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Botanical Journal of the Linnean Society, 2012, 169 , 5–40. With 1 figure

A new subfamilial and tribal classification of the pantropical flowering plant family Annonaceae informed by molecular phylogenetics

LARS W. CHATROU 1 *, MICHAEL D. PIRIE 2 , ROY H. J. ERKENS 3,4 , THOMAS L. P. COUVREUR 5 , KURT M. NEUBIG 6 , J. RICHARD ABBOTT 7 , JOHAN B. MOLS 8 , JAN W. MAAS 3 , RICHARD M. K. SAUNDERS 9 and MARK W. CHASE 10

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 Développement (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: Anaxagore- oideae, 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: Dendroking- stonieae, 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 , 5–40.

ADDITIONAL KEYWORDS: plastid markers – subfamilies – supermatrix – tribes.

6

L. W. CHATROU ET AL .

INTRODUCTION

Inventories of tropical forests on all continents invari- ably 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 Miño, 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 demon- strated (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, Chao- wasku & 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 nec- essary 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 increas- ing 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 clas- sification of Fries (1959), primarily based on floral characters, remains perhaps the most widely used. However, with few exceptions, his tribes and infor- mal groups of genera are neither characterized by unequivocal (combinations of) characters nor demon-

strably monophyletic. To quote from a recent mono- graphic 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 macromorphologi- cal 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 subse- quent studies employing DNA sequence data (Doyle, Bygrave & Le Thomas, 2000; Mols et al ., 2004; Rich- ardson 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 use- fully memorable. Improvements in generic classifica- tion 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 Annon- aceae inferred from multiple plastid DNA loci, repre- senting 94 of the 108 currently recognized genera and marking an important improvement in both the rep- resentation of taxa (at the generic level) and phylo- genetic resolution in Annonaceae compared with previous efforts (e.g. Richardson et al., 2004; Cou- vreur et al ., 2011). We place this analysis in the context of previous infrafamilial classifications, evalu- ate 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 ), Ambavio- ideae (corresponding to the ambavioid clade of Doyle & Le Thomas, 1994, 1996), Annonoideae (correspond- ing to the LBC of Richardson et al., 2004, and the inaperturate clade of Doyle & Le Thomas, 1994, 1996)

ANNONACEAE PHYLOGENETICS AND CLASSIFICATION 7

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 Annon- oideae, 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 recog- nized genera (Rainer & Chatrou, 2006), 94 were rep- resented, 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, Cou- vreur 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 Ano- mianthus 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 representa- tion 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 cetyl- trimethylammonium 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 accu- racy 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 strat- egy 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 remain- ing 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 guide- lines 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 posi- tions 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 informa- tive base changes that were revealed displayed little

8

L. W. CHATROU ET AL .

EF179350

EF179322

EF179323

EF179321

AY841550

JQ513885

AY841551

trnSG

––

––

EF179244

EF179246

EF179273

AY578140

AY841370

atpB - rbcL

JQ513883

AY841371

psbA - trnH

DQ125132

DQ125116

AY841424

AY841444

AY841426

AY841427

JQ513882

AY841442

– –

– –

DQ861842

AY238944

AY220414

AY231284

AY841734

AY841669

JQ513889

AY743456

AY319078

AY743469

AY841670

AY743458

AY743457

AY319077

AY220362

AY220415

AY841673

AY220361

AY841671

(spacer)

(spacer)

(spacer)

(intron)

(intron)

(intron)

trnLF

DQ861644

DQ861643

AY841572

JQ742022

JQ742023

JQ742021

AY841571

trnTL

EF179279

EF179280

EF179308

EF179281

JQ437546

AY841402

JQ437545

AY841401

ndhF

DQ125050

DQ125062

AY238960

AY743488

AY743477

JQ437547

AY743475

AY841393

matK

DQ861790

AY841594

AY318966

JQ513886

AY743439

AY841596

AY841656

AY743438

AY743450

AY743437

AY841592

AY238952

AY318965

AY841593

L12646

L12643

rbcL

Cultivated in UUBG, of Neotropical origin Gabon

Cultivated in UUBG, origin Australia Origin unknown

Cultivated in UUBG, origin China Cultivated in UUBG, origin Japan Vietnam

Cultivated in UUBG, origin Florida Peru

Origin unknown

Madagascar

Indonesia

Ecuador

Country

Gabon

Gabon

Brazil

Table 1. Collections and GenBank numbers

(WAG)

(WAG)

(WAG)

Chatrou , L . W .

Chatrou , L . W .

Chatrou , L . W .

Chatrou , L . W .

Chatrou , L . W .

. 5141 (L)

Wieringa , J . J.

87GR00058

Keßler , P . J. A .

Sosef , M . S . M .

Sosef , M . S . M .

Maas , P . J . M .

Maas , P . J . M .

Van Balgooy ,

Mixed origin

Mixed origin

Rabevohitra,

(U)

(U)

(L)

R. 2035

(U)

(U)

(U)

(U)

. n. (U)

(MO)

1877

8836

3640

8592

1803

3116

UUBG

467

278

279

162

M

s

Anaxagorea silvatica R.E.Fr.

Alphonsea boniana Finet &

Annickia chlorantha (Oliv.) Setten & Maas Annickia pilosa (Exell) Setten & Maas Annona glabra L.

Coelocaryon preussii Warb.

Alphonsea elliptica Hook.f.

Ambavia gerrardii (Baill.)

Galbulimima belgraveana

Annona herzogii (R.E.Fr.) H.Rainer

Degeneria vitiensis L.W.Bailey & A.C.Sm./

. roseiflora J.M.Mill.

Anaxagorea phaeocarpa

Persea americana Mill.

Liriodendron chinense

(F.Muell.) Sprague

Magnolia kobus DC.

Eupomatia bennettii

& Thomson

Le Thomas

Gagnep.

F.Muell.

Sargent

Mart.

Species

D

ANNONACEAE PHYLOGENETICS AND CLASSIFICATION 9

EF179324

EF179326

EF179329

EF179330

EF179328

EF179327

EF179332

EF179325

EF179331

AY841549

AY841548

AY841552

AY841553

EF179254

EF179249

EF179250

EF179248

EF179247

EF179252

EF179255

EF179253

EF179251

AY841374

AY841372

AY841375

AY841373

DQ125120

DQ125121

DQ125119

DQ125118

DQ125117

EF179313

AY841429

AY841428

AY841448

AY841430

AY841447

AY841432

AY841431

GQ139881

EU169757

AY238946

AY841679

AY743459

AY231286

AY841686

AY841676

AY841680

AY841678

AY743460

AY841688

AY841677

AY743565

AY841675

AY841683

AY743573

AY743461

AY841681

(spacer)

(intron)

DQ861649

DQ861646

DQ861648

AY841574

JQ742024

JQ742026

JQ742029

JQ742028

JQ742027

JQ742025

AY841573

EF179284

EF179289

EF179286

EF179288

EF179290

EF179287

EF179282

EF179285

EF179283

AY841404

AY841406

AY841405

AY841403

DQ125054

DQ125052

DQ125055

DQ125053

DQ125051

EF179277

AY841394

AY743479

AY743478

AY743550

AY743542

AY238962

AY841395

DQ124939

EU169757

AY743519

AY841599

AY743440

AY841608

AY841598

AY841600

AY841610

AY743527

JQ513887

AY841602

AY743442

AY841605

AY238953

AY841603

AY841601

AY743441

Cultivated in UUBG, of Neotropical origin Cameroon

Cultivated in UUBG, origin India

Cultivated in Kebun Raya Bogor, Indonesia Cultivated in UUBG, originating from Brazil Costa Rica

Cultivated in UUBG, origin USA Kenya

French Guiana

Costa Rica

Thailand

Guyana

Gabon

Gabon

Brazil

Peru

USA

USA

Jansen-Jacobs ,

(WAG)

4018 (WAG)

(WAG)

Chatrou , L . W .

(U) Chatrou , L . W .

(U) Chatrou , L . W .

(FLAS) Chatrou , L . W .

Chatrou , L . W.

Wieringa , J. J .

(U) Wieringa, J.J.

84GR00275

Keßler , P . J . A .

94GR01614

Scharf , U . 76

Weerasooriya ,

Robertson , A.

Mols , J . B . 11

J . M. S . 300

A . s. n. (U)

J. R. Abbott

J . 5789

(K)

(L)

Cheek , M.

(U)

(U)

(U)

(U) Miralha ,

(U)

(U)

22361

7896 UUBG

3278

7548

3199

(L) UUBG

276

468

224

M.

54

93

Artabotrys hexapetalus (L.f.) Bhandari

Cymbopetalum torulosum G.E.Schatz Dasymaschalon macrocalyx Finet & Gagnep.

Asimina triloba (L.) Dunal

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

Cymbopetalum brasiliense (Vell.) Benth. ex Baill.

Asimina angustifolia A.Gray Asimina rugelii B.L.Rob.

Bocageopsis pleiosperma

Asteranthe asterias (S. Moore) Engl. & Diels Bocageopsis multiflora (Mart.) R.E.Fr.

Annona muricata L.

Anonidium sp.

Artabotrys sp.

Maas

10

L. W. CHATROU ET AL .

EF179336

EF179335

AY841554

trnSG

EF179259

EF179258

AY841376

atpB - rbcL

psbA - trnH

DQ125124

DQ125123

AY743444

AY318977

AY841463

HM173751

HQ214069

GQ139909

EU169759

AY319174

AY841694

AY319086

AY319089

AY841690

AY740590

AY319087

AY743462

AY841692

JQ762415

AY841695

AY319173

AY740573

AY743463

trnLF

DQ861650

JQ742030

AY841575

trnTL

EF179294

EF179293

AY841407

ndhF

AY841396

AY740558

AY740541

matK

HM173779

HQ214067

EU169781

AY318974

AY841614

JQ762414

AY743444

AY319059

AY841616

AY738178

AY319060

JQ513888

AY841617

AY318977

AY841612

AY318975

AY743443

AY738161

rbcL

Hong Kong

Hong Kong

Hong Kong

Costa Rica

Costa Rica

Sri Lanka

Cameroon

Indonesia

Indonesia

Indonesia

Australia

Tanzania

Malaysia

Thailand

Thailand

Country

Bolivia

Brazil

Peru

Johnson , D . M .

(L) Chatrou , L . W .

Chatrou , L . W .

Chatrou , L . W .

Chatrou , L . W .

Forster , P . I . F .

(U) Keßler , P . J . A .

Keßler , P . J. A .

Keßler , P . J. A .

(OWU) Chan , R. 192

Maas , P . J . M .

00/07b (L)

N2 (HKU)

Wong 46009

. R . 3290

00/05 (L)

(L)

(L)

Kostermans

C.-C. Pang

(U)

(K)

Andel ,van

(L)

(L)

(L)

(U)

(U)

Law , C . L

Law , C . L

(FLAS) Takeuchi

(U)

(U)

18201

24761

2746

8826

8326

3198

1903

3201

181

301

85

94

T

Fissistigma glaucescens (Hance) Merr. Fissistigma uonicum (Dunn) Merr. Fitzalania heteropetala (F.Muell.) F.Muell.

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.

Dasymaschalon sootepense Craib Desmopsis microcarpa R.E.Fr. Desmopsis schippii Standl.

Enicosanthum membranifolium J.Sinclair Enicosanthum paradoxum Becc. Ephedranthus boliviensis Chatrou & Pirie Ephedranthus sp.

Table 1. Continued

Desmos chinensis Lour.

Species

ANNONACEAE PHYLOGENETICS AND CLASSIFICATION 11

EU169806

EF179344

EF179339

EF179340

EF179338

EF179337

AY841556

AY841555

FJ842397

EF179266

EF179260

EF179267

EF179262

EF179263

EF179261

JQ513884

AY841378

AY841377

DQ125126

DQ125128

DQ125127

DQ125197

DQ125125

AY841436

AY841469

AY841437

AY841465

EU169760

EU169761

AY743464

AY841704

AY841706

AY841696

AY841698

AY841538

AY841700

AY743470

AY841697

AY238947

AY841707

AY231287

AY743465

AY741043

AY841703

AY319091

AY743471

(spacer)

AY741011

(intron)

DQ861653.

DQ861657

DQ861652

DQ861663

AY841576

AY841577

JQ742032

JQ742033

JQ742031

EU169715

EF179296

EF179298

EF179297

EF179302

EF179295

AY841409

AY841408

JQ769093

DQ125059

DQ125058

AY743484

AY743489

AY743490

AY740945

AY740913

AY743483

AY238963

EU169782

EU169783

AY740994

AY238954

AY841524

AY841629

AY318979

AY841619

AY743446

AY841626

AY841628

AY841620

AY841618

AY740962

AY841622

AY743452

AY743445

AY841625

AY743451

Papua New Guinea

UUBG, originating from Ivory Coast

UUBG, of tropical African origin

Costa Rica

Costa Rica

Thailand

Thailand

Thailand

Mexico

Ghana

Gabon

Gabon

Gabon

Gabon

Kenya

Brazil

Peru

Peru

Peru

C . C . H . 1795

(WAG)

(WAG)

(WAG)

(WAG)

Chatrou , L . W .

Chatrou , L . W .

Chatrou , L . W .

Chatrou , L . W .

Chatrou , L . W .

Wieringa , J . J .

Wieringa , J . J.

86GR00240

Keßler , P . J. A .

Keßler , P . J . A .

Keßler , P . J. A.

Sosef , M . S . M .

Sosef , M . S . M .

84GR00382

Maas , P . J . M .

(WAG) Semsei 2376

15656 (L)

(U)

(U)

(L)

(L)

(L)

Jongkind ,

(U)

(U)

(U)

(U)

(K) Ishiki , M.

(U)

Takeuchi

2797

2287

2376

3605

3188

8828 UUBG

3189

3193

2233

UUBG

107

175

205

179

113

Greenwayodendron suaveolens (Engl. & Diels) Verdc. Guatteria anomala R.E.Fr.

Klarobelia stipitata Chatrou

Guatteria pudica N.Zamora

Hexalobus salicifolius Engl.

Isolona campanulata Engl.

Dalziel ex G.P.Cooper &

Goniothalamus griffithii Hook.f. & Thomson Goniothalamus tapis Miq.

Greenwayodendron oliveri (Engl.) Verdc.

Fusaea longifolia (Aubl.) Saff. Fusaea peruviana R.E.Fr.

Letestudoxa bella Pellegr.

Isolona cooperi Hutch. &

Hexalobus crispiflorus A.

Hornschuchia citriodora

Friesodielsia desmoides

longirostris (Scheff.)

Klarobelia inundata

Haplostichanthus

(Craib) Steenis

Friesodielsia sp.

D.M.Johnson

Heusden

Chatrou

Maas

Diels

Record

Rich.

&

&

12

L. W. CHATROU ET AL .

EU169798

AY841558

AY841557

AY841565

AY841563

trnSG

AY841379

AY841380

atpB - rbcL

AY841387

AY841385

psbA - trnH

EU169731

AY841500

AY841475

AY841473

AY841503

EU169754

EU169753

AY319094

AY238948

AY841708

AY319098

AY319140

AY231288

AY319137

AY319092

AY319095

AY319135

AY319093

AY319083

AY319153

AY841701

AY841541

(spacer)

(intron)

trnLF

AY841584

AY841579

AY841586

AY841578

trnTL

AY841416

AY841410

AY841418

AY841411

ndhF

EU169687

AY238964

AY841397

AY518872

AY518873

matK

EU169776

EU169775

AY318986

AY319039

AY319026

AY841630

AY318980

AY841527

AY318982

AY238955

AY841623

AY319023

AY318983

AY318981

AY318971

AY319021

rbcL

Papua New Guinea

Indonesia

Indonesia

Indonesia

Indonesia

Indonesia

Australia

Malaysia

Malaysia

Thailand

Country

Mexico

Gabon

Gabon

Kenya

Peru

Peru

DV-M1-1930

(WAG) Ridsdale , C . E .

(WAG)

(SAN) Chatrou , L . W .

Chatrou , L . W .

Keßler , P . J. A.

(L) Keßler , P . J. A .

Ama 16394

(L) Mols , J. B . 20

(WAG) Robertson , A.

Breteler , F . J.

(WU)

(L) SAN 143918

Jessup , L . W .

Okada 3388

(L) Mols , J. B . 1

Rastini 153

Takeuchi &

Breteler , F .

(L)

(L)

(L) Rainer , H .

(U)

(K)

13947

12858

8 (U)

7505

1593

3192

2751

706

122

(L)

Miliusa horsfieldii (Benn.) Pierre

Marsypopetalum littorale (Blume) B.Xue & R.M.K.Saunders Marsypopetalum pallidum (Blume) Kurz Meiocarpidium lepidotum (Oliv.) Engl. & Diels

Maasia glauca (Hassk.) Mols, Keßler & Rogstad Maasia sumatrana (Miq.) Mols, Keßler & Rogstad Malmea dielsiana R.E.Fr.

Lettowianthus stellatus Diels Maasia discolor (Diels) Mols, Keßler & Rogstad

Meiogyne stenopetala (F.Muell.) Heusden Meiogyne virgata (Blume) Miq. Mezzettia parviflora Becc.

Table 1. Continued

Meiogyne cylindrocarpa

Letestudoxa glabrifolia Chatrou & Repetur

(Burck) Heusden

Meiogyne sp.

Malmea sp.

Species

ANNONACEAE PHYLOGENETICS AND CLASSIFICATION 13

EU169812

EF179346

EF179348

EF179345

AY841559

AY841560

AY841561

EF179269

EF179270

EF179268

EF179271

AY841382

AY841383

AY841381

DQ125129

DQ861696

DQ125130

EF179315

AY841479

AY841477

AY841485

EU169764

EU747674

EU169787

AY319109

AY743466

AY743496

AY319179

AY743500

AY743467

AY841712

AY841715

AY841713

AY841713

AY319101

AY319110

AY319112

AY319113

AY841711

AY319111

DQ861647

JQ742034

JQ742036

AY841580

AY841582

JQ742035

AY841581

EU169721

EF179304

EF179306

EF179303

AY841414

AY841412

AY841413

DQ125060

EU169700

EF179278

AY743486

AY518876

AY518865

AY743503

EU169786

EU747680

EU169765

AY841634

AY743514

AY318989

AY318996

AY318999

AY841636

AY743510

AY743448

AY319000

AY318998

AY841637

AY743447

AY318997

AY841635

AY319065

AY841633

Cultivated in UUBG, origin Ivory Coast Cultivated in UUBG, origin Ivory Coast Costa Rica

Cultivated in UUBG, origin Kenya Cultivated in UUBG, origin Nigeria Gabon

Indonesia

Indonesia

Indonesia

Tanzania

Malaysia

Malaysia

Thailand

Thailand

Ecuador

Liberia

Bolivia

Angola

Gabon

E64GR00066 UUBG

E84GR00389 Chatrou , L . W .

Pholsena 1756

Ridsdale , C . E .

. C . H. 6992

(WAG)

(WAG)

(WAG)

DV-SR-4671

sub IV-H-73

Chatrou , L . W .

(L) Chatrou , L . W .

(WAG) Wieringa , J . J.

84GR00388 Wieringa , J. J .

(L) Keßler , P . J . A .

(L) Keßler , P . J . A .

2002–2931

Mols , J . B . 7

Gardette , E .

Slik , J. W . F .

. L . P . 85

Pitman , N .

(K)

(L)

(L) Bamps , P .

(L) Jongkind ,

Couvreur ,

(U)

(U)

. n . (U)

(WAG) UUBG

90 (U)

3226

3566

2239

4459

3833

474 UUBG

425

T

C

s

Mischogyne michelioides Exell Mitrella kentii (Blume) Miq.

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

Neo-uvaria parallelivenia (Boerl.) H.Okada & K.Ueda Onychopetalum periquino (Rusby) D.M.Johnson & N.A.Murray

Monocarpia euneura Miq.

Monodora crispata Engl.

Mitrephora polypyrena (Blume) Miq. Mitrephora teysmannii Scheff. Mkilua fragrans Verdc.

Monocyclanthus vegnei

Monanthotaxis whytei

Miliusa mollis Pierre

Monanthotaxis sp.

(Stapf) Verdc.

Keay

14

L. W. CHATROU ET AL .

AY841562

trnSG

AY841384

atpB - rbcL

psbA - trnH

AY841498

EU169767

AY841724

AY841726

AY841719

AY841720

AY841710

AY319127

AY841717

AY319125

AY841723

AY319123

AY743473

AY841721

AY319121

AY319119

AY319117

trnLF

AY841583

trnTL

AY841415

ndhF

AY743492

matK

EU169789

AY743454

AY319004

AY841646

AY841639

AY319006

AY841648

AY319008

AY319010

AY319012

AY841642

AY841632

AY841645

AY841643

AY319013

AY841641

rbcL

Papua New Guinea

Costa Rica

Costa Rica

Cameroon

Indonesia

Indonesia

Indonesia

Thailand

Thailand

Thailand

Country

Guyana

Gabon

Kenya

Peru

Peru

Peru

(WAG)

(WAG)

(WAG)

Chatrou , L . W .

Chatrou , L . W .

Chatrou , L . W .

(U) Chatrou , L . W .

Chatrou , L . W .

Wieringa , J . J .

Wieringa , J . J .

Keßler , P . J . A.

(TISTR) Keßler , P . J. A .

Keßler , P . J . A .

Robertson , A .

University of

Utteridge , T.

UG-NB-55

(TISTR) Chalermglin

Chalermglin

Okada 3457

440416-1

(L)

(L)

(L)

Guyana ,

Neotrop .

17 (KL)

(U)

(U)

(U)

(U)

(U)

440403

Botany

course

7547

1605

2030

2779

3234

2953

165

215

120

204

114

(L)

Oxandra longipetala R.E.Fr.

Oxandra macrophylla R.E.Fr. Oxandra polyantha R.E.Fr.

Phaeanthus ebracteolatus (C.Presl.) Merr. Piptostigma mortehani De Wild. Piptostigma pilosum Oliv.

Oxandra venezuelana R.E.Fr. Oxandra xylopioides Diels

Ophrypetalum odoratum Diels Orophea celebica (Blume) Miq. Orophea creaghii (Ridl.) Leonardía & Keßler Orophea enterocarpa Maingay ex Hook.f. & Thomson Orophea kerrii Keßler

Orophea polycarpa A.DC.

Oxandra asbeckii (Pulle) R.E.Fr.

Table 1. Continued

Platymitra macrocarpa

Boerl.

Species

ANNONACEAE PHYLOGENETICS AND CLASSIFICATION 15

AY319134

AY319144

AY319139

AY319146

AY319129

AY319136

AY319138

AY319130

AY319128

AY319142

AY319132

AY319145

AY319133