Phylogeny and Generic Delimitation of Asian Marantaceae

Botanical Journal of the Linnean Society, 2009, 159, 381–395. With 3 ﬁgures

Phylogeny and generic delimitation of Asian Marantaceae

PIYAKASET SUKSATHAN1,2, MATS H. GUSTAFSSON1 and FINN BORCHSENIUS1*

1Department of Biological Sciences, Aarhus University, Ny Munkegade, Building 1540, DK-8000, Downloaded from https://academic.oup.com/botlinnean/article/159/3/381/2418341 by guest on 02 October 2021 Aarhus C, Denmark 2Current address: Queen Sirikit Botanic Garden, P.O. Box 7, Mae Rim, Chiang Mai 50180, Thailand

Received 29 August 2008; accepted for publication 3 December 2008

Eight genera and approximately 55 species of Marantaceae occur in Asia. Until recently these were the most poorly understood members of the family, but over the last few years much progress have been made in understanding their alpha taxonomy and distribution. Generic delimitation and phylogenetic relationships between genera, however, remain unclear. We analysed phylogenetic relationships in Asian Marantaceae using maximum parsimony and Bayesian analysis of plastid (rps16 intron) and nuclear [internal transcribed spacer (ITS)1 and 5S-non-transcribed spacer (NTS)] DNA sequence data. The results show that two Asian genera, Halopegia and Stachyphrynium, are well-defined monophyletic entities that should be maintained in their current form. Schu- mannianthus virgatus is sister to Halopegia and should be transferred to a genus of its own. Phacelophrynium, Monophrynium and Cominsia are nested within a paraphyletic Phrynium. Within this large clade, a number of geographically focused monophyletic species groups can be identified, in some cases corroborated by flower and fruit characters not previously emphasized in taxonomic studies, but these do not provide a useful framework for a revised generic classification. A revised generic classification of Asian Marantaceae is supplied, including the description of a new genus Indianthus Suksathan & Borchs. to which S. virgatus is transferred. © 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 159, 381–395.

ADDITIONAL KEYWORDS: 5S-non-transcribed spacer (NTS) – internal transcribed spacer (ITS)1 – Malesia – nuclear DNA – plastid DNA – rps16 intron – Zingiberales.

INTRODUCTION Other synapomorphies include leaf venation with sigmoid secondary veins and evenly spaced cross Marantaceae are a family of rhizomatous ground veins and the presence of a specialized pulvinus on herbs with a pantropical distribution comprising the junction between the leaf blade and the petiole c. 550 species in 31 genera (Andersson, 1998). From that enables the leaf blade to change position accord- both molecular and morphological evidence, it has ing to intensity and angle of the sunlight. been shown that the family forms a monophyletic In Asia, the family comprises c. 55 species in eight lineage with Cannaceae as sister group (Dahlgren genera. They are found in lowland and montane rain- & Rasmussen, 1983; Kress, 1990; Smith, Kress & forests from sea level up to an altitude of 1700 m, Zimmer, 1993; Kress et al., 2001). The flower struc- ranging from India eastward to the South Pacific ture is highly complex within the family. Flowers are islands (Vanuatu), including New Guinea and the asymmetric, with specialized staminodial structures Philippines, with the highest species diversity occur- adapted to facilitate an advanced pollination system ring in Borneo (c. 20 spp.). Until recently, the Asian in which the style is held under tension and released Marantaceae were very poorly known relative to upon contact with a visiting insect (Kennedy, 1977). their Neotropical counterparts (Andersson, 1986; Kennedy, 1986; Andersson, 1998), but several recent *Corresponding author. contributions have helped clarify alpha-taxonomy E-mail: fi[email protected] (e.g. Clausager & Borchsenius, 2003; Suksathan &

Borchsenius, 2003; Poulsen & Clausager, 2004; and Sanblasia) not represented] using sequence data Suksathan & Borchsenius, 2005; Clausager, Mood for three plastid DNA regions (matK and adjoining 3′ & Borchsenius, 2006; Suksathan, Borchsenius & matK-trnK intergenic spacer; trnL-trnF intergenic Poulsen, 2006; Suksathan & Borchsenius, 2008). spacer). That study identiﬁed ﬁve major clades within Generic delimitation and phylogenetic relationships the family, three of which have Asian representatives: between genera, however, remain unclear. The most the Stachyphrynium clade (Stachyphrynium); the comprehensive systematic treatment of the family Maranta clade [Halopegia, Schumannianthus virga- produced to date is the monograph by Schumann tus (Roxb.) Rolfe] and the Donax clade [remaining (1902). In this work, the Asian taxa were referred to Asian genera plus Schumannianthus dichotomus eight different genera: Actoplanes K. Schum. (= Donax (Roxb.) Gagnep.]. Problems with generic delimitation

Lour.), Cominsia Hemsl., Donax (= Schumannianthus were detected in two cases: Schumannianthus was Downloaded from https://academic.oup.com/botlinnean/article/159/3/381/2418341 by guest on 02 October 2021 Gagnep.), Halopegia K. Schum., Monophrynium K. found to be polyphyletic and Phacelophrynium was Schum., Phacelophrynium K. Schum., Phrynium nested within Phrynium. The analysis, however, Willd. and Stachyphrynium K. Schum. Since then, included only a single species of Phacelophrynium. generic concepts have remained essentially unalt- Prince & Kress (2006b) found the same five major ered (Andersson, 1998) and only nomenclature has clades in an analysis of a more limited taxon sample changed. but including data from eight DNA regions represent- The Marantaceae have traditionally been divided ing the plastid (matK, ndhF, rbcL, rps16 intron and into two tribes: Phrynieae Petersen with three fertile trnL-trnF intergenic spacer), mitochondrial (cox1) and ovary locules and Maranteae Meisn. with one fertile nuclear genomes [internal transcribed spacer (ITS) ovary locule (Petersen, 1889). An alternative classifi- region and the 5′-end of 26S]. cation was proposed by Andersson (1998), who divided In this paper, we present a densely sampled phy- the family into five informal groups based on inflo- logeny for Asian Marantaceae based on a combination rescence and floral structures: the Phrynium, of plastid and nuclear DNA sequences. The taxon Calathea, Donax, Maranta and Myrosma groups. sample covers all Asian genera and more than 75% of According to this classification, the SE Asian genera the species currently known from that continent, belonged to two different groups: (1) the Phrynium several represented by more than one accession. The group (Phrynium, Monophrynium, Phacelophrynium specific objectives of the study were (1) to reconfirm and Stachyphrynium), characterized by flower groups the position of the Asian members within the family (‘cymules’) with strongly condensed axes (brachy- using a large taxon sample and (2) to address the blastic) or with slightly extended axes (moderately unsettled questions concerning generic delimitation dolichoblastic), bracteole absent, interphylls usually using a combination of plastid and nuclear genome present, corolla tube short or long and 1–2 outer markers. staminodes; and (2) the Donax group (Donax and Schumannianthus), characterizd by flower groups with extended axes, interphyll absent, a small, glan- MATERIAL AND METHODS dular bracteole present, corolla tube short (rarely TAXON SAMPLING AND DATASETS moderately long) and two outer staminodes. Two Forty-eight Asian and five non-Asian Marantaceae Asian genera, Halopegia and Cominsia, were left by samples were sequenced for the plastid rps16 intron, Andersson as ‘genera of uncertain affinity’. nuclear ITS1 and 5S-non-transcribed spacer (NTS). Andersson & Chase (2001) published the first For the rps16 intron, we additionally downloaded densely sampled phylogenetic study of Marantaceae, sequences for 42 Marantaceae and ten other members including both morphological and molecular data of Zingiberales from GenBank. Most of these (plastid DNA rps16 intron) for 59 species of Maran- sequences form part of the data set studied by Ander- taceae in 21 genera. The results showed that neither sson & Chase (2001). Finally, one additional non- the traditional subdivision of Marantaceae into a trio- Asian sample [Marantochloa filipes (Benth. & Hook. vulate (Phrynieae) and uniovulate (Maranteae) tribe f.) Hutch.] was sequenced for the rps16 intron and (Petersen, 1889) nor the five informal groups pro- included in the family level analysis. A complete list posed by Andersson (1998) were natural. Only the of plant accessions, voucher specimens and GenBank Calathea and Myrosma groups were monophyletic, accession numbers is given in Table 1. The data were the Maranta and Phrynium groups were polyphyletic organized into three datasets: and the Donax group formed a grade involving a number of independent evolutionary lineages within 1. Family level rps16 intron dataset, with sequence the family. Prince & Kress (2006a) analysed a larger data for 95 ingroup samples from the Marantaceae sample of taxa [80 accessions in 27 genera; only four (one of the 48 Asian samples failed to produce genera (Monophrynium, Monophyllanthe, Myrosma a useful rps16 intron sequence, see RESULTS),

Table 1. Source and GenBank accession numbers for sequences used in this analysis

Taxon Source/voucher rps16 ITS1 5S-NTS

Outgroup Canna aff. indica L. GenBank AF141039 – – Costus woodsonii Maas GenBank AF141040 – – Cautleya gracilis (Sm.) Dandy GenBank AF414550 – – Ensete superbum (Roxb.) Cheesman GenBank AF141046 – – Globba sp. GenBank AF141047 – – Heliconia solomonensis W. J. Kress GenBank AF430116 – – Downloaded from https://academic.oup.com/botlinnean/article/159/3/381/2418341 by guest on 02 October 2021 Heliconia rostrata Ruiz & Pav. GenBank AF141050 – – Orchidantha ﬁmbriata Holttum GenBank AF430098 – – Orchidantha siamensis K. Larsen GenBank AF430106 – – Zingiber officinale Roscoe GenBank AF141095 – – Ingroup Afrocalathea rhizantha K. Schum. A. Ley 7 (WAG) EF382847 EF382839 EF382835 Ataenidia conferta (Benth.) Milne-Redh. I Grown in Botanic AY914603 AY914649 – Garden Copenhagen, no voucher Ataenidia conferta (Benth.) Milne-Redh. II GenBank AF141024 – – Calathea altissima Horan. GenBank AF141025 – – Calathea capitata Lindl. GenBank AF141026 – – Calathea crotalifera S. Watson GenBank AF141027 – – Calathea cylindrical K. Schum. GenBank AF141028 – – Calathea lancifolia Boom GenBank AF141029 – – Calathea metallica Körn. ex Regel GenBank AF141030 – – Calathea micans Körn GenBank AF141031 – – Calathea picturata K. Koch & Linden GenBank AF141033 – – Calathea splendida Hort. Ex Correa GenBank AF141036 – – Calathea veitchiana J. J. Veitch F. Borchsenius AY914604 AY914151 – 673 (AAU) Calathea zebrine Lindl. GenBank AF141038 – – Cominsia gigantean (Scheff.) K. Schum. Dissing et al. EF382848 EF382840 – 1862 (C) Ctenanthe burle-marxii H. Kenn. GenBank AF141041 – – Ctenanthe dasycarpa K. Schum. GenBank AF141042 – – Donax canniformis (G. Forst.) K. Schum. I P. Suksathan AY914616 AY914663 AY914704 3306 (QBG) Donax canniformis (G.Forst.) K. Schum. II Origin Borneo, no AY914617 AY914662 AY914705 voucher Donax canniformis (G.Forst.) K. Schum. III GenBank AF141045 – – Halopegia azurea K. Schum. GenBank AF141048 – – Halopegia blumei (Körn.) K. Schum. P. Suksathan AY914605 AY914150 – 3429 (QBG) Hylaeanthe hoffmannii (K. Schum.) Jonker GenBank AF141051 – – Hypselodelphys violacea (Ridl.) Milne-Redh. GenBank AF141052 – – Ischnosiphon leucophaeus (Poepp. & Endl.) Körn. GenBank AF141053 – – Ischnosiphon ovatus Körn. GenBank AF141054 – – Koernickanthe orbiculata (Körn.) L.Andersson GenBank AF141055 – – Maranta kerchoviana E. Morren GenBank AF141056 – – Maranta massangeana E. Morren GenBank AF141058 – – Maranta protracta Miq. GenBank AF141059 – – Maranta ruiziana Körn. GenBank AF141060 – – Maranta sobolifera L. Andersson GenBank AF141061 Marantochloa congensis (K. Schum.) J.Leonard & GenBank AF141062 – – Mullend.

Table 1. Continued

Taxon Source/voucher rps16 ITS1 5S-NTS

Marantochloa cuspidata (Roscoe) Milne-Redh. GenBank AF141063 – – Marantochloa filipes (Benth. & Hook. f.) Hutch. GenBank AF141064 Marantochloa flexuosa (Benth.) Hutch. F. Borchsenius AY914622 – – 672 (AAU) Marantochloa leucantha (K. Schum.) Milne-Redh. GenBank AF141066 – – Monophrynium fasciculatum (Presl.) K. Schum. P. Suksathan AY914646 AY914691 AY914732 3419 (QBG) Downloaded from https://academic.oup.com/botlinnean/article/159/3/381/2418341 by guest on 02 October 2021 Monophrynium simplex Elmer P. Suksathan AY914647 AY914692 AY914733 3525 (AAU, PNH, QBG) Monotagma densiflorum K. Schum. GenBank AF141068 – – Monotagma dolosum J. F. Macbr. GenBank AF141069 – – Myrosma cannifolia L.f. GenBank AF141070 – – Phacelophrynium aurantium Clausager & S. Johannsen 12 AY914623 AY914668 AY914709 Borchs. (AAU, SAN) Phacelophrynium cylindricum Merr. P. Suksathan AY914624 AY914669 AY914710 3531 (AAU, PNH, QBG) Phacelophrynium interruptum Warb. ex K. P. Suksathan AY914625 AY914670 AY914711 Schum. 3409 (QBG) Phacelophrynium laxum Clausager & Borchs. S. Johannsen 16 AY914626 AY914671 AY914712 (AAU, SAN) Phacelophrynium maximum (Blume) K. Schum. I S. Johannsen 9 AY914627 AY914672 AY914713 (AAU, SAN) Phacelophrynium maximum (Blume) K. Schum. P. Suksathan AY914628 AY914673 AY914714 II 3530 (AAU, PNH, QBG) Phacelophrynium maximum (Blume) K. Schum. Origin Borneo, no AY914629 AY914674 AY914715 III voucher Phacelophrynium maximum (Blume) K. Schum. A.D. Poulsen EF382850 EF382842 EF382836 IV 2277 (AAU) Phacelophrynium sapiense Clausager, Mood & S. Johannsen 25 AY914630 AY914675 AY914719 Borchs. (AAU, SAN) Phacelophrynium sp. 1 de Vogel 6721 EF382849 EF382841 (failed) (NY) Phrynium fissifolium Ridl. J. Mood 2050 EF382851 EF382843 EF382837 (AAU) Phrynium grandibracteatum Clausager & S. Johannsen 11 AY914631 AY914676 AY914720 Borchs. (AAU, SAN) Phrynium hainanense T.L.Wu & S. J. Chen P. Suksathan AY914632 AY914677 AY914721 2967 (AAU, QBG) Phrynium hirtum Ridl. S. Johannsen 3 AY914633 AY914678 AY914722 (AAU, SAN) Phrynium imbricatum Roxb. I P. Suksathan AY914634 AY914679 AY914723 3357 (QBG) Phrynium imbricatum Roxb. II P. Suksathan AY914635 AY914680 AY914724 3542 (QBG) Phrynium kaniense Loes. & G. M. Schulze L.J. Brass 5190 (failed) EF382844 (failed) (NY) Phrynium macrocephalum K. Schum. M. Lovave 144 EF382852 EF382845 EF382838 (AAU) Phrynium obscurum Teijsm. & Binn. P. Suksathan AY914636 AY914681 AY914725 3326 (QBG)

Table 1. Continued

Taxon Source/voucher rps16 ITS1 5S-NTS

Phrynium pedunculiferum D. Fang P. Suksathan AY914637 AY914683 AY914726 3399 (QBG) Phrynium pubinerve Blume I P. Suksathan AY914638 AY914684 AY914716 3314 (QBG) Phrynium pubinerve Blume II P. Suksathan AY914639 AY914685 AY914717 3318 (QBG) Phrynium pubinerve Blume III A.D. Poulsen AY914640 AY914686 AY914718 Downloaded from https://academic.oup.com/botlinnean/article/159/3/381/2418341 by guest on 02 October 2021 2291 (AAU) Phrynium pubinerve Blume IV GenBank AF141072 – – Phrynium sp. 1 (Vietnam) P. Suksathan AY914644 AY914689 AY914730 3544 (QBG) Phrynium sp. 2 (Vietnam) P. Suksathan AY914645 AY914690 AY914731 3546 (QBG) Phrynium tonkinense Gagnep. P. Suksathan AY914641 AY914682 AY914732 3543 (QBG) Phrynium tristachyum Ridl. P. Suksathan AY914642 AY914687 AY914728 3334 (QBG) Phrynium villosulum Miq. I S. Johannsen 13 AY914643 AY914688 AY914729 (AAU, SAN) Phrynium villosulum Miq. II GenBank AF141073 – – Pleiostachya pruinosa K. Schum. GenBank AF141075 – – Saranthe leptostachya Eichl. GenBank AF141080 – – Sarcophrynium brachystachyum K. Schum. GenBank AF141082 – – Sarcophrynium sp. 1 GenBank AF141084 – – Schumannianthus dichotomus (Roxb.) Gagneg. I S. Johannsen 33 AY914618 AY914665 AY914707 (AAU, SAN) Schumannianthus dichotomus (Roxb.) Gagnep. II P. Suksathan AY914619 AY914664 AY914708 3333 (QBG) Schumannianthus monophyllus Suksathan, A.D. Poulsen AY914621 AY914667 AY914706 Borchs. & A. D. Poulsen 1943 (AAU) Schumannianthus virgatus (Roxb.) Rolfe J. Skornikova AY914620 AY914666 – 84124 (AAU, SING) Stachyphrynium calcicola Clausager & A. D. A.D. Poulsen AY914606 AY914652 AY914694 Poulsen et al. 2026 (AAU) Stachyphrynium latifolium (Blume) K. Schum. I P. Suksathan AY914607 AY914653 AY914695 3328 (QBG) Stachyphrynium latifolium (Blume) K. Schum. II S. Johannsen 8 AY914608 AY914654 AY914696 (AAU, SAN) Stachyphrynium latifolium (Blume) K. Schum. GenBank AF141085 – – III Stachyphrynium longispicatum Suksathan & P. Suksathan AY914609 AY914655 AY914697 Borchs. 3321 (QBG) Stachyphrynium placentarium (Lour.) Clausager P. Suksathan AY914610 AY914656 AY914698 & Borchs. 2947 (QBG) Stachyphrynium repens (Koern.) Suksathan & P. Suksathan AY914611 AY914657 AY914699 Borchs. I 3307 (QBG) Stachyphrynium repens (Koern.) Suksathan & GenBank AF141086 – – Borchs. II Stachyphrynium sp. 1 (Borneo) A.D. Poulsen AY914615 AY914661 AY914703 et al. 2301 (AAU)

Table 1. Continued

Taxon Source/voucher rps16 ITS1 5S-NTS

Stachyphrynium spicatum (Roxb.) K. Schum. P. Suksathan AY914612 AY914658 AY914700 3356 (QBG) Stachyphrynium sumatranum K. Schum. I S. Johannsen 10 AY914613 AY914659 AY914701 (AAU, SAN) Stachyphrynium sumatranum K. Schum. II A.D. Poulsen AY914614 AY914660 AY914702 et al. 2256 (AAU) Downloaded from https://academic.oup.com/botlinnean/article/159/3/381/2418341 by guest on 02 October 2021 Stromanthe jacquinii (Roem. & Schult.) H.Kenn. GenBank AF141087 – – & Nicolson Thalia dealbata Fraser F. Borchsenius AY914648 AY914693 (failed) 671 (AAU) Thalia geniculata L. I F. Borchsenius EF382853 EF382846 (failed) 670 (AAU) Thalia geniculata L. II GenBank AF141092 – – Trachyphrynium braunianum (K. Schum.) Baker GenBank AF141093 – –

Voucher specimens are only listed for samples sequenced in this study. ITS, internal transcribed spacer; NTS, non-transcribed spacer.

representing 79 different species in 26 genera, and DNA polymerase or PCR Beads (Pharmacia) accord- ten outgroup samples representing six other fami- ing to the manufacturer’s directions. Thermal cycling lies of the Zingiberales. was performed in 32 cycles of 95 °C for 30 s, 59 °C for 2. Stachyphrynium combined dataset, with sequence 1 min and 72 °C for 2 min (rps16 intron); 29 cycles of data for the rps16 intron, ITS1 and 5S-NTS 94 °C for 30 s, 55 °C for 1 min and 72 °C for 1 min regions for ten samples of Stachyphrynium repre- (ITS1); 26 cycles of 94 °C for 1 min, 65 °C for 1 min senting eight species and one sample of Afroca- and 72 °C for 2 min (5S). All PCR products were lathea rhizantha K. Schum. (ingroup 11 total) checked by gel electrophoresis. When multiple bands and four outgroup samples from other clades of were detected, the target band was cut out of the Marantaceae, including Ataenidia conferta gel and purified using QIAquick gel extraction kit (Benth.) Milne-Redh., a representative of the sister (Qiagen, Valencia, CA, USA). PCR products were group to Stachyphrynium in the analysis by Prince cleaned using QIAquick spin columns and sequenced & Kress (2006a). Afrocalathea rhizantha was using an ABI 377 Automated DNA sequencer (Applied included among the ingroup taxa as these authors Biosystems, Foster City, CA, USA). For weak signal found it to be nested within Stachyphrynium. sequences, the following internal sequencing primers 3. Donax clade combined dataset, with sequence data were used in addition to the aforementioned ones: rps for the rps16 intron, ITS1 and 5S-NTS regions for int (forward) – 5′-GTATGTTGGTGTCCTTTTGA-3′; 38 ingroup samples representing 30 species and all rps int (reverse) – 5′-ATCATTAGGTTTAGACATTA-3′. genera of the Donax clade and seven outgroup samples representing other clades of Marantaceae. PHYLOGENETIC ANALYSES Contig assembly and sequence editing was performed DNA EXTRACTION AND AMPLIFICATION using Sequencher version 3.0 (Gene Codes, Ann Arbor, Total genomic DNA was extracted using a DNeasy MI, USA). A preliminary alignment was obtained using Plant minikit (Qiagen, Valencia, CA, USA) following the program ClustalW as implemented in BioEdit the manufacturer’s protocol. Amplification of the v7.0.5 and this alignment was subsequently refined by plastid rps16 intron region was accomplished using eye. Missing sequences were coded as unknown char- primers rpsF and rpsR2 (Oxelman, Lidén & Ber- acters in all combined analyses. Indels were coded as glund, 1997). The ITS1 region was amplified using binary characters using the simple gap coding method the universal primers published by White et al. of Simmons & Ochoterena (2000) and included in (1990). The 5S-NTS region was amplified with the the parsimony analysis. To assess the impact of indel 5sp1R and 5sp2F primers (Cox, Bennett & Dyer, characters on phylogenetic resolution, we analysed 1992). All amplifications used either Ampliqon Taq the data with these included and excluded. Fitch’s

© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 159, 381–395 ASIAN MARANTACEAE 387 maximum parsimony (MP) analyses were conducted We used a Shimodaira–Hasegawa likelihood using PAUP* 4b10 for PC (Swofford, 2002) with ratio test (Shimodaira & Hasegawa, 1999; see also unweighted characters, random addition sequence and Goldman, Anderson & Rodrigo, 2000) implemented in ten replicates. In the case of the family level rps16 PAUP 4.10b to measure the effect of three different intron dataset, heuristic search yielded an excessive topological constraints on the Donax clade combined number of trees and a two-step search procedure dataset, representing different possible classification was adopted. First, we conducted 1000 searches with schemes: (1) monophyletic Schumannianthus; (2) random addition sequence, saving up to 20 trees from monophyletic Phrynium; (3) four monophyletic genera each replicate. Second, we swapped the resulting Phrynium, Phacelophrynium, Monophrynium and 20 000 trees with the steepest descent option, in effect Cominsia. For constraints 2 and 3, which involved a saving a total of 20 000 trees. After filtering the trees monophyletic Phrynium, the New Guinean species Downloaded from https://academic.oup.com/botlinnean/article/159/3/381/2418341 by guest on 02 October 2021 (PAUP command: filter best = yes) to avoid the poten- P. macrocephalum K. Schum. was treated as a mem- tial effect of a known bug in PAUP4b10, the latter set ber of Phacelophrynium, because recent observations of trees was used to compute a strict consensus tree. show that it has flowers with only a single outer Bootstrap analyses (Felsenstein, 1985) of the Stachy- staminode and therefore rightly should be transferred phrynium and the Donax clade combined datasets to that genus (M. Simbiak, pers. comm.). The second were performed in PAUP using 1000 replicates and a New Guinean species included in our taxon sample, heuristic search. Bootstrap analysis of the family level P. kaniense Loes. & G. M. Schulze, is poorly known rps16 intron dataset was conducted using 100 000 morphologically and it is uncertain if this should be fast-swap replicates. transferred to Phacelophrynium also. We therefore Prior to combining data partitions for the Stachy- excluded it from the analysis of topological con- phrynium and Donax clade datasets, respectively, we straints 2 and 3. Monophrynium simplex Elmer, an tested for incongruence using a simultaneous parti- endemic Philippine species, was included in Phace- tion homogeneity test (PHT) as implemented in lophrynium because our reinvestigation of floral PAUP4b10. material of that species shows that it has flowers in In addition to MP analyses, we performed Bayesian pairs, not solitary as in Monophrynium. The test analysis (Huelsenbeck & Ronquist, 2001) on all three distribution used to assess the significance of the datasets using MrBayes 3.1. In these analyses, indel likelihood ratio was generated by the re-sampling characters were omitted. For the Stachyphrynium estimated log-likelihood method (RELL; Kishino, and Donax clade combined datasets, the three DNA Miyata & Hasegawa, 1990). The difference in likeli- regions were concatenated into a single partition. hood was calculated between the unconstrained and Molecular evolution models were estimated using constrained MP trees with the highest likelihood. Modeltest 3.7 (Posada & Crandall, 1998) with model choice based on the Akaike information criterion RESULTS (Akaike, 1974). The preferred model was GTR+I+G for the family level rps16 intron dataset and for the The rps16 sequences were obtained for all samples Stachyphrynium combined dataset and TVM+I+G for included in the analysis with the exception of the Donax clade combined dataset. The corresponding Phrynium kaniense, which failed to produce a settings for MrBayes were in all cases Nst = 6 and sequence, probably because of the age of the her- rates = invgamma. Otherwise we used the default barium collection available (Brass 5190, NY, collected prior settings. All analyses were run with two in 1933). For the 5S-NTS region, outgroup sequences replicates, each consisting of four chains. Analysis of could not be aligned with the ingroup and they were the family level rps16 intron dataset was run for coded as unknown in the combined datasets. Two 2 000 000 generations with a burn-in of 200 000 gen- species of Thalia L. and three other accessions from erations (i.e. the number of cycles necessary for the the Donax clade (Phrynium kaniense, Phace- MCMC algorithm to stabilize around a likelihood lophrynium sp. 1, Cominsia gigantean K. Schum.) maximum for representative sampling of topologies failed to produce 5S-NTS sequences and were coded and parameters). Analyses of the Stachyphrynium as unknown in the combined datasets. Good ITS1 and the Donax clade combined datasets were run for sequences were obtained for all samples available. 300 000 generations, with a burn-in of 50 000 genera- The PHT indicated no incongruence between the tions. These settings resulted in close convergence three DNA regions in either the Stachyphrynium between parameter estimates for the two replicates in combined dataset (P = 0.94) or in the Donax clade each analysis. In all cases, one tree was sampled combined dataset (P = 0.42). For this reason, only the every 100 generations and posterior probabilities results of combined analyses are presented. Informa- were estimated from the joint pool of retained trees tion about the number of samples in each analysis, from the two independent runs. sequence lengths, number of characters (total and

© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 159, 381–395 388 P. SUKSATHAN ET AL. informative), number of MP trees and their charac- teristics are given in Table 2.

ANALYSIS OF THE FAMILY LEVEL rps16 Figure INTRON DATASET In the strict consensus tree derived from 20 000 MP trees with indels included, Asian taxa belong to three independent monophyletic lineages (Fig. 1). The ﬁrst is the genus Stachyphrynium, species of which form a strongly supported monophyletic group [91% bootstrap support (BS)], also including the African mono- Downloaded from https://academic.oup.com/botlinnean/article/159/3/381/2418341 by guest on 02 October 2021 typic genus Afrocalathea. This clade in turn forms an unresolved trichotomy with a clade corresponding to the Maranta clade of Prince & Kress (2006a) and a clade including the remaining genera of those authors’ Stachyphrynium clade, i.e. the African genera Marantochloa Brongn. ex Gris and Ataenidia. MP results The second lineage contains the African/Asian genus Halopegia (two species sampled) and the S Asian species Schumannianthus virgatus, which form a clade with 100% BS. This clade in turn is placed as sister to a group of seven South American genera,

Hyleanthe, Koernickanthe, Myrosma, Maranta, Total/ informative Trees Length CI RI Saranthe, Ctenanthe and Stromanthe with 82% BS. The third and largest lineage of Asian Marantaceae includes the six genera Donax, Schumannianthus (two of three spp.), Phrynium, Phacelophrynium, Monophrynium and Cominsia (93% BS). The Ameri- can genus Thalia appears as sister to this clade but Aligned/ informative without bootstrap support. Together these taxa make up the Donax clade of Prince & Kress (2006a). Within the genus Stachyphrynium, a clade of three Bornean–Sumatra species (S. sumatranum K. Schum., Unaligned S. calcicola A. D. Poulsen & Clausager, S. sp. 1) was Sequence length (bp) Indels recovered with 75% BS. Within the Donax clade resolution was poor. The four genera Phrynium, Phace- lophrynium, Monophrynium and Cominsia formed a 45 1279–1538 1785/451 284/138 2 2157 0.62 0.66 Figure 3 clade (from here termed the Phrynium complex), but 15 1273–1416 1567/226 149/56 4 861 0.80 0.67 Figure 2 this had no bootstrap support. Interspeciﬁc relationships within this group were unresolved. Exclusion of indel characters resulted in markedly reduced resolution of the backbone of the phylogeny. 5S-NTS 5S-NTS + The Asian representatives of the Donax clade were + recovered as monophyletic. Stachyphrynium plus rps16 rps16 ITS1 Afrocalathea were recovered as sister to Maran- ITS1 + tochloa plus Ataenidia but without bootstrap support. + Bayesian analysis recovered the same major clades as intron 106 822–910 1234/290 373/180 20 000 1516 0.64 0.78 Figure 1 intron the MP analysis with indels included and further- intron more placed Stachyphrynium plus Afrocalathea as rps16 Combined sister to Marantochloa plus Ataenidia with 0.92 posterior probability (PP).

ANALYSIS OF THE STACHYPHRYNIUM Data sets analysed, sequence and search statistics

COMBINED DATASET clade Combined The MP analysis of these data with indels included Family Stachyphrynium Table 2. Analysis scope DNA regionCI, consistency index; ITS, internal Samples transcribed spacer; MP, maximum parsimony; NTS, non-transcribed spacer; RI, retention index. resulted in four trees (Fig. 2). In the strict consensus Donax

Phrynium imbricatum I Phrynium pubinerve III Phrynium pubinerve II Phrynium pubinerve IV* Phrynium pubinerve I 72 Phrynium imbricatum II - Phrynium sp. 1 (Vietnam) Cominsia gigantea Phrynium macrocephalum Phacelophrynium sp. 1 (Sulawesi) Phrynium fissifolium Phacelophrynium aurantium Phacelophrynium maximum I 89 Phrynium villosulum I - Phrynium villosulum II* Monophrynium fasciculatum Monophrynium simplex Phacelophrynium cylindricum Phacelophrynium laxum Asia 3 Phacelophrynium interruptum - Downloaded from https://academic.oup.com/botlinnean/article/159/3/381/2418341 by guest on 02 October 2021 Phacelophrynium maximum II 51 Phacelophrynium maximum III Phacelophrynium maximum IV Phacelophrynium sapiense Phrynium grandibracteatum Phrynium hainanense Phrynium hirtum Phrynium obscurum 93 Phrynium pedunculiferum 81 Phrynium sp. 2 (Vietnam) Phrynium tonkinense Phrynium tristachyum 67 Donax canniformis III* 100 61 Donax canniformis I 68 99 Donax canniformis II - 100 Schumannianthus dichotomus I 99 Schumannianthus dichotomus II Schumannianthus monophyllus 100 Thalia geniculata I 100 100 Thalia geniculata II* 100 Thalia dealbata America Calathea capitata* 76 Calathea metallica* 73 Calathea picturata* 54 Calathea veitchiana 87 83 - Calathea cylindrica* 99 66 Calathea zebrina* 72 - 99 Calathea lancifolia* 61 Calathea micans* 98 Calathea altissima* America 76 Calathea splendida* 99 Ischnosiphon leucophaeus* 99 90 Ischnosiphon ovatus* 80 92 Pleiostachya pruinosa* 77 Calathea crotalifera* 96 Monotagma densiflorum* 98 Monotagma dolosum* 96 Ctenanthe dasycarpa* 75 74 Stromanthe jacquinii* 87 Ctenanthe burle-marxii* 90 Maranta protracta* 88 Maranta ruiziana* Maranta sobolifera* 92 Saranthe leptostachyum* America 91 Hylaenthe hoffmannii* Koernickanthe orbiculata* 82 Maranta massengeana* Maranta kerchoviana* 73 Myrosma cannifolia* 100 Halopegia azurea* 100 100 Halopegia blumei Asia 2 100 Schumannianthus virgatus 88 Stachyphrynium latifolium I - 94 Stachyphrynium latifolium II 58 Stachyphrynium latifolium III* - 86 Stachyphrynium repens I 59 63 Stachyphrynium repens II* Stachyphrynium longispicatum Stachyphrynium spicatum - Afrocalathea rhizantha Asia 1 94 Stachyphrynium sumatranum I 60 83 91 86 Stachyphrynium sumatranum II 75 80 Stachyphrynium calcicola 88 65 Stachyphrynium sp. 1 (Borneo) Stachyphrynium placentarium 79 Marantochloa congensis* 94 80 67 Marantochloa filipes* 90 90 100 Marantochloa flexuosa Marantochloa leucantha* 100 100 Marantochloa cuspidata* Africa 100 59 Ataenidia conferta I - Ataenidia conferta II* 97 Hypselodelphys violacea* Africa 81 Trachyphrynium braunianum* OUTGROUP 100 Sarcophrynium brachystachyum* Africa 99 Sarcophrynium sp. 1*

Figure 1. Strict consensus of 20 000 most parsimonious trees (MPTs) from the 106 taxon family level rps16 intron data set including indel characters. Numbers above and below the branches are bootstrap support values with indels included and excluded, respectively. Bold branches are those having more than 0.95 Bayesian posterior probabilities. The ten-taxon outgroup consisting of Canna aff. indica (Cannaceae), Costus woodsonii (Costaceae), Cautleya gracilis (Zingiberaceae), Ensete superbum (Musaceae), Globba sp. (Zingiberaceae), Heliconia solomonensis and H. rostrata (Heliconiaceae), Orchidantha ﬁmbriata and O. siamensis (Lowiaceae) and Zingiber officinale (Zingiberaceae) has been pruned.

100 Stachyphrynium sumatranum I 70 100 Stachyphrynium sumatranum II 100 78 Stachyphrynium sp. 1 (Borneo) 98 Stachyphrynium calcicola 98 Stachyphrynium spicatum 90 65 99 Stachyphrynium longispicatum 80 68 Stachyphrynium repens I - Stachyphrynium latifolium I 100 - 100 100 100 Stachyphrynium latifolium II Stachyphrynium placentarium

Afrocalathea rhizantha Downloaded from https://academic.oup.com/botlinnean/article/159/3/381/2418341 by guest on 02 October 2021 Ataenidia conferta 55 Calathea veitchiana - Thalia dealbata

Schumannianthus virgatus OUTGROUP

Figure 2. Strict consensus of four most parsimonious trees (MPTs) from the 15 taxon combined rps16 intron + ITS1 + 5S- NTS data set for Stachyphrynium including indel characters. Numbers above and below the branches are bootstrap support values with indels included and excluded, respectively. Bold branches are those having more than 0.95 Bayesian posterior probabilities. ITS, internal transcribed spacer; NTS, non-transcribed spacer. tree Afrocalathea was recovered as sister to a well- Exclusion of indel characters changed the topology supported monophyletic Stachyphrynium (90% BS). only a little. The sister-group relationship between Three Bornean species (S. calcicola + S. suma- S. monophyllus and the Phrynium complex was tranum + S. sp. 1) formed a clade with 100% BS. not recovered and species groups 6–8 formed a tri- Stachyphrynium spicatum K. Schum. and S. longispi- chotomy. In addition, S. dichotomus and Donax can- catum Suksathan & Borchs. were recovered as sister niformis formed a clade with 52% bootstrap support. species with 98% BS. Exclusion of indel characters Bayesian analysis placed S. monophyllus as sister to did not change the topology, except for placing S. all other Asian members of the Donax clade and placentarium (Lour.) Clausager & Borchs. as sister to resolved S. dichotomus and D. canniformis as a grade the remaining taxa of its clade, and bootstrap support below a monophyletic Phrynium complex. Within the values obtained with and without indel characters latter complex, only a single change in topology was were similar (Fig. 2). The topology of the 50% major- observed in species group 8 where Phacelophrynium ity rule consensus tree resulting from Bayesian sp. from Sulawesi was unresolved relative to analysis was identical to the strict consensus topology Monophrynium fasciculatum and a clade formed by from MP analysis with indels excluded. the remaining three taxa. Posterior probabilities for clades were in general higher than the corresponding MP–BS values. ANALYSIS OF THE DONAX CLADE COMBINED DATASET MP analysis of these data with indels included TOPOLOGICAL CONSTRAINTS resulted in two trees (Fig. 3). The analysis gave 100% The Shimodaira–Hasegawa test failed to reject the BS for the monophyly of the Asian members of the null hypothesis of a monophyletic Schumannianthus Donax clade and 52% BS for a sister relationship (excluding S. virgatus; P = 0.12). A monophyletic between that clade and Thalia. The four genera of Phrynium, excluding its New Guinea members (P. the Phrynium complex (Phrynium, Phacelophrynium, macrocephalum K. Schum., P. kaniense), was also not Cominsia and Monophrynium) formed a clade with rejected (P = 0.11). However, the test clearly rejected a 92% BS. None of these four genera was resolved as classification maintaining the four genera of the monophyletic. Instead, eight monophyletic groups of Phrynium complex as currently defined (P = 0.001). one to four species each could be recognized (Fig. 3). Seven of these has BS > 80% and the last (group 3) DISCUSSION had 60% BS. Schumannianthus monophyllus was resolved as sister to the Phrynium complex but Our analyses of the family level rps16 intron dataset with no BS. Schumannianthus dichotomus formed a corroborate the results of Prince & Kress (2006a) in trichotomy with Donax canniformis and the clade finding that Asian Marantaceae are made up by three formed by S. monophyllus plus the Phrynium well-supported monophyletic lineages: (1) the genus complex. Stachyphrynium; (2) Halopegia and Schumannian-

100 Monophrynium simplex 70 100 Phacelophrynium interruptum 8. Philippines - 81 Phacelophrynium cylindricum and Wallacea 80 Phacelophrynium sp. 1 (Sulawesi) Monophrynium fasciculatum 73 Cominsia gigantea 92 56 Phrynium kaniense 7. New Guinea 67 Phrynium macrocephalum 94 Phacelophrynium aurantium 74 78 Phacelophrynium maximum I 94 64 99 Phacelophrynium maximum II 6. West Malesia 82 99 Phacelophrynium maximum III 57 Phacelophrynium maximum IV 97 Phacelophrynium laxum 51 Downloaded from https://academic.oup.com/botlinnean/article/159/3/381/2418341 by guest on 02 October 2021 95 Phacelophrynium sapiense 5. Borneo 100 Phrynium imbricatum II 90 100 Phrynium sp. 1 (Vietnam) 93 100 Phrynium imbricatum I 100 69 Phrynium pubinerve I 4. Widespread 100 78 Phrynium pubinerve III 100 Phrynium pubinerve II 64 Phrynium villosulum I 100 62 Phrynium hirtum 60 99 Phrynium fissifolium 3. West Malesia 52 80 Phrynium tristachyum 92 77 Phrynium obscurum 92 Phrynium grandibracteatum 2. Borneo 99 Phrynium hainanense 60 90 96 Phrynium pedunculiferum - 100 57 Phrynium tonkinense 1. Indochina 100 100 Phrynium sp. 2 (Vietnam) 100 Schumannianthus monophyllus 100 Donax canniformis I 52 100 Donax canniformis II 72 100 Schumannianthus dichotomus I 100 Schumannianthus dichotomus II 100 Thalia dealbata 100 Thalia geniculata I 66 Stachyphrynium latifolium II 100 73 Stachyphrynium spicatum 100 Stachyphrynium placentarium 60 100 Halopegia blumei 100 68 Schumannianthus virgatus Ataenidia conferta OUTGROUP Calathea veitchiana

Figure 3. Strict consensus of two most parsimonious trees (MPTs) from the 45 taxon combined rps16 intron + ITS1 + 5S- NTS data set for the Donax clade including indel characters. Numbers above and below the branches are bootstrap support values with indels included and excluded, respectively. Bold branches are those having more than 0.95 Bayesian posterior probabilities. ITS, internal transcribed spacer; NTS, non-transcribed spacer. thus virgatus; and (3) the remaining six Asian genera to western Malesia. Eight species, including one (Donax, two species of Schumannianthus, Phrynium, undescribed taxon recently discovered in Sarawak Phacelophrynium, Monophrynium and Cominsia). By (Stachyphrynium sp. 1), are included in this study increasing the taxon sample, realigning the dataset and some are represented by more than one sample. and coding all gaps, we obtained increased support for Stachyphrynium was at one time believed to be the latter clade relative to the analysis of rps16 intron closely related to Phrynium (Andersson, 1998), but data conducted by Andersson & Chase (2001), 93% BS this and other phylogenetic studies (Andersson & (Fig. 1) vs. 81% jackknife support in that study based Chase, 2001; Prince & Kress, 2006a, b) suggest that it on molecular data alone. Our bootstrap consensus is related to the African genera Afrocalathea, Maran- tree is, however, fully congruent with the jackknife tochloa and Ataenidia. The analysis by Prince & consensus tree presented by Andersson & Chase. Kress (2006a) suggested that Afrocalathea should be merged with Stachyphrynium. Our analyses of com- STACHYPHRYNIUM bined data for Stachyphrynium (Fig. 2) support the The genus Stachyphrynium consists of nine species monophyly of the genus. Andersson (1998) stressed ranging from Sri Lanka and India through Indochina the combination of a long corolla tube and short

© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 159, 381–395 392 P. SUKSATHAN ET AL. sepals (maximum one-third of the length of the The basal relationships among the Asian members corolla tube, but usually much shorter) as a unique of the Donax clade are not resolved in our study. Four character combination for Stachyphrynium.InAfro- independent lineages, represented by D. canniformis, calathea sepals are more than half the length of the S. dichotomus, S. monophyllus and a large clade corolla tube (Schumann, 1902). including the reamaining taxa (the Phrynium complex: Phrynium, Phacelophrynium, Monophry- HALOPEGIA AND SCHUMANNIANTHUS VIRGATUS nium and Cominsia) form different constellations in the different analyses and bootstrap support is always Halopegia is the only genus of Marantaceae that is low. The poor resolution of the relationship between distributed in both Africa and Asia. It includes three Donax and Schumannianthus is perhaps somewhat species, one in the Congo basin (H. azurea K. Schum.), surprising, as both genera possess a specialized glan- Downloaded from https://academic.oup.com/botlinnean/article/159/3/381/2418341 by guest on 02 October 2021 one in Madagascar (H. perrieri Guillaumin) and one dular bracteole associated with the flowers that would (H. blumei K. Schum.) with a disjunct distribution in seem to be a synapomorphy as it is absent in Thalia SE Asia (Myanmar, Thailand, Cambodia) and Java. and the Phrynium complex. The bracteole is trans- Schumann (1902) distinguished Halopegia mainly by formed into an extrafloral nectary which functions to its unique, strongly dimorphic sepals. The two species attract aggressive ants that protect the flowers and of Halopegia included in the family level rps16 intron young fruits during their development. The occur- dataset form a strongly supported monophyletic group rence of dolichoblastic flower groups in both genera placed as sister to the South Indian species S. virgatus (i.e. with flower-bearing axes extended and clearly (Fig. 1). Halopegia and S. virgatus differ in a number perceptible) is another shared character, but if Thalia of aspects, e.g. habit (rosulate in Halopegia vs. caules- is regarded as the sister group to the remainder of the cent in S. virgatus), inflorescence structure (a robust Donax clade then that character must be regarded as main axis with none or few branches enveloped by the plesiomorphic. Prince & Kress (2006a) found strong leaf sheath in Halopegia vs. with numerous flimsy, support for a sister relationship between D. cannifor- fully exposed branches in S. virgatus) and flowers mis and S. dichotomus, but these authors did not (sepals dimorphic only in Halopegia). The two groups include the recently discovered Bornean endemic are therefore best regarded as separate genera. S. monophyllus in their analysis. That species was Studies of recently collected material of S. virgatus described as a Schumannianthus by Suksathan et al. also show that this taxon does not posses the glandular (2006) because of its capsular fruit (vs. berry in bracteoles otherwise characteristic of the genus Schu- Donax), but it has a different habit, being a rosulate mannianthus. The conclusion is that S. virgatus plant rather than with emergent, branching stems, should be removed from Schumannianthus and trans- and its flowers resemble those of Donax in having a ferred to a new genus. short staminal tube, rather than the long staminal tube of S. dichotomus. The 5S-NTS sequences are of THE DONAX CLADE comparable lengths in S. monophyllus and in the The Donax clade sensu Prince & Kress (2006a) com- Phrynium complex (c. 420 bp), whereas in D. canni- prises seven genera of which one is American (Thalia) formis and S. dichotomus they are some 160 bp and the remaining Asian (Donax, Schumannianthus, shorter. The sequences could perhaps represent dif- Phrynium, Phacelophrynium, Monophrynium and ferent paralogues. Short sequences were, however, Cominsia). The six Asian genera together comprise 43 never obtained in the Phrynium complex and long species corresponding to more than 70% of all species sequences were never obtained from D. canniformis of Marantaceae in Asia. A monophyletic Donax clade or S. dichotomus. The application of topological was recovered in analysis of both the rps16 intron constraints to the tree shows that a monophyletic family level dataset (Fig. 1) and the Donax clade Schumannianthus (excluding S. virgatus) cannot be combined dataset (Fig. 3), but with missing or low refuted by our data. However, no analysis indicates bootstrap support. The results of Andersson & Chase a sister relationship between S. dichotomus and (2001) placed Donax and Thalia in a grade close to S. monophyllus. Further studies are needed to deter- the base of the tree, whereas Phrynium was placed as mine whether the latter taxon should be placed in a sister to four South American genera. This result, genus of its own. however, relied on morphological rather than molecu- Within the Donax clade, the four genera, Phrynium, lar data. Analysis of molecular data alone placed Phacelophrynium, Monophrynium and Cominsia form Donax as sister to Phrynium with 81% jackknife a well-supported monophyletic group. This group support. Prince & Kress (2006a, b) found a monophyl- includes 40 species (including some recently discov- etic Donax clade with Thalia as sister to the Asian ered and still-undescribed species from Vietnam and taxa with 68% and 52% BS, respectively, in their New Guinea), distributed from NW India to the analyses of combined data. Solomon Islands. Generic limits within this group have

© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 159, 381–395 ASIAN MARANTACEAE 393 traditionally been defined by a few key characters REVISED GENERIC CLASSIFICATION OF (Schumann, 1902; Holttum, 1951), namely the ASIAN MARANTACEAE arrangement of inflorescence bracts (spiral in 1. Stachyphrynium K. Schum., in Engler, Pflan- Phrynium vs. distichous in Phacelophrynium), the zenr. 4(48): 45 (1902). Nom. cons. prop., Taxon 54: number of outer staminodes (one in Phacelophrynium, 833–834. Phyllodes Lour. Fl. Cochinch. 16 (1790). two in the other genera), the number of flowers per Nom. rej. prop. [ibid.]. flower group (one in Monophrynium, two in the other Rosulate herbs. Flower groups brachyblastic (i.e. with genera) and the length of the corolla tube (extremely axes strongly condensed ), two-flowered, interphylls long in Cominsia; short to moderately long in the other present or absent, bracteoles absent, sepals one-third genera). Our analysis does not support the current the length of corolla tube or much shorter, corolla generic classification. Rather than four monophyletic Downloaded from https://academic.oup.com/botlinnean/article/159/3/381/2418341 by guest on 02 October 2021 tube equalling lobes or longer, outer staminodes 2, genera, we recovered eight more or less well-supported anther appendage hood-like. Ovary with three fertile species groups, each with a strong geographic focus locules. Fruit one- to two-seeded, dehiscent. Nine (Fig. 3). In some cases, morphological characters cor- species, India to Borneo. roborate these groups; for example, the clade of the Indochinese species (group 1) all have cup-shaped 2. Halopegia K. Schum., Engler, Pflanzenr. 4(48): 49 corolla tube and caducuous capsule walls. In other (1902). cases, the results indicate extreme diversification Rosulate herbs. Flower groups dolichoblastic (with between closely related clades; for example, small axes expanded), two-flowered, interphylls and bract- flowers with a short corolla tube in the Philippine eoles absent, sepals strongly dimorphic, corolla tube species (group 8) vs. large flowers with an extremely short, outer staminodes 2. Ovary with three fertile long corolla tube in the New Guinean ones (group 7). locules. Fruit one-seeded, indehiscent, caryopsis-like. A central question raised by the findings of this Three species, Madagascar, Congo Basin and study is how to revise the generic classification of the Myanmar–Thailand–Cambodia plus Java). Phrynium complex. On the one hand, our current data 3. Indianthus Suksathan & Borchs. gen. nov. Type: are not sufficiently strong to reject statistically the Phrynium virgatum Roxb., Asiat. Res. 11: 324 (1810) possibility that Phrynium as currently defined could be [Syn: Schumannianthus virgatus (Roxb.) Rolfe, J. monophyletic. On the other hand, no tree in any of our Bot. 45: 244 (1907).] analyses, individual or combined, indels included or Herbae caulescentes, caulibus simplicibus fascicula- excluded, recovered Phrynium or any substantial part tis. Folia alterna, petiolis brevibus. Gregae florium of that genus as monophyletic and the current classi- dolichoblastae bracteolis carentibus. Staminodia fication with four genera was clearly refuted by the externa 2. Ovarium perfecte triloculare. Fructus Shimodaira–Hasegawa test. If Phrynium is main- 3-seminalis, dehiscens. tained in its current form, then the remaining taxa Caulescent herbs with clustered, simple stems, to could be united into a single genus, for which the name 4 m tall. Leaves alternate, evenly spaced, arranged in Phacelophrynium would apply, or they might be split two opposite rows; petiole short, less than 3 cm long. into three groups (Fig. 3): a west-Malesian Phace- Inflorescence a lax-flowered, terminal panicle. Flower lophrynium (groups 5–6); a New Guinean Cominsia groups dolichoblastic, interphylls and bracteoles (group 7); and a Philippine–Wallacean Monophrynium absent, corolla tube inconspicuous, outer staminodes (group 8). The three genera would, however, have to be 2, fertile stamen with a conspicuous petaloid append- completely re-circumscribed and we know of no mor- age. Ovary with three fertile locules. Fruit three- phological synapomorphies that could be used to define seeded, dehiscent. One species, S India and Sri them. A four-genus classification is therefore unattrac- Lanka: Indianthus virgatus (Roxb.) Suksathan & tive and unjustified at this stage. Maintaining the Borchs. comb. nov., basionym Phrynium virgatum current artificial classification, however, is also unsat- Roxb., Asiat. Res. 11: 324 (1810). isfactory, as it would necessitate the transfer of, for example, Phrynium macrocephalum to Phace- 4. Donax Lour., Fl. Cochinch. 1: 11. (1790). lophrynium, in spite of explicit molecular evidence that Caulescent herbs with tall, branching stems. Flower it is more closely related to Cominsia. We therefore groups dolichoblastic, two-flowered, interphylls find that the best solution to the problem is to merge absent, bracteoles present, small and glandular, the four genera of the Phrynium complex into one. corolla tube equalling lobes, staminal tube incon- Such a classification eliminates false indications of spicuous, outer staminodes 2. Ovary with three fertile relationships signalled by current generic limits and locules. Fruit one- to two-seeded, indehiscent. One secures a monophyletic taxonomy and nomenclatural species, from India (Andaman Islands) throughout SE stability irrespective of the exact species level relation- Asia to the New Hebrides (Vanuatu) and north to ships that further studies may reveal. Taiwan (Orchid Island).

5. Schumannianthus Gagnep., Bull. Soc. Bot. Phrynium minor (Valeton) Suksathan & Borchs. France, 51: 169 (1904). comb. nov. Basionym: Cominsia minor Valeton, Bull. Similar to Donax, but habit variable (rosulate forest Jard. Bot. Buitenzorg Ser. 3(2): 351 (1920). herbs or caulescent marsh plants), corolla tube half Phrynium rubrum (Valeton) Suksathan & Borchs. the length of the lobes, staminal tube inconspicuous comb. nov. Basionym: Cominsia rubra Valeton, in or long, fruit three-seeded, dehiscent. Two species, Merrill, Interpr. Rumph. Herb. Amboin.: 168 (1917). Myanmar to Borneo. Phrynium congestum (Ridl.) Suksathan & Borchs. comb. nov. Basionym: Monophrynium congestum 6. Phrynium Willd., Sp. Pl., ed. 5 (Willdenow) 1: 17 Ridl., Philipp. J. Sci., C. 4: 197 (1909). (1797). Phrynium simplex (Elmer) Suksathan & Borchs. Cominsia Hemsl., Ann. Bot. (Oxford) 5: 508 (1891). comb. nov. Basionym: Monophrynium simplex Elmer, Downloaded from https://academic.oup.com/botlinnean/article/159/3/381/2418341 by guest on 02 October 2021 Syn. Nov. Leafl. Philipp. Bot. 1: 276 (1908). Monophrynium K. Schum., in Engler, Pflanzenr. Phrynium aurantium (Clausager & Borchs.) Suk- 4(48): 68 (1902). Syn. Nov. sathan & Borchs. comb. nov. Basionym: Phace- Phacelophrynium K. Schum., in Engler, Pflanzenr. lophrynium aurantium Clausager & Borchs., Kew 4(48): 120 (1902). Syn. Nov Bull. 58(3): 653 (2003). Rosulate herbs. Flower groups brachyblastic or Phrynium minutiflorum Suksathan & Borchs. nom. sub-brachyblastic, one- or two-flowered, interphylls nov. Synonym: Phacelophrynium cylindricum Merr., usually present, bracteoles absent, or if present then Philipp. J. Sci., C. 13: 269 (1918). The name only one per flower, sepals ± half the length of corolla Phrynium cylindricum Roscoe is the basionym of tube or longer, corolla tube variable in length, 0.5–3 Calathea cylindrica (Roscoe) K. Schum. The new times the length of the lobes, outer staminodes name has been chosen to reflect that the species has (0–)1–2. Ovary with three fertile locules. Fruit one- to unusually small flowers for the genus. three-seeded, dehiscent. c. 40 species, India to New Phrynium interruptum (Warb. ex K. Schum.) Suk- Guinea and Solomon Islands. sathan & Borchs. comb. nov. Basionym: Phace- The combination of rosulate habit, brachyblastic lophrynium interruptum Warb. ex K. Schum., in flower groups, 0(-1) bracteoles, sepals at least half as Engler, Pflanzenr. 4(48): 121 (1902). long as the corolla tube and an ovary with three Phrynium laxum (Clausager & Borchs.) Suksathan & fertile locules is diagnostic. Rosulate habit and Borchs. comb. nov. Basionym: Phacelophrynium brachyblastic flower groups are shared by several laxum Clausager & Borchs., Kew Bull. 58(3): 656 American genera in the Calathea and Maranta (2003). clades (sensu Prince & Kress, 2006a), but these Phrynium longispicum (Warb. ex K. Schum.) Suk- have either only one fertile locule in the ovary (Mono- sathan & Borchs. comb. nov. Basionym: Phace- tagma, Ischnosiphon, Pleiostachya and all American lophrynium longispica Warb. ex K. Schum., in Engler, genera of the Maranta clade) or (usually) two or more Pflanzenr. 4(48): 122 (1902). bracteoles per flower pair (Sanblasia, Calathea). Phrynium robinsonii (Valeton) Suksathan & Borchs. A few Calathea species, however, lack bracteoles. comb. nov. Basionym: Phacelophrynium robinsonii A character that appears to consistently separate Valeton, in Merrill, Interpr. Rumph. Herb. Amboin.: Phrynium from Calathea is the shape of the trigger 166 (1917). appendage of the hooded staminode. It is elephant-ear Phrynium sapiense (Clausager, J. Mood & Borchs.) shaped in Phrynium but thumb shaped in Calathea Suksathan & Borchs. comb. nov. Basionym: Phace- (Ley, 2008). The African genus Thaumatococcus lophrynium sapiense Clausager, J. Mood & Borchs., differs from Phrynium in having one glandular Nord. J. Bot. 24: 297 (2006). bracteole for each flower pair (Andersson, 1998). Phrynium whitei (Ridl.) Suksathan & Borchs. comb. Stachyphrynium differs in its short sepals (at most nov. Basionym: Phacelophrynium whitei Ridl., Proc. one-third of the corolla tube). Roy. Soc. Queensland 31: 21 (1922).

ACKNOWLEDGEMENTS NEW COMBINATIONS OF ACCEPTED We are grateful to Axel D. Poulsen and Jana Leong- SPECIES NAMES IN PHRYNIUM Škornicˇkova for providing us with valuable DNA Phrynium magniﬁcum Suksathan & Borchs. nom. samples. The ﬁrst author (PS) would like to give nov. Synonym: Cominsia maxima Hatusima, Bot. special thanks to Domingo Madulid, Nguyen Tien Hiep Mag. (Tokyo) 56: 427 (1942). The name Phrynium and Jacinto Regalado for their warm hospitality maximum is occupied [Phrynium maximum Blume; during his visits to the Philippines and Vietnam. syn: Phacelophrynium maximum (Blume) K. Schum.] Thanks are also due to Anni Sloth for her competent

© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 159, 381–395 ASIAN MARANTACEAE 395 help in the laboratory. Linda Prince and John Kress Kress WJ. 1990. The phylogeny and classification of the kindly shared their unpublished results during the Zingiberales. Annals of the Missouri Botanical Garden 77: initial phase of this study. Benjamin Øllgaard made 698–721. the Latin diagnosis of Indianthus. Two anonymous Kress WJ, Prince LM, Hahn WJ, Zimmer EA. 2001. reviewers helped us to significantly improve the first Unraveling the evolutionary radiation of the families of version of this manuscript. This work was supported Zingiberales using morphological and molecular evidence. financially by the DANCED project: ‘Capacity Building Systematic Biology 50: 926–944. in Biodiversity–Queen Sirikit Botanic Garden’ through Ley A. 2008. 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