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A New Genus for Trichosanthes Amara, the Caribbean Sister Species of All Sicyeae

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A New Genus for Trichosanthes Amara, the Caribbean Sister Species of All Sicyeae Systematic Botany (2008), 33(2): pp. 349–355 © Copyright 2008 by the American Society of Plant Taxonomists Linnaeosicyos (Cucurbitaceae): a New Genus for Trichosanthes amara, the Caribbean Sister Species of all Sicyeae Hanno Schaefer, Alexander Kocyan, and Susanne S. Renner1 Systematic Botany, Department of Biology, University of Munich (LMU), Menzinger Strasse 67, D-80638 Munich, Germany 1Author for correspondence ([email protected]) Communicating Editor: Thomas A. Ranker Abstract—The Old World genus Trichosanthes has flowers with strikingly fringed petals, and Linnaeus therefore placed a species from Hispaniola that he only knew from an illustration (showing such fringed petals) in that genus. The species remained hidden from the attention of subsequent workers until acquiring new relevance in the context of molecular-biogeographic work on Cucurbitaceae. Based on molecular data, it is the sister to all Sicyeae, a New World clade of about 125 species in 16 genera. We here place this species in a new genus, Linnaeosicyos, describe and illustrate it, and discuss its phylogenetic context using molecular and morphological data. Judging from Dominican amber, elements of the flora of Hispaniola date back 15–20 my, and the occurrence on the island of at least five endemic species of Cucurbitaceae (Linnaeosicyos amara, Melothria domingensis, Sicana fragrans, and the sister species Anacaona sphaerica and Penelopeia suburceolata) points to its long occupation by Cucurbitaceae. Keywords—Flora of Hispaniola, fringed petals, lectotypification, Linnaeus, Plumier. With about 100 accepted species, Trichosanthes L. is the newly available collections, and discuss the implications of a largest genus of the family Cucurbitaceae (Rugayah and De Hispaniola taxon being sister to the Sicyeae. Wilde 1999; Huang et al. 2007). It is endemic in Asia and Australia, except for T. amara L., a species from the Caribbean ATERIALS AND METHODS island of Hispaniola in the Greater Antilles. Linnaeus (1753) M described T. amara based on an illustration from Plumier’s Morphology—Specimens were borrowed from JBSD, NY, S, and U. All measurements are from dry herbarium specimens. Pollen was taken from Description des plantes de l’Amerique (1693, pp. 86–87) and a single male flower bud, mounted on a carbon film, coated with gold in placed it in the genus Trichosanthes because of its striking a sputter coater (SCD 050, BAL-TEC, Witten, Germany) and observed and fringed petals, otherwise then only known from Trichosan- photographed using a scanning electron microscope (LEO 438 VP, ZEISS, thes. Wild species of Trichosanthes are restricted to eastern Oberkochen, Germany). Taxon Sampling and Sequencing—DNA extraction and sequencing fol- Asia, tropical Australia, and Fiji (Jeffrey 1980, 1990; Rugayah lowed standard procedures, using the rbcL, matK, rpl20–rps12, and trnL and De Wilde 1997, 1999), and Linnaeus only knew them and trnL–F primers and polymerase chain reaction (PCR) protocols listed from illustrations. Thus, he described T. cucumerina and T. in Kocyan et al. (2007). Total genomic DNA was isolated from silica-dried nervifolia from plates in Rheede’s Hortus Indicus Malabricus leaves or from herbarium specimens with a commercial plant DNA ex- traction kit (NucleoSpin, MACHEREY-NAGEL, Düren, Germany), fol- (Jarvis 2007). These species have white flowers with deeply lowing the manufacturer’s manual. PCR Reaction products were purified divided petals, similar to the fringed petals in the Hispaniola using the Wizard SV PCR clean-up kit (PROMEGA GmbH, Mannheim, species. Of the latter, Linnaeus apparently only saw Plu- Germany), and cycle sequencing was performed with BigDye Terminator mier’s plate, a plate also cited by Ray (1704). Because T. amara v3.0 cycle sequencing kit on an ABI Prism 3100 Avant automated se- quencer (Applied Biosystems, Foster City, California). Fifty-eight se- L. was treated in very few floras (with the notable exception quences were newly generated for this study, representing twelve species of Liogier 1986) and was never studied in a broader context, of Trichosantheae not included in our previous studies. Genbank acces- it was never formally excluded from Trichosanthes. The most sion numbers and vouchers are listed in appendix 1. Accession numbers recent monographer of the family, Cogniaux (1881), placed it for all other sequences used for the analyses are given in Kocyan et al. (2007). Parsimony and maximum likelihood analyses were conducted under Species dubiae, and the broadest modern specialist on with the family dataset of Kocyan et al. (2007), which includes 123 of the the family, Charles Jeffrey, suspected that it did not belong in 132 genera of Cucurbitaceae (representing all tribes and subtribes) and Trichosanthes but could not decide in which genus it belonged 171 of the c. 960 species. Additional sequences come from a biogeographi- (C. Jeffrey, St. Petersburg, personal communication, March cal analysis of the Cucurbitaceae (Schaefer and Renner, unpubl.), includ- ing those of the genera Anangia, Austrobryonia, Gomphogyne, Indomelothria, 2006). Pseudosicydium, Urceodiscus, and Zanonia, which augmented our sampling For a molecular phylogenetic study of the family (Kocyan to 130 of 132 genera currently recognized in Cucurbitaceae. The two et al. 2007) we sought to include as many geographically genera of Cucurbitaceae that have not yet been sequenced are Khmeriosi- disjunct entities as possible, which led to the sequencing of cyos De Wilde & Duyfjes, a monotypic genus from Cambodia, known only from the type, and Papuasicyos Duyfjes, a monotypic genus from modern material of T. amara. In the resulting trees, T. amara Papua New Guinea. Judging from their floral morphology, both are ex- was placed closer to the New World clade Sicyeae (125 spe- pected to fall in Benincaseae, far from Trichosanthes, Linnaeosicyos, and the cies in 16 genera) than to any of the three Asian species of Sicyeae. In a second analysis for the present study, we used a reduced Trichosanthes included. Here, we test this result with much dataset of 90 species that represent all tribes, major subtribes, and genera containing Caribbean species. broader sampling of the Trichosantheae (as circumscribed by Sequence Alignment and Phylogenetic Analyses—Sequences were ed- Jeffrey 2005) and conclusively show that Trichosanthes is not ited with Sequencher (4.6; Gene Codes, Ann Arbor, Michigan) and monophyletic, even after exclusion of Linnaeus’s Caribbean aligned by eye, using MacClade 4.06 (Maddison and Maddison 2003). The T. amara. We therefore transfer T. amara to a new genus, aligned plastid matrix comprises 4733 nucleotides after exclusion of a poly-T run in the matK gene, a poly-A and a poly-G run in the trnL intron Linnaeosicyos, redescribe and illustrate the species based on and a TATATA microsatellite region in the trnL–F intergenic spacer. Data matrix and trees have been deposited in TreeBASE (study number S1883). Equally weighted parsimony (MP) analyses for matrices of nucleotides were conducted using PAUP 4.0b10 (Swofford 2002). The search strategy Dedicated to Linnaeus on the occasion of his 300th birthday involved 100 random addition replicates with TBR branch swapping, 349 350 SYSTEMATIC BOTANY [Volume 33 saving all optimal trees. For the parsimony analyses, gaps were treated as missing data. To assess node support, parsimony bootstrap analyses were performed using 1000 replicate heuristic searches, each with 10 random addition replicates and TBR branch swapping, saving all optimal trees. Maximum likelihood (ML) analyses (and ML bootstrap searches) were performed using GARLI 0.951 (Zwickl 2006) available at www.bio.utexas .edu/faculty/antisense/garli/Garli.html and RAxML-VI-HPC v4.0.0 (A. Stamatakis 2006, available at http://phylobench.vital-it.ch/raxml-bb/). GARLI and RAxML searches relied on the GTR+G+Imodel. Model parameters were estimated over the duration of specified runs. To test the phylogenetic position of Trichosanthes (Linneaosicyos) amara, we performed additional ML analyses with constrained topologies that forced the new genus to group with Trichosanthes and compared the likelihood scores of the respective trees with that of the unconstrained tree. RESULTS FIG. 1. Scanning electron microscope photo of the pollen of Linnaeo- Morphologically, Linnaeosicyos matches neither Tricho- sicyos amara (scale bar = 5 ␮m). Collection: García 589 (JBSD). santheae nor Sicyeae. Sicyeae have filaments united into a central column (Jeffrey 1962) and pollen grains that are 4- to coming treatment of the Cucurbitaceae for The Families and 16-colporate or -colpate with a mostly echinate exine or per- Genera of the Vascular Plants series. forate to reticulate exine (Stafford and Sutton 1994; Khunwasi 1998; subtribes Sicyinae and Cyclantherinae, which were Linnaeosicyos H. Schaef. & Kocyan, gen. nov.—TYPE: characterized by these different exine types, are not mutually Trichosanthes amara L., Sp. Pl. 1008. 1753. monophyletic; Kocyan et al. 2007). In Trichosantheae, the fila- Planta cirrhis scandens, corolla alba longe et eleganter fim- ments are free, pollen grains are 3- or 4-colporate or porate, briata, a Trichosanthes differt patria neotropica, foliis minori- but never colpate, and the exine structure is variable (Marti- bus (c. 4.5 × 4.2 cm), pustulis in ambo latere foliorum con- corena 1963; Huang et al. 1997; Pruesapan and van der Ham spicuis orbicularibus albis. 2005). In Linnaeosicyos, the filaments are free as in Trichosan- Perennial dioecious climbers
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