
are lower than in Annonoideae and Ambavioideae
DISCUSSION
Molecular phylogenetic studies, such as this, benefit
in part from the availability of many more characters
(Chase & Cox, 1998). A further benefit of DNA
sequence data over morphological characters that
have been used previously to infer phylogenetic relationships is the ability to isolate conflicting phylogenetic signals that can be confounded in patterns
of inheritance of morphological variation. We used
sequence data from eight plastid loci, representing a
large number of characters that are always inherited
as a single unit (the plastid genome) without recombination (Birky, 2001). In one instance, differing phylogenetic signals caused by paralogy have been
identified for putative plastid sequences in Annonaceae (Pirie et al., 2007), but, in general, congruence
of plastid loci has been demonstrated. Congruence
between low-copy and plastid loci analyses has been
documented in other families (e.g. Grniak, Paun &
Chase, 2010). In the absence of contradictory evidence
(in the form of independent DNA loci), we assume
that this plastid tree (Fig. 1) broadly reflects the
potentially more complex phylogenetic history underlying the complete genomes of the taxa involved.
Support for this topology is largely robust, at least for
the purposes of defining major clades, although resolution in these clades is, in some cases, poor. Poor
resolution does not affect the creation of an infrafamilial classification for Annonaceae because weakly
supported/resolved clades are not given taxonomic
recognition. The supermatrix approach employed here
works well, particularly for the resolution of deeper
nodes, and the generally higher Bayesian PPs (com-
24
Figure 1. Continued
Figure 1. Continued
25
26
pared with BPs) reported here are a further attribute

known to be associated particularly with matrices
comprising a proportion of missing data (Wiens, 2006;
Pirie et al., 2008). We consider PP 0.95 to be robust,
even if BPs are considerably lower.
MORPHOLOGICAL CHARACTERS AND THE HISTORY

OF ANNONACEAE CLASSIFICATION
The family of Annonaceae is a very natural one. With
this statement, King (1893) was hardly exaggerating
the perceived monophyly of the family, although he
clearly would not have used that term. Apart from
frequent inclusion of the monotypic Eupomatiaceae in
the past (e.g. Baillon, 1868; Diels, 1912), delimitation
of the Annonaceae has never been ambiguous,
because of the presence of synapomorphies, such as
simple vessel perforations, a cobweb-like wood structure in cross-section (caused by broad and high multiseriate xylem rays with many narrow, tangential
parenchyma bands perpendicular to the xylem rays;
Koek-Noorman & Westra, 2012), alternate, distichous
leaves, trimerous calyx and corolla, and perichalazal
ovules (Sauquet et al., 2003). On the other hand,
ambiguity has governed the delimitation of groups
within the family from the stance of their recognition.
A number of attempts have been made to formally
classify Annonaceae in tribes or subfamilies (e.g.
Endlicher, 1839; Hutchinson, 1923) or to produce
informal groupings of genera (e.g. Diels, 1932; Fries,
1959; Walker, 1971). Each of these classifications
differs in the kinds of characters that were emphasized (a summary is provided in Table 4). Following
the first treatment of the family by Dunal (1817),
several authors used fruit characters for the main
divisions of the family (Endlicher, 1839; Diels, 1932).
Baillon (1868) and Prantl (1891) produced similar
treatments, as the groups they proposed were based
solely on floral characters. Fries (1959) produced a
comprehensive treatment of the family, the size of
which had greatly expanded because of his numerous
revisionary works (e.g. Fries, 1930, 1931, 1934, 1937,
1939). Floral characters plus a single fruit character
(free vs. fused carpels) formed the basis for the
delimitation of informal groups of genera (natrliche
Gruppen) in tribes. The work of Fries (1959) is probably the most influential classification of Annonaceae
to date, in particular having served as a guide for the
planning of taxonomic studies in the family. It has,
however, not gone without criticism, even before the
application of molecular phylogenetic data. Le
Thomas (1969), for example, expressed doubts as to
the systematic value of sepal and petal aestivation,
one of the key floral characters in the classification of
Annonaceae, notably in the system by Fries (1959),
but also by Hooker & Thomson (1855). In Le Thomas
(1969) treatment of Annonaceae for the Flore du

Gabon, the limited systematic value of petal aestivation was illustrated with reference to Uvarieae. This
tribe featured genera with both apocarpous (e.g.
Uvaria, Cleistopholis Pierre ex Engl.) and syncarpous
[Letestudoxa, Pachypodanthium Engl. & Diels (now
Duguetia)] fruits. In addition, substantial variation in
the number of ovules and placentation type occurs
within these seven genera. In effect, Uvarieae was
considered to be related only because of imbricate
petals and occasional stellate hairs. In this article, we
will limit ourselves to a few examples, such as that of
Uvarieae given here. Almost any past classification
can be justified to some extent, in that the responsible
author hypothesized a close relationship between particular genera, which, with hindsight, appears to have
been correct. However, in each case, there are also as
many (if not more) problems to be pointed out. We
consider that there is little point in evaluating in
detail these various classification schemes, as the
common methodological ground and explicit justification that are necessary to clarify or test the reasons
for differences between them are missing. They are all
highly intuitive and therefore irrefutable.
Students of Annonaceae in the 19th and most of the
20th century assembled impressive numbers of collections, observations and taxonomic papers, but
simply lacked the rigour of using any formal methodology to establish a classification. In reviewing
those leading up to that of Fries (1959), it does,
however, become apparent that a limited number of
key characters have consistently been used for infrafamilial classification. These can be summarized as
those concerning phyllotaxy, indument, inflorescence
position, sepal and petal aestivation, petal fusion,
shape and form, anther connective form, carpel fusion
and placentation.
Subsequent to Fries (1959), Annonaceae systematics has focused on a wider range of differing sources of
data and has generally involved a variety of more or
less formal methodologies. Walker (1971) used pollen
and, to a lesser extent, floral morphology and phytogeography. Following this pioneering work, Le
Thomas (1980, 1981), Le Thomas & Lugardon (1976)
and Walker (1971, 1972) assembled a comprehensive
overview of palynological characters of Annonaceae.
Although these data were largely novel, the analytical
approach was similar to that of several preceding
studies: observed similarities between Annonaceae,
on the one hand, and presumed primitive
angiosperms, extant and fossil, on the other, together
with assumed transformation series, were taken as a
primary guide to hypothesize relationships. In addition, Le Thomas (1980, 1981) based several decisions
on ancestral and derived pollen characters on presumed evolutionary trends (series), for instance from
27
Table 4. Overview of previous infrafamilial classifications of Annonaceae. Informal names given in inverted commas.
Lists of genera included in infrafamilial taxa are not comprehensive, and are restricted to major genera and generally to
names currently recognized
Publication
Taxa
Diagnostic characters (and key genera included)
Rafinesque (1815)
Subfamily Anonoideae Raf.

Subfamily Uvarioideae Raf.
Subfamily Xylopioideae Raf.
Monocarps fused (Annona)

Monocarps free, indehiscent (Guatteria, Melodorum, Porcelia and Uvaria)
Monocarps free, dehiscent (Xylopia)
Kosteletzky (1836)
Subfamily Anonoideae Raf.

Subfamily Monodorioideae Kostel.
Subfamily Uvarioideae Raf.
Monocarps many, fused (Annona)

Monocarps single, possibly fused (Monodora)
Monocarps many, free (Artabotrys, Polyalthia, Uvaria and Xylopia)
Reichenbach (1837)
Anonariae
Uvarieae (subgroup)
Bocageeae (subgroup)
Anoneae genuinae
(subgroup)
Cardiopetaleae
Guatterieae
Petals free; monocarps free or fused

Stamens many; monocarps free (Asimina, Porcelia and Xylopia)
Stamens 6, opposite the petals (Bocagea)
Stamens many; monocarps fused (Annona and Monodora)
Tribe Anoneae Endl.

Tribe Bocageeae Endl.
Tribe Xylopieae Endl.
Stamens many; ovules basal (Anaxagorea, Annona, Artabotrys, Duguetia

and Guatteria)
Stamens few; ovules ventral (Bocagea, Miliusa, Orophea and Popowia)
Stamens many; ovules ventral (Hexalobus, Polyalthia, Uvaria and Xylopia)
Tribe Anoneae Endl.
Monocarps fused (Annona)
Tribe Guatterieae Hook.f. & Thomson
Petals flat or basally slightly curved (Anaxagorea, Artabotrys, Cananga,

Cyathocalyx, Guatteria, Phaeanthus and Polyalthia)
Stamens loosely imbricate (Miliusa and Orophea)
Inner petals clawed (Goniothalamus, Mitrephora, Orophea and Popowia)
Petal aestivation imbricate (Sageraea, Stelechocarpus and Uvaria)
Inner petals thick, 3-angled (Melodorum and Xylopia)
Endlicher (1839)
Hooker & Thomson

(1855)*
Tribe
Tribe
Tribe
Tribe
Bentham (1863)
Miliuseae Hook.f. & Thomson

Mitrephoreae Hook.f. & Thomson
Uvarieae Hook.f. & Thomson
Xylopieae Endl.
Tribe Miliuseae Hook.f. & Thomson

Tribe Mitrephoreae Hook.f. & Thomson
Subtribe Eumitrephoreae Benth. &
Hook.f.
Subtribe Phaeantheae Benth. &
Hook.f.
Tribe Unoneae Benth. & Hook.f.
Tribe Uvarieae Hook.f. & Thomson

Baillon (1868)
Prantl (1891)
Tribe Anoneae Endl.

Subtribe Oxymitreae Baill.
Subtribe Rollinieae Baill.
Subtribe Unoneae Baill.
Subtribe Uvarieae Baill.
Subtribe Xylopieae Baill.
Tribe Eupomatieae Baill.
Tribe Monodoreae Baill.
Tribe Eupomatieae Baill.
Tribe Melodoreae Prantl
Tribe Mitrephoreae Hook.f. & Thomson
Petals basally fused (Hexalobus, Miliusa and Orophea)

Petals connivent or patent; monocarps single-seeded (Anaxagorea,
Artabotrys, Duguetia, Guatteria and Polyalthia)
Petals diverse; stamens loosely imbricate, connective dorsally conspicuously

or not enlarged (Alphonsea, Bocagea, Miliusa and Orophea)
Petals valvate, outer apert, inner connivent or connate
Inner petals shorter than outer or subequal, often basally clawed
(Goniothalamus, Mitrephora and Monodora)
Inner petals much larger than outer, erect (Cymbopetalum and
Phaeanthus)
Petals flat, slightly unequal or inner smaller than outer, generally apert
(Anaxagorea, Artabotrys, Asimina, Cananga, Cyathocalyx, Disepalum,
Polyalthia, Popowia, Hexalobus and Unona)
Petals flat, spreading, at least inner imbricate; stamens densely crowded,
connective apex enlarged (Duguetia, Guatteria, Porcelia, Sageraea,
Stelechocarpus and Uvaria)
Outer petals thick, connivent or slightly apert; inner petals enclosed, small
or absent (Annona, Melodorum and Xylopia)
(Cymbopetalum, Mitrephora, Orophea and Oxymitra)
(Artabotrys, Cyathocalyx, Hexalobus and Rollinia)
(Anaxagorea, Bocagea, Disepalum, Popowia and Unona)
(Cananga, Oxandra, Sageraea and Uvaria)
(Annona and Xylopia)
(Eupomatia)
(Miliusa and Phaeanthus)
(Monodora)
Perianth absent; perigynous (Eupomatia)
All or only inner petals erect, petals touching; stamens numerous;
apocarpous; hairs simple (Melodorum, Phaeanthus and Piptostigma)
Stamens connective apex not expanded over anthers; stamens few;
apocarpous; hairs simple (Alphonsea, Bocagea, Mezzettia, Miliusa,
Oxandra and Sageraea)
Inner petals usually clawed, apically connivent; stamens sometimes few;
apocarpous; flowers small (Mitrephora, Orophea and Popowia)
28
Table 4. Continued
Publication
Taxa
Diagnostic characters (and key genera included)
Tribe Monodoreae Baill.
Syncarpous, unilocular with parietal placentation; petals more or less

fused at base; valvate (Monodora)
Petals subequal, spreading or slightly converging; stamens numerous;
hairs simple (Anaxagorea, Cananga, Cymbopetalum, Disepalum,
Polyalthia and Unona)
At least outer petals imbricate, spreading or slightly erect; stamens
numerous (Asimina, Duguetia, Guatteria, Porcelia, Stelechocarpus and
Uvaria)
Petals spoon-shaped at base, more or less constricted above and then
spreading or laterally compressed (Annona, Artabotrys, Cyathocalyx,
Hexalobus and Xylopia)
Hutchinson (1923,
1964)
Subfamily Annonoideae Raf.


Subtribe Annonineae Hutch.
Subtribe Xylopiineae Hutch.
Subfamily Monodoroideae Kostel.

Fries (1959)
Subfamily Annonoideae Raf.

Tribe Tetramerantheae R.E.Fr.
Subfamily Monodoroideae Kostel.
Carpels free or fused into multilocular syncarp; stigmas erect (rarely

radiating)
Petals in one or two whorls, valvate; outer petals smaller than inner
(Cymbopetalum, Marsypopetalum, Miliusa, Orophea, Phaeanthus,
Piptostigma and Trivalvaria)
Petals in one or two whorls, valvate; outer petals subequal or larger than
inner
Carpels fused (Annona)
Carpels free or only slightly fused (Alphonsea, Anaxagorea, Artabotrys,
Asimina, Cyathocalyx, Dasymaschalon, Desmopsis, Desmos, Disepalum,
Drepananthus, Goniothalamus, Haplostichanthus, Hexalobus,
Hornschuchia, Meiogyne, Melodorum, Mezzettia, Mitrephora,
Monanthotaxis, Monocarpia, Orophea, Platymitra, Polyalthia, Popowia,
Unonopsis, Uvariastrum, Uvariopsis and Xylopia)
Petals in two whorls, both or inner imbricate; leaf indument stellate or
lepidote (Duguetia, Enicosanthum, Ephedranthus, Fusaea, Guatteria,
Malmea, Oxandra, Porcelia, Sageraea, Sapranthus, Stelechocarpus and
Uvaria)
Carpels fused into unilocular ovary, placentation parietal; stigmas
radiating (Isolona and Monodora)
Carpels spirally arranged (sometimes few in a whorl); apocarpous, rarely
syncarpous (forming multilocular syncarp)
Petals in whorls of four, imbricate; stigma 3-lobed, appressed to ovary;
leaves spirally arranged (Tetrameranthus)
Petals (at least outer) valvate (imbricate in Porcelia); leaves distichous
(Alphonsea, Anaxagorea, Annona, Anonidium, Artabotrys, Cananga,
Cyathocalyx, Cymbopetalum, Dasymaschalon, Desmos, Disepalum,
Drepananthus, Fissistigma, Goniothalamus, Marsypopetalum,
Meiocarpidium, Meiogyne, Mezzettia, Miliusa, Mitrephora,
Monanthotaxis, Monocarpia, Neostenanthera, Onychopetalum, Orophea,
Phaeanthus, Piptostigma, Polyalthia, Polyceratocarpus, Popowia,
Porcelia, Pseuduvaria, Sphaerocoryne, Trigynaea, Trivalvaria, Unonopsis,
Uvariastrum, Uvariodendron, Uvariopsis and Xylopia)
Petals imbricate; leaves distichous (Asimina, Cleistopholis,
Cremastosperma, Desmopsis, Duguetia, Enicosanthum, Ephedranthus,
Fusaea, Guatteria, Hexalobus, Malmea, Oxandra, Pseudoxandra,
Sageraea, Sapranthus, Stelechocarpus, Stenanona and Uvaria)
Carpels whorled, fused in unilocular ovary, placentation parietal (Isolona
and Monodora)
*Partial study, geographically focused on taxa from British India.

Listed as tribe Saccopetaleae (Hooker & Thomson, 1855: pp. 91, 92).
Similar infrafamilial classification adopted by Hooker & Thomson (1872), although without recognition of subtribes within tribe
Mitrephoreae.
Descriptions not provided for tribes and subtribes, although with extensive descriptions of genera included.
Now excluded from Annonaceae as Eupomatiaceae.

simple to complex characters or from free to fused
parts, and on an analogy between morphological
series in pollen characters and macromorphological
characters. Although Le Thomas (1980, 1981) mentioned the concepts of homology and convergent
evolution, she lacked the analytical tools to demonstrate the significant levels of homoplasy that
have since been demonstrated (Doyle & Le Thomas,
2012). Noteworthy contributions to the classification
of Annonaceae (van Heusden, 1992; van Setten &
Koek-Noorman, 1992) appeared immediately before
the first cladistic papers (Doyle & Le Thomas, 1994,
1995), allowing the last two publications to benefit
from the comprehensive overviews of floral morphology (van Heusden, 1992) and fruit and seed
morphology (van Setten & Koek-Noorman, 1992).
Observations that led to intuitive groupings of
genera in each of these publications separately
were combined and used for a phenetic analysis
(Koek-Noorman, van Setten & van Zuilen, 1997).
Koek-Noorman et al. (1997) used a neighbor-joining
tree derived from these data to produce an informal
classification (grouping) that was similar to that of
van Setten & Koek-Noorman (1992). In a few cases,
particular results from the neighbor-joining tree were
disregarded in the classification, for example, in the
case of Porcelia Ruiz & Pav.: established opinion
based on inflorescence type, anther septation and
pollen size was that the genus was allied to the other
genera in Bocageeae (Fig. 1B), but, in the analysis of
Koek-Noorman et al. (1997), it was clustered distant
from its putative close relatives, possibly as a result of
the absence of a seed appendage, either an aril or a
caruncle (Johnson & Murray, 1995), that is otherwise
present in all species of Bocageeae.
The first formal cladistic analyses based on morphological, anatomical and palynological characters
revealed rampant homoplasy. The consistency index
of 79 characters scored for 42 genera of Annonaceae
was as low as 0.27 in Doyle & Le Thomas (1996). The
retention index was not reported, but, as autapomorphies were absent and the number of symplesiomorphies was low, the proportion of similarity in their
tree to be interpreted as synapomorphies is also likely
to have been low. There are several reasons for this
high level of homoplasy, one of which is the difficulty
of homology assessment, as acknowledged by Doyle &
Le Thomas (1996), in cases in which observations on
living material were absent and characters were
scored on the basis of observations of herbarium
material (e.g. petal connivence, fruit wall thickness).
Moreover, some characters were included that have
been shown to be derived via different developmental
pathways. Because of the lack of similarity in
anatomy and development, it comes as no surprise
that these characters were demonstrated by Doyle &
29
Le Thomas (1996) to be homoplasious. An example of

such a character is syncarpous fruits, as opposed to
those consisting of free monocarps. Several papers
have demonstrated that syncarpy can better be interpreted as different, nonhomologous, suites of characters related to fusion or coherence between carpels,
fusion or coherence between carpels and receptacle,
and syncarpy in flowering stage (Briechle-Mck,
1994; Chatrou & He, 1999; Chatrou et al., 2000; Couvreur et al., 2008). Finally, part of the homoplasy as
found by Doyle & Le Thomas (1996) can be explained
by patterns apparent in their family-wide analysis. In
many cases, homoplasy was not distributed evenly
across the tree. This can be illustrated by the fact
that similar characters, when used in phylogenetic
analyses of morphological characters of clades within
Annonaceae (Johnson & Murray, 1995; Chatrou et al.,
2000), showed little to no homoplasy. Examples are
the occurrence of different trichome types, lianescent
habit and presence vs. absence of styles in the clade
comprising Duguetia and related genera (Chatrou
et al., 2000), and the occurrence of bilobed arils and
different shapes of the floral receptacle in Bocageeae
(Johnson & Murray, 1995). These characters do not
exhibit homoplasy in these relatively small, more
exclusive clades, but have all evolved in parallel
multiple times in Annonaceae as a whole.
A NEW INFRAFAMILIAL CLASSIFICATION

OF ANNONACEAE
Because classifications are important for communication and information retrieval, stability and universal
applicability should be their main features. Previous
classifications of Annonaceae, to a large extent, fail to
meet both criteria.
We assign the rank of subfamily to four clades:
Anaxagorea (Anaxagoreoideae); clade C (Ambavioideae), corresponding to the clade previously referred
to informally as the ambavioids (e.g. Doyle & Le
Thomas, 1994, 1995, 1996; Doyle et al., 2000; Sauquet
et al., 2003); clade E (Annonoideae), the LBC or inaperturate clade (e.g. Richardson et al., 2004; Erkens
et al., 2007; Couvreur et al., 2008; Zhou et al., 2009);
and clade F (Malmeoideae), the SBC or malmeoid/
piptostigmoid/miliusoid clade (e.g. Richardson et al.,
2004; Pirie et al., 2006). These four clades include all
the genera sampled for these analyses (i.e. 90% of all
accepted genera).
Clade E, which includes the genus Annona, must be
assigned the name Annonoideae Raf. (McNeill et al.,
2006; art. 19.4). All other previously described subfamilies of Annonaceae are based on names of genera
that belong to Annonoideae, namely Bocageoideae
Pfeiff., Monodoroideae Kostel., Uvarioideae Raf. and
30
Xylopioideae Raf., and are therefore all superfluous.

The somewhat curious bias towards subfamilies
based exclusively on annonoid genera can be
explained by their greater morphological variability
(particularly in fruit characters). In the absence of
further available subfamilial names, Anaxagoreoideae, Ambavioideae and Malmeoideae are newly
described here.
As with all recent classificatory endeavours in
angiosperms (e.g. APG III, 2009), strongly supported
monophyly is the foremost principle, at any taxonomic level. For our classification of Annonaceae, this
is also true. Monophyly is the only characteristic that
these subfamilies have in common, however: they are
not otherwise equivalent in terms of age, geographical
distribution or any other biological attributes (and
should not be expected to be so). Following monophyly, morphological diagnosability is an important
subsidiary criterion for the classification of groups,
which, in this case, is challenging. As stated above,
clear morphological synapomorphies have yet to be
identified for most clades of Annonaceae. However, we
do not believe that this should prevent us from recognizing infrafamilial taxa, especially because the use
of different terms for the same clades, as mentioned
above, is likely to cause misunderstanding (APG I,
1998). The plethora of informally named groups
resulting from the classifications proposed to date
demonstrates the need for named units within the
family. Furthermore, there are many characters
awaiting evaluation for their diagnostic value; two
recently published examples of characters that have a
good, although not perfect, fit onto the phylogenetic
tree for Annonaceae are phyllotaxis (Johnson, 2003)
and orbicules (Huysmans et al., 2010).
The need to identify clades and to name them
extends beyond the level of subfamilies. A comprehensive classification of Annonaceae recognizes further
taxa at lower, namely tribal, ranks. Characters that
are diagnostic for these less inclusive clades are more
straightforward to identify than for the four subfamilies. Nevertheless, extensive homoplasy still makes
the diagnosis of tribes only possible by the enumeration of a suite of characters that individually are
found in several clades (i.e. that are individually
homoplasious). Some useful characters include phyllotaxis (distichous phyllotaxis is shared by members
of clade L), habit (a climbing habit is common to
species of clade Q, although with exceptions, e.g. in
most species of Dasymaschalon (Hook.f. & Thomson)
Dalla Torre & Harms: Wang, Chalermglin & Saunders, 2009) and pollen characters (clade R is characterized by cryptoaperturate/disulculate pollen grains;
T. Chaowasku et al., unpubl. data). The phylogenetic
tree presented here includes some poorly resolved
clades, but the lack of resolution does not prevent
formal classification at the tribal level. The composition of taxa at lower ranks, such as tribes, has frequently changed, and they have rarely been used in
formal classifications. Fries (1959) named only three
tribes in his classification of the family: Uvarieae,
Unoneae and Tetramerantheae. Of these, Tetramerantheae included the ambavioid genus Tetrameranthus R.E.Fr. only. Uvarieae and Unoneae, by contrast,
included genera dispersed across Annonoideae,
Malmeoideae and Ambavioideae as circumscribed
here. A more recent revision and recircumscription of
Saccopetaleae (Keler, 1988) also resulted in a nonmonophyletic group of genera (this study; T. Chaowasku et al., unpubl. data). As many clades are well
supported, it makes sense to recognize them formally,
and thus, in addition to the naming of subfamilies, we
provide a set of tribes in order to avoid adding further
disorder to the classification of Annonaceae.
Eupomatia R.Br., containing three species, has previously been included in Annonaceae (Bentham, 1863;
Baillon, 1868; Prantl, 1891; Diels, 1912), usually in
its own tribe: Eupomatieae Baill. Subsequent precladistic classifications (e.g. Hutchinson, 1973;
Cronquist, 1988; Takhtajan, 1997) always considered
Eupomatiaceae to be a separate family from Annonaceae. Given this classificatory history and the fact
we are presenting a new classification of Annonaceae,
the classification of Eupomatia needs to be addressed
here. Eupomatia has been shown to be sister to
Annonaceae in several phylogenetic analyses of
angiosperms (e.g. Qiu et al., 2005) and Magnoliales
(Sauquet et al., 2003). Therefore, both recognition and
rejection of familial status for Eupomatia would be in
agreement with the principle of monophyly. Despite
the annonaceous appearance of Eupomatia, there are
hardly any characters that are synapomorphic for
Annonaceae and Eupomatia combined. Sauquet et al.
(2003) only listed fibrous mesotesta as a possible
synapomorphy. The similarities between Annonaceae
and Eupomatia are often symplesiomorphies as
they are shared with the sister clade of Annonaceae/
Eupomatia, consisting of Himantandraceae and
Degeneriaceae. These characters include adaxial prophylls, a flat-concave floral receptacle, apical extension of the connective and testal ruminations (Doyle
& Le Thomas, 1997; Endress & Doyle, 2009; Endress
& Armstrong, 2011). Furthermore, the clearest
synapomorphies of Annonaceae (that is, characters
showing no or hardly any homoplasy) are not shared
with Eupomatia. Despite considerable variation in
floral morphology (Xu & Ronse De Craene, 2010),
the floral bauplan of Annonaceae is uniform
(Saunders, 2010) and provides several synapomorphies (Endress & Armstrong, 2011), such as a whorled
floral phyllotaxis (vs. spiral in Eupomatiaceae),
plicate carpels (vs. ascidiate carpels) and trimerous

perianth (vs. many tepals). The broad and high multiseriate xylem rays with many narrow, tangential
parenchyma bands perpendicular to the xylem rays is
a typical wood anatomical feature characterizing
every species of Annonaceae investigated so far
(Koek-Noorman & Westra, 2012). This wood structure is absent in Eupomatia (L. Y. T. Westra &
L. W. Chatrou, pers. observ.; http://insidewood.lib.
ncsu.edu). Given the character distribution described
here, we do not favour the inclusion of Eupomatia in
Annonaceae and leave it out of the classification presented here.
Because subfamily Anaxagoreoideae consists of
Anaxagorea only, we feel that it would be taxonomically redundant to also recognize this clade at the
tribal level. Subfamily Ambavioideae comprises nine
genera and just over 50 species. To split this subfamily
further into tribes would involve the recognition of
three tribes, consisting of Meiocarpidium, the clade
containing Cananga (DC.) Hook.f. & Thomson, and the
clade containing Ambavia Le Thomas, respectively.
Apart from creating undesirably species-poor tribes,
this alternative would focus on differences between the
three groups, such as the basic chromosome number
x = 7 for the Canaga clade and x = 8 for the Ambavia
clade. In order to avoid insoluble debates about the
level of morphological difference required for a clade to
be recognized as a classificatory unit, not just in
Ambavioideae but in other subfamilies as well, we
focus on synapomorphies recognizing clades that are
as inclusive as possible. In the case of Ambavioideae,
these are the presence of a middle integument (Christmann, 1989) and some palynological synapomorphies
(Doyle & Le Thomas, 2012).
Parts of the tree for Annonaceae that require additional sampling of taxa and character include the
relationships among species-rich clades in Annonoideae (clades I, J, K and L). We argue that these
species-rich clades can be given tribal status without
their interrelationships being fully resolved. The
clades are morphologically distinct and, to a large
extent, they have been recognized in the past as
groups of related genera. An exception is the clade
comprising Artabotrys and Xylopia, for which clear
synapomorphies have yet to be identified.
The clade that would require much better resolution before any classificatory conclusion can be drawn
is clade X, containing most Asian and Central American endemic genera in Malmeoideae. Sequence divergence is low among species in this clade and, as a
result, support is low in general. So far, our knowledge of phylogenetic relationships is based on only
one-eighth of the species in clade X. An advantageous
strategy would seem to be to increase taxon sampling,
as this would provide a more accurate estimation of
phylogenetic model parameters (Heath, Hedtke &
31
Hillis, 2008). In the light of this, we recircumscribe

tribe Miliuseae (clade X excluding Monocarpia) and
envisage that its classification be revisited once relationships are better resolved. The inclusion of the
genus Monocarpia in Miliuseae would have been possible from the perspective of monophyly; we prefer,
however, to erect a new tribe for Monocarpia alone as
this genus has never previously been included in
Miliuseae (Mols & Keler, 2003; Mols et al., 2004).
Monocarpia furthermore lacks cryptoaperturate/
disulculate pollen, which is synapomorphic for Miliuseae as circumscribed here (Chaowasku, Keler &
van der Ham, 2012). Relationships among clades V, W
and X are unresolved. We apply a similar reasoning
here as for clades I, J, K and L in Annonoideae: the
lack of interclade resolution does not hinder the recognition of tribes, which are morphologically distinct.
Saunders et al. (2011) demonstrated that the Malagasy genus Fenerivia Diels, unsampled in this study,
is part of this polytomy. Hence, clades V, W, X and
Fenerivia are given tribal status. Furthermore, we
classify the genus Dendrokingstonia Rauschert in
tribe Dendrokingstonieae, in accordance with results
of phylogenetic analyses (Chaowasku et al., 2012). In
doing so, we assign all genera of Annonaceae without
exception to a tribe.
Considering the nomenclature of tribes, the principle has been adopted that published names of
tribes, based on a generic name, are assigned to
clades containing that genus. To a large extent, we
could use tribal names that have been published
before, using the oldest names that apply to clades in
our tree. Names that have become superfluous are
Tetramerantheae R.E.Fr., Melodoreae Prantl, Mitrephoreae Hook.f. & Thomson and Unoneae Benth. &
Hook.f. Six new tribes need to be described as none of
the existing names could be applied.
The macromorphological characters most frequently
emphasized in classifications of Annonaceae concern
the form of the fruit, inflorescence position, and shape
and aestivation of the sepals and petals. Some are
demonstrably nonhomologous, such as syncarpous
fruits (as discussed above). The primary homology of
further historically important characters, such as
numbers of carpels, numbers of ovules per carpel,
fusion of petals, and shape and insertion of petals, can
best be tested in the light of our tree. We have not
attempted a formal character analysis here. It is,
however, clear from the phylogenetic relationships
presented here that historically important characters
do not consistently characterize major clades. Indeed,
it is not obvious which, if any, individual traits might
be interpreted as unequivocal diagnostic characters for
more inclusive clades. In our description of subfamilies
and tribes, we document what we see as suites of
characters most useful for broadly defining clades.
32
These characters have been taken from our own observations and those of Maas & Westra (1984), Westra
(1985), Morawetz & Le Thomas (1988), van Heusden
(1992), van Setten & Koek-Noorman (1992), Johnson &
Murray (1995), Doyle & Le Thomas (1996), Svoma
(1998), Johnson (2003), Maas, Westra & Chatrou
(2003), Tsou & Johnson (2003), Scharaschkin & Doyle
(2005, 2006), Su & Saunders (2006), Maas, Westra
&Vermeer (2007), Couvreur (2009), Huysmans et al.
(2010), Surveswaran et al. (2010) and Weerasooriya &
Saunders (2010).
Anaxagoreoideae Chatrou, Pirie, Erkens
& Couvreur, subfam. nov.TYPE:
Anaxagorea A.St.-Hil.
Trees with distichous phyllotaxis; hermaphroditic;
carpels free in flower and fruit; stamen apex pointed
or rounded; connective extension anthers nonseptate;
inner staminodes present; orbicules present; ovules
two (basal); monocarp abscission at base of stipe;
monocarps ventrally dehiscent; seeds not arillate,
asymmetrical; middle seed integument absent; basic
chromosome number x = 8.
Included genus: Anaxagorea.
Ambavioideae Chatrou, Pirie, Erkens & Couvreur,
subfam. nov.TYPE: Ambavia Le Thomas
Trees with spiral or distichous phyllotaxis; hermaphroditic; carpels free in flower and fruit; apical connective prolongation tongue-shaped, peltate-apiculate or
peltate-truncate; anthers nonseptate; staminodes
absent; ovules twonumerous (lateral); orbicules
present; monocarp abscission at apex or base of stipe;
monocarps indehiscent; seeds sometimes arillate,
symmetrical; middle seed integument usually
present; endosperm ruminations irregular; basic chromosome number x = 7 or 8.
Included genera: Ambavia, Cananga, Cleistopholis,
Cyathocalyx Champ. ex Hook.f. & Thomson, Drepananthus Maingay ex Hook.f., Lettowianthus Diels,
Meiocarpidium, Mezzettia Becc., Tetrameranthus.
A synapomorphy for this clade is a middle integument (Christmann, 1989; Svoma, 1998; Lucas et al.,
2012).
Annonoideae Raf., Anal. Nat. 175., AprJul 1815
(Annonidia), descr. emend.TYPE: Annona L.
Trees or lianas with spiral or distichous phyllotaxis;
hermaphroditic, sometimes (andro)dioecious, rarely
(andro)monoecious; carpels free or fused in flower and
fruit; ovules one (basal, rarely apical) to numerous
(lateral); apical connective prolongation peltatetruncate, peltate-apiculate, rarely tongue-shaped
or absent; anthers septate or nonseptate; outer staminodes rarely present; orbicules usually absent;
monocarps indehiscent or dehiscent (adaxially or
abaxially); seeds sometimes arillate, symmetrical;

middle seed integument absent (only present in Artabotrys); endosperm ruminations usually lamelliform,
sometimes irregular; basic chromosome number x = 7,
8 or 9.
Although Bocagea A.St.-Hil., Cardiopetalum
Schltdl. and Froesiodendron R.E.Fr. have not been
sampled for our phylogenetic analyses, we believe
their inclusion in Annonoideae is warranted. Together
with Cymbopetalum Benth., Mkilua Verdc., Porcelia
and Trigynaea Schltdl., these genera belong to Bocageeae, which are clearly set apart from other Annonaceae by a combination of inflorescence, pollen and
seed characters (Johnson & Murray, 1995). The inflorescence is an internodal pedicel that is articulated at
the base (Murray, 1993; Johnson & Murray, 1995).
The lack of bracts, below and above the articulation,
precludes sympodial growth of the inflorescence and,
as a consequence, the flowers are solitary. Like solitary flowers, columellar polyads (Johnson & Murray,
1995; Tsou & Fu, 2007; Doyle & Le Thomas, 2012)
only occur in this clade of Annonaceae, and therefore
are clear synapomorphies. Bilobed arils (Murray,
1993; Johnson & Murray, 1995) are an additional
feature characteristic of the genera in clade G, even
though these are also present in Asimina, Xylopia
and Cananga. Given that these three characters occur
in the three unsampled genera, they are included
here.
The unsampled genus Afroguatteria Boutique is
also included in Annonoideae. This genus of two
species has not been included in any molecular phylogenetic analysis. However, in a morphological cladistic analysis by Doyle & Le Thomas (1996), it was
found to be in a clade of climbers that corresponds to
clade O in our analyses. Species of Afroguatteria are
climbers, which, on its own, merits inclusion in
Annonoideae. The many-seeded apocarpous fruits,
valvate sepals and imbricate petals could indicate a
close relationship between Afroguatteria and Uvaria.
A climbing habit also supports the addition of two
monotypic African genera, Exellia Boutique and Gilbertiella Boutique, to Annonoideae. These two genera
have habitually been treated as Monanthotaxis s.l.,
based on pollen and flower morphology (Le Thomas,
1969; Le Thomas & Doyle, 1996). Bygrave (2000)
included Exellia scamnopetala (Exell) Boutique in his
phylogenetic analysis of rbcL sequences of Annonaceae, which placed it in an unresolved position in a
clade of climbing taxa, compatible with our clade O.
We were, however, unable to obtain that rbcL
sequence.
Cleistochlamys Oliv. is a third monotypic genus
that has been associated with Monanthotaxis (in this
case, Popowia Endl.; Verdcourt, 1971). Its facultative
climbing habit and association with Hexalobus A.DC.

and other annonoid genera based on pollen characters (Walker, 1971) underpin its incorporation in
Annonoideae.
Despite its absence in our phylogenetic analyses,
the monotypic African genus Boutiquea Le Thomas is
placed in Annonoideae, based on palynological characters. Boutiquea has pollen tetrads, with a granular
infratectum similar to Neostenanthera (Le Thomas,
1980; Doyle & Le Thomas, 2012). Pollen characters
are also among the characters to support inclusion of
Duckeanthus R.E.Fr. in Annonoideae. Pollen of this
relatively poorly known monotypic genus bears strong
resemblance to that of Fusaea in having large tetrads
with a minutely granular exine structure (Walker,
1971; Le Thomas, Lugardon & Doyle, 1994; Doyle &
Le Thomas, 2012). Moreover, Fusaea and Duckeanthus share characters of inflorescences, stamen
anatomy and aril structure, which made them appear
as sister genera in a morphological cladistic analysis
(Chatrou et al., 2000). The only genus we include in
our classification without reference to published data
is Schefferomitra Diels. Just before submitting this
paper, sequence data became available (PhD project
of S. Meinke), showing affiliation of this monotypic
genus with clade R in our analyses.
The genus Diclinanona Diels was shown to belong
to Malmeoideae (Erkens et al., 2009). Because of suspicion of a mixed origin of the available sequence data
of Diclinanona, T. Chaowasku et al. (unpubl. data)
extracted and sequenced Diclinanona again, and
showed it to belong to Annonoideae, confirming the
phylogenetic position found by Richardson et al.
(2004), and congruent with the absence of orbicules
(Huysmans et al., 2010).
CIRCUMSCRIPTION
OF TRIBES IN
ANNONOIDEAE
Bocageeae Endl., Gen. Pl.: 830, Jun 1839TYPE:

Bocagea A.St.-Hil.
Trees with spiral phyllotaxis; indument of simple
hairs; bracts absent; flowers solitary, terminal,
bisexual; carpels free in flower and fruit; placentation
lateral, uni- or biseriate; monocarp abscission at base
of stipe; aril bilobed, rarely absent; ruminations
lamelliform; pollen inaperturate.
Included genera: Bocagea, Cardiopetalum, Cymbopetalum, Froesiodendron, Hornschuchia, Mkilua, Porcelia, Trigynaea.
This tribe is equivalent to clade G (Fig. 1B).
Xylopieae Endl., Gen. Pl.: 831, Jun 1839TYPE:
Xylopia L.
Trees or lianas with spiral phyllotaxis; indument of
simple hairs; bracts present; inflorescences rhipidiate,
terminal or axillary; flowers bisexual; carpels free in
flower and fruit; placentation basal or lateral and
33
uniseriate; monocarp abscission at base of stipe; aril

absent, rudimentary or bilobed; ruminations spiniform to lamelliform; pollen inaperturate or sulcate.
Included genera: Artabotrys, Xylopia.
This tribe is equivalent to clade I (Fig. 1B).
Duguetieae Chatrou & R.M.K.Saunders, tribus
nov.TYPE: Duguetia A.St.-Hil.
Trees, sometimes lianas, with spiral phyllotaxis;
indument of lepidote, stellate and/or simple hairs;
bracts present; inflorescences rhipidiate, terminal;
flowers bisexual; carpels free in flower, in fruit
usually fused; placentation basal; stipe absent; aril
rudimentary, rarely absent; ruminations lamelliform;
pollen inaperturate, sometimes sulculate.
Included genera: Duckeanthus, Duguetia, Fusaea,
Letestudoxa, Pseudartabotrys.
This tribe is equivalent to clade J (Fig. 1B).
Guatterieae Hook.f. & Thomson, Fl. Ind. 1: 92,
126, Jul 1855TYPE: Guatteria Ruiz & Pav.
Trees, phyllotaxis unknown; indument of simple hairs;
bracts present; inflorescences rhipidiate, axillary,
rarely terminal; flowers bisexual; carpels free in flower
and fruit; placentation basal; monocarp abscission at
base of stipe; aril absent or rudimentary; ruminations
spiniform to lamelliform; pollen sulculate.
Included genus: Guatteria.
This tribe is equivalent to clade K (Fig. 1B).
Annoneae Endl., Gen. Pl.: 833, Jun 1839
TYPE: Annona R.E.Fr.
Trees with distichous phyllotaxis; indument of
simple hairs, rarely stellate hairs; bracts present;
inflorescences rhipidiate, terminal or axillary;
flowers bisexual, sometimes (andro)dioecious; carpels
free in flower, free or fused in fruit; placentation
basal or lateral and uni- or biseriate; monocarp
abscission at base of stipe, sometimes at apex, or
stipe absent; aril bilobed, rudimentary or absent;
ruminations spiniform, irregular pegs or lamelliform;
pollen inaperturate.
Included genera: Annona, Anonidium, Asimina,
Boutiquea, Diclinanona, Disepalum, Goniothalamus,
Neostenanthera.
This tribe is equivalent to clade M (Fig. 1B).
Monodoreae Baill., Hist. Pl. 1: 263, 288. AugDec
1868TYPE: Monodora Dunal.
Trees with distichous phyllotaxis; indument of simple
hairs; bracts present; inflorescences rhipidiate, terminal or axillary; flowers bisexual, sometimes dioecious;
carpels free or fused in flower, free or fused in fruit;
placentation parietal, or lateral and uni- or biseri-
34
ate; monocarp abscission at base of stipe, or stipe

absent; aril absent; ruminations lamelliform; pollen
inaperturate.
Included genera: Asteranthe Engl. & Diels, Hexalobus, Isolona Engl., Mischogyne Exell, Monocyclanthus
Keay, Monodora Dunal, Ophrypetalum, Sanrafaelia,
Uvariastrum Engl., Uvariodendron (Engl. & Diels)
R.E.Fr., Uvariopsis Engl.
This tribe is equivalent to clade O plus clade P
(Fig. 1B).
appeared to be of mixed origin; the generic name was

therefore never formally reduced to synonymy with
Meiogyne. Okada (1996) subsequently described Oncodostigma microflorum H.Okada, in effect revitalizing
the generic name. The taxonomy of Oncodostigma
needs further clarification and, for now, we list the
name in our classification. Fitzalania F.Muell. has
been accommodated here even though a proposal has
been published to give priority to the name Meiogyne
(Chaowasku, Zijlstra & Chatrou, 2011).
Uvarieae Hook.f. & Thomson, Fl. Ind. 1: 91, 92.

119 Jul 1855TYPE: Uvaria L.
Lianas, rarely trees, with distichous phyllotaxis;
indument of stellate, sometimes simple hairs; bracts
present; inflorescences rhipidiate, terminal or axillary; flowers bisexual; carpels free in flower and fruit;
placentation basal, or lateral and uni- or biseriate;
monocarp abscission at base of stipe; aril rudimentary
or absent; ruminations lamelliform; pollen inaperturate; sometimes sulculate.
Included genera: Afroguatteria, Cleistochlamys,
Dasymaschalon, Desmos Lour., Dielsiothamnus
R.E.Fr., Exellia, Fissistigma Griff., Friesodielsia, Gilbertiella, Melodorum Lour., Monanthotaxis, Pyramidanthe Miq., Schefferomitra, Sphaerocoryne (Boerl.)
Scheff. ex Ridl., Toussaintia, Uvaria.
This tribe is equivalent to clade Q (Fig. 1B).
Piptostigmateae Chatrou & R.M.K.Saunders,

tribus nov.TYPE: Piptostigma Oliv.
Trees; indument of simple hairs; bracts present; inflorescences rhipidiate, terminal or axillary; flowers
bisexual or androdioecious; carpels free in flower and
fruit; placentation basal or lateral and uni- or biseriate; monocarp abscission at base or apex of stipe; aril
absent; ruminations spiniform, sometimes irregular
pegs; endosperm glass-like; pollen monosulcate.
Included genera: Annickia Setten & Maas, Greenwayodendron Verdc., Mwasumbia Couvreur &
D.M.Johnson, Piptostigma, Polyceratocarpus Engl. &
Diels.
This tribe is equivalent to clade T (Fig. 1C).
Malmeoideae Chatrou, Pirie, Erkens & Couvreur,

subfam. nov.TYPE: Malmea R.E.Fr.
Trees with spiral phyllotaxis; hermaphroditic, sometimes (andro)dioecious, rarely (andro)monoecious;
carpels free in flower and fruit; apical connective
prolongation
peltate-truncate,
peltate-apiculate,
tongue-shaped or absent; anthers nonseptate; outer
staminodes rarely present; ovules one to numerous
(basal or lateral, rarely apical); orbicules usually
present; monocarps indehiscent; seeds not arillate,
symmetrical; middle seed integument absent;
endosperm ruminations usually spiniform, sometimes
lamelliform or irregular; basic chromosome number
x = 8 or 9.
Dendrokingstonia
Rauschert
is
placed
in
Malmeoideae even though we did not include it in our
analyses. Analyses by Chaowasku et al. (2012) put it in
this subfamily, in a moderately supported position
sister to clade X (Fig. 1C). The genus Fenerivia is
absent from our analyses. Ten species that were until
recently included in Polyalthia have been transferred
to Fenerivia by Saunders et al. (2011). Oncodostigma
Diels is included in Malmeoideae, but it may not be
worthy of recognition: van Heusden (1994) brought the
then recognized Oncodostigma spp. into synonymy
under Meiogyne Miq., but treated the type species
O. leptoneura Diels as a dubious name as the holotype
CIRCUMSCRIPTION
OF TRIBES IN
MALMEOIDEAE
Malmeeae Chatrou & R.M.K.Saunders, tribus

nov.TYPE: Malmea R.E.Fr.
Trees; indument of simple hairs; bracts present; inflorescences rhipidiate, terminal or axillary; flowers
bisexual or androdioecious; carpels free in flower and
fruit; placentation basal, rarely lateral; monocarp
abscission at base of stipe; aril absent; ruminations
spiniform, irregular pegs or lamelliform; endosperm
glass-like or soft; pollen monosulcate.
Included genera: Bocageopsis R.E.Fr., Cremastosperma R.E.Fr., Ephedranthus S.Moore, Klarobelia
Chatrou, Malmea, Mosannona Chatrou, Onychopetalum R.E.Fr., Oxandra A.Rich., Pseudephedranthus
Aristeg., Pseudomalmea Chatrou, Pseudoxandra
R.E.Fr., Ruizodendron R.E.Fr., Unonopsis R.E.Fr..
This tribe is equivalent to clade V (Fig. 1C).
Maasieae Chatrou & R.M.K.Saunders, tribus
nov.TYPE: Maasia Mols, Keler & Rogstad
Trees; indument of simple hairs; bracts present; inflorescences rhipidiate, axillary; flowers bisexual;
carpels free in flower and fruit; placentation basal,
rarely ventral; monocarp abscission at base of stipe;
aril absent; ruminations spiniform; endosperm glasslike; pollen monosulcate.
Included genus: Maasia.
This tribe is equivalent to clade W (Fig. 1C).

Fenerivieae Chatrou & R.M.K.Saunders, tribus
nov.TYPE: Fenerivia Diels.
Trees; indument of simple hairs; bracts present;
flowers solitary, axillary, bisexual; carpels free in
flower and fruit; placentation basal; monocarp abscission at base of stipe; aril absent; ruminations spiniform; endosperm glass-like; pollen monosulcate.
Included genus: Fenerivia.
This tribe is not represented in our analyses. Monophyly of Fenerivia has been demonstrated by Saunders et al. (2011), who also found a polytomy
comprising the tribes Malmeeae, Maasieae, Monocarpieae together with Miliuseae, and Fenerivieae.
This result is confirmed by T. Chaowasku et al.
(unpubl. data).
Dendrokingstonieae Chatrou & R.M.K.Saunders,
tribus nov.TYPE: Dendrokingstonia Rauschert.
Trees; indument of simple, rarely stellate, hairs;
bracts present; inflorescences rhipidiate, axillary, or
flowers solitary; flowers bisexual; carpels free in
flower and fruit; placentation lateral, uni- or biseriate; monocarp abscission at base of stipe; aril absent;
ruminations lamelliform; endosperm soft; pollen
monosulcate.
Included genus: Dendrokingstonia.
Monocarpieae Chatrou & R.M.K.Saunders, tribus
nov.TYPE: Monocarpia Miq.
Trees; indument of simple hairs; bracts present; inflorescences rhipidiate, terminal; flowers bisexual;
carpels free in flower and fruit; placentation lateral;
monocarp abscission at base of stipe; aril absent;
ruminations spiniform; endosperm glass-like; pollen
monosulcate.
Included genus: Monocarpia.
Miliuseae Hook.f. & Thomson, Fl. Ind. 1: 147. 119
Jul 1855TYPE: Miliusa Lesch. ex A.DC.
Trees; indument of simple hairs, rarely T-shaped
hairs; bracts present; inflorescences rhipidiate, terminal or axillary, flowers rarely solitary; flowers
bisexual or (andro)dioecious, rarely monoecious;
carpels free in flower and fruit; placentation basal or
lateral; monocarp abscission at base of stipe; aril
absent; ruminations spiniform, irregular pegs or
lamelliform; endosperm soft or glass-like; pollen
cryptoaperturate/disulculate.
Included genera: Alphonsea Hook.f. & Thomson,
Desmopsis, Enicosanthum Becc., Fitzalania, Haplostichanthus
F.Muell.,
Marsypopetalum
Scheff.,
Meiogyne, Miliusa, Mitrephora (Blume) Hook.f. &
Thomson, Neo-uvaria Airy Shaw, Oncodostigma,
Orophea Blume, Phaeanthus Hook.f. & Thomson,
Phoenicanthus Alston, Platymitra Boerl., Polyalthia,
Popowia, Pseuduvaria Miq., Sageraea Dalzell,
35
Sapranthus, Stelechocarpus (Blume) Hook.f. &

Thomson, Stenanona, Tridimeris, Trivalvaria (Miq.)
Miq., Woodiellantha Rauschert.
This tribe is equivalent to clade X excluding Monocarpia (Fig. 1C).
CONCLUSIONS
The phylogenetic tree presented here represents a
significant improvement in both the generic representation and resolution when compared with previous
work on Annonaceae. Previous informal classifications failed to find general acceptance and were
unstable with the addition of new data or the application of different methods of analysis. The knowledge of the phylogenetics of Annonaceae has now
reached the point at which it is possible to define a
formal classification, with the four subfamilies and 14
tribes treated here, which is likely to be stable in the
face of new data. Such a classification is warranted as
an aid to communication in this important and widely
distributed tropical plant family.
ACKNOWLEDGEMENTS
We gratefully acknowledge critical comments by Gea
Zijlstra and Tanawat Chaowasku on an earlier draft,
translations of Latin and German literature by
Lubbert Westra and Daniel Thomas, respectively, and
editorial support from Mike Fay and Hassan Rankou.
This work has been supported in part by the Netherlands Organization for Scientific Research (NWO,
grant S85-324) to LWC and the Innovational
Research Incentives Scheme (VENI, nr. 863.09.017;
NWO-ALW) to RHJE.
REFERENCES
APG I. 1998. An ordinal classification for the families of
flowering plants. Annals of the Missouri Botanical Garden
85: 531553.
APG III. 2009. An update of the Angiosperm Phylogeny
Group classification for the orders and families of flowering
plants: APG III. Botanical Journal of the Linnean Society
161: 105121.
Baillon HE. 1868. Anonaces. Paris: L. Hachette et Cie.
Bentham G. 1863. Ordo V. Anonaceae. In: Bentham G,
Hooker JD, eds. Genera plantarum, Vol. 1. London: A.
Black, 2029.
Birky CWJ. 2001. The inheritance of genes in mitochondria
and chloroplasts: laws, mechanisms, and models. Annual
Review of Genetics 35: 125148.
Brandley MC, Schmitz A, Reeder TW. 2005. Partitioned
Bayesian analyses, partition choice, and the phylogenetic
relationships of scincid lizards. Systematic Biology 54: 373
390.
36
Briechle-Mck MH. 1994. Beitrge zur Histogenese des

Blten und Frchte pseudosynkarper Annonaceen-Arten.
Frankfurt: Egelsbach.
Bygrave PC. 2000. Molecular systematics of Annonaceae
Juss. PhD Thesis, University of Reading.
Chaowasku T, Keler PJA, van der Ham RWJM. 2012. A
taxonomic revision and pollen morphology of the genus
Dendrokingstonia (Annonaceae). Botanical Journal of the
Linnean Society 168: 7690.
Chaowasku T, Zijlstra G, Chatrou LW. 2011. (2029) Proposal to conserve the name Meiogyne against Fitzalania
(Annonaceae). Taxon 60: 15221523.
Chase MW, Cox AV. 1998. Gene sequences, collaboration and
analysis of large data sets. Australian Systematic Botany
11: 215229.
Chatrou LW. 1999. The Annonaceae and the Annonaceae
Project: a brief overview of the state of affairs. Acta Horticulturae 497: 4349.
Chatrou LW, Escribano MP, Viruel MA, Maas JW, Richardson JE, Hormaza JI. 2009. Microsatellite flanking
regions provide a new source of data for plant species-level
phylogenetics. Molecular Phylogenetics and Evolution 53:
726733.
Chatrou LW, He P. 1999. Studies in Annonaceae XXXIII. A
revision of Fusaea (Baill.) Saff. Brittonia 52: 181203.
Chatrou LW, Koek-Noorman J, Maas PJM. 2000. Studies
in Annonaceae XXXVI. The Duguetia alliance: where the
ways part. Annals of the Missouri Botanical Garden 87:
234245.
Christmann M. 1989. Die tritegmischen annonaceensamen.
Botanische Jahrbcher fr Systematik, Pflanzengeschichte
und Pflanzengeographie 110: 433439.
Couvreur TLP. 2009. Monograph of the syncarpous African
genera Isolona and Monodora (Annonaceae). Systematic
Botany Monographs 87: 1150.
Couvreur TLP, van der Ham RWJM, Mbele YM, Mbago
FM, Johnson DM. 2009. Molecular and morphological
characterization of a new monotypic genus of Annonaceae,
Mwasumbia, from Tanzania. Systematic Botany 34: 26
276.
Couvreur TLP, Pirie MD, Chatrou LW, Saunders RMK,
Su YCF, Richardson JE, Erkens RHJ. 2011. Early evolutionary history of the flowering plant family Annonaceae:
steady diversification and boreotropical geodispersal.
Journal of Biogeography 38: 664680.
Couvreur TLP, Richardson JE, Sosef MSM, Erkens
RHJ, Chatrou LW. 2008. Evolution of syncarpy and other
morphological characters in African Annonaceae: a posterior
mapping approach. Molecular Phylogenetics and Evolution
47: 302318.
Cronquist A. 1988. The evolution and classification of flowering plants. New York: The New York Botanical Garden.
Cummings MP, Meyer A. 2005. Magic bullets and golden
rules: data sampling in molecular phylogenetics. Zoology
108: 329336.
Diels L. 1912. Die Anonaceen von Papuasien. Botanische
Jahrbcher fr Systematik, Pflanzengeschichte und Pflanzengeographie 49: 113167.
Diels L. 1932. Die Gliederung der Anonaceae und ihre Phylogenie. Sitzungsberichte der Preussischen Akademie der
Wissenschaften 1932: 7785.
Doyle JA, Bygrave P, Le Thomas A. 2000. Implications of
molecular data for pollen evolution in Annonaceae. In:
Harley MM, Morton CM, Blackmore S, eds. Pollen and
spores: morphology and biology. Kew: Royal Botanic
Gardens, 259284.
Doyle JA, Le Thomas A. 1994. Cladistic analysis and pollen
evolution in Annonaceae. Acta Botanica Gallica 141: 149
170.
Doyle JA, Le Thomas A. 1995. Evolution of pollen characters and relationships of African Annonaceae: implications
of a cladistic analysis. In: Le Thomas A, Roche E, eds. 2nd
Symposium on African Palynology, Tervuren (Belgium).
Orlans: Centre International pour la Formation et les
changes Gologiques, 241254.
Doyle JA, Le Thomas A. 1996. Phylogenetic analysis
and character evolution in Annonaceae. Bulletin du
Musum National dHistoire Naturelle, Paris, 4e srie,
Section B, Adansonia 18: 279334.
Doyle JA, Le Thomas A. 1997. Significance of palynology for
phylogeny of Annonaceae: experiments with removal of
pollen characters. Plant Systematics and Evolution 206:
133159.
Doyle JA, Le Thomas A. 2012. Evolution and phylogenetic
significance of pollen in Annonaceae. Botanical Journal of
the Linnean Society 169: 190221.
Doyle JJ, Doyle JL. 1987. A rapid DNA isolation procedure
for small quantities of fresh leaf tissue. Phytochemical Bulletin 19: 1115.
Dunal MF. 1817. Monographie de la famille des Anonaces.
Paris: Treuttel & Wrtz.
Endlicher S. 1839. Genera plantarum secundum ordines
naturales disposita. Vienna: Fr. Beck Universitatis
Bibliopolam.
Endress PK, Armstrong JE. 2011. Floral development and
floral phyllotaxis in Anaxagorea (Annonaceae). Annals of
Botany 108: 835845.
Endress PK, Doyle JA. 2009. Reconstructing the ancestral
angiosperm flower and its initial specializations. American
Journal of Botany 96: 2266.
Erkens RHJ, Chatrou LW, Koek-Noorman J, Maas JW,
Maas PJM. 2007. Classification of a large and widespread
genus of Neotropical trees, Guatteria (Annonaceae) and its
three satellite genera Guatteriella, Guatteriopsis and Heteropetalum. Taxon 56: 757774.
Erkens RHJ, Cross H, Maas JW, Hoenselaar K, Chatrou
LW. 2008. Assessment of age and greenness of herbarium
specimens as predictors for successful extraction and amplification of DNA. Blumea 53: 407428.
Erkens RHJ, Maas JW, Couvreur TLP. 2009. From Africa
via Europe to South America: migrational route of a speciesrich genus of Neotropical lowland rain forest trees (Guatteria; Annonaceae). Journal of Biogeography 36: 23382352.
Erkens RHJ, Maas PJM. 2008. The Guatteria group disentangled: sinking Guatteriopsis, Guatteriella, and Heteropetalum into Guatteria. Rodrigusia 59: 401406.

Farris JS. 1989. The retention index and homoplasy excess.
Systematic Zoology 38: 406407.
Fitch WM. 1971. Toward defining the course of evolution:
minimum change for a specified tree topology. Systematic
Zoology 20: 406416.
Fries RE. 1930. Revision der Arten einiger AnonaceenGattungen I. Acta Horti Bergiani 10: 1128.
Fries RE. 1931. Revision der Arten einiger AnonaceenGattungen II. Acta Horti Bergiani 10: 129341.
Fries RE. 1934. Revision der Arten einiger AnonaceenGattungen III. Acta Horti Bergiani 12: 1220.
Fries RE. 1937. Revision der Arten einiger AnnonaceenGattungen IV. Acta Horti Bergiani 12: 221288.
Fries RE. 1939. Revision der Arten einiger AnnonaceenGattungen V. Acta Horti Bergiani 12: 289577.
Fries RE. 1959. Annonaceae. In: Engler A, Prantl K, eds. Die
natrlichen Pflanzenfamilien, 2nd edn, Vol. 17aII. Berlin:
Duncker & Humblot, 1171.
van Gemerden BS, Olff H, Parren MPE, Bongers F. 2003.
The pristine rain forest? Remnants of historical human
impacts on current tree species composition and diversity.
Gentry AH. 1988. Tree species richness of upper Amazonian
forests. Proceedings of the National Academy of Sciences of
the United States of America 85: 156159.
Grniak M, Paun O, Chase MW. 2010. Phylogenetic relationships within Orchidaceae based on a low-copy nuclear
coding gene, Xdh: congruence with organellar and nuclear
ribosomal DNA results. Molecular Phylogenetics and Evolution 56: 784795.
Graybeal A. 1998. Is it better to add taxa or characters
to a difficult phylogenetic problem? Systematic Biology 47:
917.
Guindon S, Gascuel O. 2003. A simple, fast, and accurate
algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52: 696704.
Heath TA, Hedtke SM, Hillis DM. 2008. Taxon sampling
and the accuracy of phylogenetic analyses. Journal of Systematics and Evolution 46: 239257.
van Heusden ECH. 1992. Flowers of Annonaceae: morphology, classification, and evolution. Leiden: Rijksherbarium /
Hortus Botanicus.
van Heusden ECH. 1994. Revision of Meiogyne (Annonaceae). Blumea 38: 487511.
Hooker JD, Thomson T. 1855. Flora indica, Vol. 1. London:
W. Pamplin, 86153.
Hooker JD, Thomson T. 1872. Annonaceae. In: Hooker JD,
ed. The flora of British India, Vol. 1. London: L. Reeve &
Co., 4594.
Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP.
2001. Bayesian inference of phylogeny and its impact on
evolutionary biology. Science 294: 23102314.
Hutchinson J. 1923. Contributions towards a phylogenetic
classification of flowering plants II. The genera of Annonaceae. Bulletin of Miscellaneous Information, Royal Botanic
Gardens, Kew 1923: 241261.
Hutchinson J. 1964. The genera of flowering plants, ed. 2, I.
Dicotyledones. Oxford: Clarendon Press.
37
Hutchinson J. 1973. The families of flowering plants

(arranged according to a new system based on their probable
phylogeny). London: Oxford University Press.
Huysmans S, Verstraete B, Smets E, Chatrou LW. 2010.
Distribution of orbicules in Annonaceae mirrors evolutionary trend in angiosperms. Plant Ecology and Evolution 143:
199211.
Johnson DM. 2003. Phylogenetic significance of spiral and
distichous architecture in the Annonaceae. Systematic
Botany 28: 503511.
Johnson DM, Murray NA. 1995. Synopsis of the tribe Bocageeae (Annonaceae), with revisions of Cardiopetalum, Froesiodendron, Trigynaea, Bocagea, and Hornschuchia.
Brittonia 47: 248319.
Kass RE, Raftery AE. 1995. Bayes factors. Journal of the
American Statistical Association 90: 773795.
Kelchner SA. 2000. The evolution of non-coding chloroplast
DNA and its application in plant systematics. Annals of the
Missouri Botanical Garden 87: 482498.
Kelchner SA, Clark LG. 1997. Molecular evolution and
phylogenetic utility of the chloroplast rpl16 intron in
Chusquea and the Bambusoideae (Poaceae). Molecular Phylogenetics and Evolution 8: 385397.
Keler PJA. 1988. Revision der Gattung Orophea Blume
(Annonaceae). Blumea 33: 180.
King G. 1893. The Anonaceae of British India. Annals
of the Royal Botanic Garden, Calcutta 4: 1169; pl. 161
220.
Kluge AG, Farris JS. 1969. Quantitative phyletics and the
evolution of anurans. Systematic Zoology 18: 132.
Koek-Noorman J, van Setten AK, van Zuilen CM. 1997.
Studies in Annonaceae. XXVI. Flower and fruit morphology
in Annonaceae. Their contribution to patterns in cluster
analysis. Botanische Jahrbcher fr Systematik, Pflanzengeschichte und Pflanzengeographie 119: 213230.
Koek-Noorman J, Westra LYT. 2012. Macrophotographic
wood atlas of Annonaceae. Botanical Journal of the Linnean
Society 169: 135189.
Kosteletzky
VF.
1836.
Allgemeine
medizinischpharmazeutische Flora. Flora 5: 17051716.
Le Thomas A. 1969. Annonaces. Flore du Gabon, Vol. 16.
Paris: Musum National dHistoire Naturelle.
Le Thomas A. 1980. Ultrastructural characters of the pollen
grains of African Annonaceae and their significance for the
phylogeny of primitive Annonaceae (first part). Pollen and
Spores 22: 267342.
Le Thomas A. 1981. Ultrastructural characters of the pollen
grains of African Annonaceae and their significance for the
phylogeny of primitive Annonaceae (second part). Pollen
and Spores 23: 536.
Le Thomas A, Doyle JA. 1996. Geographic relationships of
Malagasy Annonaceae. In: Loureno WR, ed. Biogographie
de Madagascar. Paris: ditions de lORSTOM, 8594.
Le Thomas A, Lugardon B. 1976. De la structure grenue a
la structure columellaire dans le pollen des Annonacees.
Adansonia, n.s. 15: 543572.
Le Thomas A, Lugardon B, Doyle JA. 1994. Pollen ultrastructure and relationships of Fusaea (Baillon) Safford and
38
Duguetia A. Saint-Hilaire (Annonaceae). Review of Palaeobotany and Palynology 83: 5564.

Lucas PW, Gaskins JT, Lowrey TK, Harrison ME,
Morrogh-Bernard HC, Cheyne SM, Begley MR. 2012.
Evolutionary optimization of material properties of a tropical seed. Journal of the Royal Society Interface 9: 3442.
Maas PJM. 1983. Project systematics of Annonaceae. Taxon
32: 528529.
Maas PJM, Westra LYT. 1984. Studies in Annonaceae. II. A
monograph of the genus Anaxagorea A.St.Hil., part 1. Botanische Jahrbcher fr Systematik, Pflanzengeschichte und
Pflanzengeographie 105: 73134.
Maas PJM, Westra LYT, Chatrou LW. 2003. Duguetia.
Flora Neotropica monograph 88. New York: The New York
Botanical Garden.
Maas PJM, Westra LYT, Vermeer M. 2007. Revision of the
Neotropical genera Bocageopsis, Onychopetalum, and Unonopsis (Annonaceae). Blumea 52: 413554.
Maddison DR, Maddison WP. 2000. MacClade version 4:
analysis of phylogeny and character evolution. Sunderland,
MA: Sinauer Associates.
McNeill J, Barrie FR, Burdet HM, Demoulin V, Hawksworth DL, Marhold K, Nicolson DH, Prado J, Silva
PC, Skog JE, Wiersema JH, Turland NJ. 2006. International code of botanical nomenclature (Vienna Code).
Ruggell, Liechtenstein: A.R.G. Gantner Verlag.
Mitchell A, Mitter C, Regier JC. 2000. More taxa or more
characters revisited: combining data from nuclear proteinencoding genes for phylogenetic analyses of Noctuoidea
(Insecta: Lepidoptera). Systematic Biology 49: 202224.
Mols JB, Gravendeel B, Chatrou LW, Pirie MD, Bygrave
P, Chase MW, Keler PJA. 2004. Identifying clades in
Asian Annonaceae: monophyletic genera in the polyphyletic
Miliuseae. American Journal of Botany 91: 590600.
Mols JB, Keler PJA. 2003. Studies in the Miliuseae. V.
Review of the taxonomic history of a polyphyletic tribe.
Telopea 10: 113124.
Mols JB, Keler PJA, Rogstad SH, Saunders RMK. 2008.
Reassignment of six Polyalthia species to the new genus
Maasia (Annonaceae): molecular and morphological congruence. Systematic Botany 33: 490494.
Morawetz W, Le Thomas A. 1988. Karyology and systematics of the genus Ambavia and other Annonaceae from
Madagascar. Plant Systematics and Evolution 158: 155
160.
Morrison DA. 2007. Increasing the efficiency of searches for
the maximum likelihood tree in a phylogenetic analysis of
up to 150 nucleotide sequences. Systematic Biology 56:
9881010.
Mller KF. 2005. The efficiency of different search strategies
in estimating parsimony jackknife, bootstrap, and Bremer
support. BMC Evolutionary Biology 5: 58.
Murray NA. 1993. Revision of Cymbopetalum and Porcelia.
Systematic Botany Monographs 40: 1121.
Nakkuntod M, Su YCF, Seelanan T, Saunders RMK.
2009. Molecular phylogenetic and morphological evidence
for the congeneric status of Goniothalamus and Richella
(Annonaceae). Taxon 58: 127132.
Nixon KC. 1999. The parsimony ratchet, a new method for

rapid parsimony analysis. Cladistics 15: 407414.
Nylander JAA, Wilgenbusch JC, Warren DL, Swofford
DL. 2008. AWTY (are we there yet?): a system for graphical
exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24: 581583.
Okada H. 1996. New genus and new species of the Annonaceae from the Malesian wet tropics. Acta Phytotaxonomica
et Geobotanica 47: 19.
Philippe H, Snell EA, Bapteste E, Lopez P, Holland
PWH, Casane D. 2004. Phylogenomics of eukaryotes:
impact of missing data on large alignments. Molecular
Biology and Evolution 21: 17401752.
Phillips OL, Miller J. 2002. Global patterns of plant diversity: Alwyn H. Gentrys forest transect data set. St. Louis,
MO: Missouri Botanical Garden Press.
Pirie MD, Balcazar Vargas MP, Botermans M, Bakker
FT, Chatrou LW. 2007. Ancient paralogy in the cpDNA
trnL-F region in Annonaceae: implications for plant molecular systematics. American Journal of Botany 94: 10031016.
Pirie MD, Chatrou LW, Erkens RHJ, Maas JW, van der
Niet T, Mols JB, Richardson JE. 2005. Phylogeny reconstruction and molecular dating in four Neotropical genera of
Annonaceae: the effect of taxon sampling in age estimation.
In: Bakker FT, Chatrou LW, Gravendeel B, Pelser PB, eds.
Plant species-level systematics: new perspectives on pattern
and process, Vol. 143. Ruggell, Liechenstein: A.R.G.
Gantner Verlag, 149174.
Pirie MD, Chatrou LW, Mols JB, Erkens RHJ, Oosterhof
J. 2006. Andean-centred genera in the short-branch clade
of Annonaceae: testing biogeographical hypotheses using
phylogeny reconstruction and molecular dating. Journal of
Biogeography 33: 3146.
Pirie MD, Humphreys AM, Galley C, Barker NP,
Verboom GA, Orlovich D, Draffin SJ, Lloyd K, Baeza
CM, Negritto M, Ruiz E, Sanchez JHC, Reimer E,
Linder HP. 2008. A novel supermatrix approach improves
resolution of phylogenetic relationships in a comprehensive
sample of danthonioid grasses. Molecular Phylogenetics and
Evolution 48: 11061119.
Posada D, Crandall KA. 1998. Modeltest: testing the model
of DNA substitution. Bioinformatics 14: 817818.
Prantl K. 1891. Anonaceae. In: Engler A, Prantl K, eds. Die
natrlichen Pflanzenfamilien, Vol. III, 2. Leipzig: W. Engelmann, 2329.
Provan J, Powell W, Hollingsworth PM. 2001. Chloroplast
microsatellites: new tools for studies in plant ecology and
evolution. Trends in Ecology & Evolution 16: 142147.
Qiu Y-L, Dombrovska O, Lee J, Li L, Whitlock BA,
Bernasconi-Quadroni F, Rest JS, Davis CC, Borsch T,
Hilu KW, Renner SS, Soltis DE, Soltis PS, Zanis MJ,
Cannone JJ, Gutell RR, Powell M, Savolainen V,
Chatrou LW, Chase MW. 2005. Phylogenetic analyses of
basal angiosperms based on nine plastid, mitochondrial,
and nuclear genes. International Journal of Plant Sciences
166: 815842.
Rafinesque CS. 1815. Analyse de la nature. Palermo: Aux
dpens de lauteur.

Rainer H. 2007. Monographic studies in the genus Annona L.
(Annonaceae): inclusion of the genus Rollinia A.St.-Hil.
Annalen des Naturhistorischen Museums in Wien. Serie B,
Botanik und Zoologie. Vienna 108: 191205.
Rainer H, Chatrou LW. 2006. AnnonBase: world species
list of Annonaceae version 1.1, 12 Oct 2006. Available
at: http://www.sp2000.org and http://www.annonaceae.org.
Accessed 4 December 2011.
Rambaut A, Drummond AJ. 2007. Tracer v1.4. Available at:
http://beast.bio.ed.ac.uk/Tracer. Accessed 22 May 2011.
Reichenbach HGL. 1837. Handbuch des natrlichen Pflanzensystems. Dresden, Leipzig: Arnoldschen Buchhandlung.
Richardson JE, Chatrou LW, Mols JB, Erkens RHJ,
Pirie MD. 2004. Historical biogeography of two cosmopolitan families of flowering plants: Annonaceae and Rhamnaceae. Philosophical Transactions of the Royal Society of
London, Series B: Biological Sciences 359: 14951508.
Rokas A, Carroll SB. 2005. More genes or more taxa? The
relative contribution of gene number and taxon number to
phylogenetic accuracy. Molecular Biology and Evolution 22:
13371344.
Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian
phylogenetic inference under mixed models. Bioinformatics
19: 15721574.
Saunders RMK. 2010. Floral evolution in the Annonaceae:
hypotheses of homeotic mutations and functional convergence. Biological Reviews 85: 571591.
Saunders RMK, Su YCF, Xue B. 2011. Phylogenetic affinities of Polyalthia species (Annonaceae) with columellarsulcate pollen: enlarging the Madagascan endemic genus
Fenerivia. Taxon 60: 14071416.
Sauquet H, Doyle JA, Scharaschkin T, Borsch T, Hilu
KW, Chatrou LW, Le Thomas A. 2003. Phylogenetic
analysis of Magnoliales and Myristicaceae based on multiple data sets: implications for character evolution. Botanical Journal of the Linnean Society 142: 125186.
Scharaschkin T, Doyle JA. 2005. Phylogeny and historical
biogeography of Anaxagorea (Annonaceae) using morphology and non-coding chloroplast sequence data. Systematic
Botany 30: 712735.
Scharaschkin T, Doyle JA. 2006. Character evolution in
Anaxagorea (Annonaceae). American Journal of Botany 93:
3654.
van Setten AK, Koek-Noorman J. 1992. Studies in Annonaceae. XVII. Fruits and seeds of Annonaceae: morphology
and its significance for classification. Stuttgart: E.
Schweizerbartsche Verlagsbuchhandlung.
Sikes DS, Lewis PO. 2001. PAUPRat: PAUP implementation
of the parsimony ratchet, Version 1, beta ed. Distributed by
the authors.Storrs, CT: Department of Ecology and Evolutionary Biology, University of Connecticut.
Simmons MP, Ochoterena H. 2000. Gaps as characters in
sequence-based phylogenetic analysis. Systematic Biology
49: 369381.
Sinsheimer JS, Lake JA, Little RJA. 1996. Bayesian
hypothesis testing of four-taxon topologies using molecular
sequence data. Biometrics 52: 193210.
Slik JWF, Poulsen AD, Ashton PS, Cannon CH, Eich-
39
horn KAO, Kartawinata K, Lanniari I, Nagamasu H,

Nakagawa M, van Nieuwstadt MGL, Payne J, Saridan
A, Sidiyasa K, Verburg RW, Webb CO, Wilkie P. 2003.
A floristic analysis of the lowland dipterocarp forests of
Borneo. Journal of Biogeography 30: 15171531.
Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihoodbased phylogenetic analyses with thousands of taxa and
mixed models. Bioinformatics 22: 26882690.
Stamatakis A, Hoover P, Rougemont J. 2008. A rapid
bootstrap algorithm for the RAxML web servers. Systematic
Biology 57: 758771.
Su YCF, Chaowasku T, Saunders RMK. 2010. An
extended phylogeny of Pseuduvaria (Annonaceae) with
descriptions of three new species and a reassessment of the
generic status of Oreomitra. Systematic Botany 35: 3039.
Su YCF, Mols JB, Takeuchi W, Keler PJA, Saunders
RMK. 2005. Reassessing the generic status of Petalolophus
(Annonaceae): evidence for the evolution of a distinct
sapromyophilous lineage within Pseuduvaria. Systematic
Botany 30: 494502.
Su YCF, Saunders RMK. 2006. Monograph of Pseuduvaria
(Annonaceae). Systematic Botany Monographs 79: 1204.
Su YCF, Saunders RMK. 2009. Evolutionary divergence
times in the Annonaceae: evidence of a late Miocene origin
of Pseuduvaria in Sundaland with subsequent diversification in New Guinea. BMC Evolutionary Biology 9: 153.
Surveswaran S, Wang RJ, Su YCF, Saunders RMK. 2010.
Generic delimitation and historical biogeography in the
early-divergent ambavioid lineage of Annonaceae:
Cananga, Cyathocalyx and Drepananthus. Taxon 59: 1721
1734.
Svoma E. 1998. Studies on the embryology and gynoecium
structures in Drimys winteri (Winteraceae) and some Annonaceae. Plant Systematics and Evolution 209: 205229.
Swofford DL. 2000. PAUP*. Phylogenetic analysis using parsimony (* and other methods), version 4.0b10, 4.0b10 edn.
Sunderland, MA: Sinauer Associates.
Takhtajan A. 1997. Diversity and classification of flowering
plants. New York: Columbia University Press.
Tchouto MGP, Yemefack M, de Boer WF, de Wilde JJFE,
van der Maesen LJG, Cleef AM. 2006. Biodiversity
hotspots and conservation priorities in the Campo-Maan
rain forests, Cameroon. Biodiversity and Conservation 15:
12191252.
Thongpairoj U. 2008. Taxonomy and molecular phylogeny of
Artabotrys R. Brown and palynology of tribe Unoneae
(Annonaceae) in Thailand. PhD Thesis, Chiang Mai
University.
Tsou C-H, Fu Y-L. 2007. Octad pollen formation in Cymbopetalum (Annonaceae): the binding mechanism. Plant Systematics and Evolution 263: 1323.
Tsou C-H, Johnson DM. 2003. Comparative development of
aseptate and septate anthers of Annonaceae. American
Journal of Botany 90: 832848.
Valencia R, Balslev H, Paz Y Mio C. G. 1994. High tree
alpha-diversity in Amazonian Ecuador. Biodiversity and
Conservation 3: 2128.
Verdcourt B. 1971. Annonaceae. Flora of Tropical East
40
Africa, Vol. 1, part 1. London: Crown Agents for Overseas

Governments and Administrations.
Walker JW. 1971. Pollen morphology, phytogeography and
phylogeny of the Annonaceae. Contributions from the Gray
Herbarium of Harvard University 202: 1132.
Walker JW. 1972. Chromosome numbers, phylogeny, phytogeography of the Annonaceae and their bearing on the
(original) basic chromosome number of angiosperms. Taxon
21: 5765.
Wang J. 2009. Systematics and phylogeny of Dasymaschalon
(Annonaceae). PhD Thesis, The University of Hong Kong.
Wang J, Chalermglin P, Saunders RMK. 2009. The genus
Dasymaschalon (Annonaceae) in Thailand. Systematic
Botany 34: 252265.
Weerasooriya AD, Saunders RMK. 2010. Monograph of
Mitrephora (Annonaceae). Systematic Botany Monographs
90: 1167.
Westra LYT. 1985. Studies in Annonaceae. IV. A taxonomic
revision of Tetrameranthus R.E.Fries. Proceedings of the
Koninklijke Nederlandse Akademie van Wetenschappen,
Series C 88: 449482.
Wiens JJ. 2005. Can incomplete taxa rescue phylogenetic
analyses from long-branch attraction? Systematic Biology
54: 731742.
Wiens JJ. 2006. Missing data and the design of phylogenetic
analyses. Journal of Biomedical Informatics 39: 3442.
Xu F, Ronse De Craene L. 2010. Floral ontogeny of Annonaceae: evidence for high variability in floral form. Annals of
Botany 106: 591605.
Xue B, Su YCF, Mols JB, Keler PJA, Saunders RMK.
2011. Further fragmentation of the polyphyletic genus Polyalthia (Annonaceae): molecular phylogenetic support for a
broader delimitation of Marsypopetalum. Systematics and
Biodiversity 9: 1726.
Zhou L, Su YCF, Chalermglin P, Saunders RMK. 2010.
Molecular phylogenetics of Uvaria (Annonaceae): relationships with Balonga, Dasoclema and Australian species of
Melodorum. Botanical Journal of the Linnean Society 163:
3343.
Zhou L, Su YCF, Saunders RMK. 2009. Molecular phylogenetic support for a broader delimitation of Uvaria (Annonaceae), inclusive of Anomianthus, Cyathostemma, Ellipeia,
Ellipeiopsis and Rauwenhoffia. Systematics and Biodiversity
7: 249258.
Zhou L, Su YCF, Thomas DC, Saunders RMK. 2012.
Out-of-Africa dispersal of tropical floras during the Miocene
climatic optimum: evidence from Uvaria (Annonaceae).
Zwickl DJ. 2006. Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets
under the maximum likelihood criterion. PhD Dissertation,
The University of Texas.

J 1095-8339 2012 01235 X PDF

Uploaded by

Document Information

Original Description:

Original Title

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

J 1095-8339 2012 01235 X PDF

Uploaded by

Copyright:

Available Formats

bs_bs_banner

A new subfamilial and tribal classification of the

Wageningen University, Biosystematics Group, Droevendaalsesteeg 1, 6708 PB Wageningen, the

ADDITIONAL KEYWORDS: plastid markers subfamilies supermatrix tribes.

*Corresponding author. E-mail: lars.chatrou@wur.nl

ANNONACEAE PHYLOGENETICS AND CLASSIFICATION

MATERIAL AND METHODS

We used previously published plus unpublished

et al. (2008). PCR products were purified using

Annona herzogii (R.E.Fr.)

Annickia chlorantha (Oliv.)

Anaxagorea silvatica R.E.Fr.

Alphonsea boniana Finet &

Coelocaryon preussii Warb.

Persea americana Mill.

Table 1. Collections and GenBank numbers

Asteranthe asterias (S.

Asimina triloba (L.) Dunal

Cananga odorata (Lam.)

Artabotrys hexapetalus (L.f.)

ANNONACEAE PHYLOGENETICS AND CLASSIFICATION

Disepalum pulchrum (King)

Desmos elegans (Thwaites)

Desmos chinensis Lour.

Letestudoxa bella Pellegr.

Isolona cooperi Hutch. &

Guatteria pudica N.Zamora

Fusaea longifolia (Aubl.)

Papua New Guinea

ANNONACEAE PHYLOGENETICS AND CLASSIFICATION

Miliusa horsfieldii (Benn.)

Maasia glauca (Hassk.)

Papua New Guinea

Monodora crispata Engl.

Monocarpia euneura Miq.

Miliusa mollis Pierre

ANNONACEAE PHYLOGENETICS AND CLASSIFICATION

Oxandra longipetala R.E.Fr.

Oxandra asbeckii (Pulle)

Orophea polycarpa A.DC.

Polyalthia obliqua Hook.f.

Polyalthia cf. longifolia

Polyalthia longifolia (Sonn.)

Polyalthia debilis (Pierre)

Polyalthia congesta (Ridl.)

Polyalthia cauliflora Hook.f.

Polyalthia borneensis Merr.

ANNONACEAE PHYLOGENETICS AND CLASSIFICATION

Popowia pisocarpa (Blume)

Popowia odoardi Diels

Polyalthia viridis Craib

Papua New Guinea

ANNONACEAE PHYLOGENETICS AND CLASSIFICATION

Uvaria cherrevensis (Pierre

Uvaria chamae P.Beauv.

Unonopsis stipitata Diels

Trigynaea duckei (R.E.Fr.)

Uvaria siamensis (Scheff.)

Uvaria grandiflora Roxb. ex

ANNONACEAE PHYLOGENETICS AND CLASSIFICATION

T. Chaowasku et al. (unpubl. data).

Nakkuntod et al. (2009).