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Wax Plants Disentangled: a Phylogeny of Hoya (Marsdenieae, Apocynaceae) Inferred from Nuclear and Chloroplast DNA Sequences

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Wax Plants Disentangled: a Phylogeny of Hoya (Marsdenieae, Apocynaceae) Inferred from Nuclear and Chloroplast DNA Sequences Molecular Phylogenetics and Evolution 39 (2006) 722–733 www.elsevier.com/locate/ympev Wax plants disentangled: A phylogeny of Hoya (Marsdenieae, Apocynaceae) inferred from nuclear and chloroplast DNA sequences Livia Wanntorp a,b,¤, Alexander Kocyan a, Susanne S. Renner a a Systematic Botany, Ludwig Maximilians University Munich, Menzinger Strasse 67, D-80638 Munich, Germany b Swedish Museum of Natural History, Box 50007, SE-10405 Stockholm, Sweden Received 13 September 2005; revised 29 December 2005; accepted 9 January 2006 Available online 3 March 2006 Abstract Hoya (Marsdenieae, Apocynaceae) includes at least 200 species distributed from India to the PaciWc Islands. We here infer major spe- cies groups in the genus based on combined sequences from the chloroplast atpB-rbcL spacer, the trnL region, and nuclear ribosomal DNA ITS region for 42 taxa of Hoya and close relatives. To assess levels of ITS polymorphism, ITS sequences for a third of the acces- sions were obtained by cloning. Most ITS clones grouped by species, indicating that speciation in Hoya usually predates ITS duplication. One ITS sequence of H. carnosa, however, grouped with a sequence of the morphologically similar H. pubicalyx, pointing to recent hybridization or the persistence of paralogous copies through a speciation event. The topology resulting from the combined chloroplast and nuclear data recovers some morphology-based sections, such as Acanthostemma and Eriostemma, as well as a well-supported Austra- lian/New Guinean clade. The combined data also suggest that morphological adaptations for ant-symbiosis evolved at least three times within Hoya. © 2006 Elsevier Inc. All rights reserved. Keywords: atpB-rbcL spacer; Bayesian inference; Chloroplast DNA; Hoya; Nuclear ribosomal DNA ITS region; Paralogus; Parsimony; trnL region 1. Introduction genus is generally characterized by persistent inXorescences with Xowers having rotate corollas, staminal coronas with Hoya is a taxonomically complex genus of Xowering revolute margins, pollinia with pellucid margins, and nar- plants distributed from India to the PaciWc Islands (Fig. 1). row, spindle-shaped seeds without conspicuous wings Over 500 names have been published (The Plant Names (Omlor, 1998; this study Fig. 2). Several eVorts have been Project, 1999), and at least 200 species are currently recog- made in the past to subdivide the genus based on morphol- nized (Kleijn and van Donkelaar, 2001), with new ones ogy (Hooker, 1885; Schumann, 1895; Schlechter, 1913, being added every year. The introduction of about 100 spe- 1916), but the only recent such attempts come from the hor- cies of Hoya into the horticultural trade reXects the plants’ ticultural world (Burton, 1985, 1995, 1996; Kloppenburg, large appeal, but the unbridled naming of diVerent forms 1993, 2001a). Because none of these infrageneric classiWca- has led to nomenclatural confusion and heightened the tions is complete or conclusive, many species of Hoya have need for a taxonomic revision, also based on a molecular never been assigned to sections, making appropriate sam- phylogenetic scaVold. pling of the genus for phylogenetic work diYcult. Most species of Hoya are herbaceous lianas with succu- The systematic position of Hoya in the tribe Mars- lent leaves, often growing as epiphytes in the rainforest. The denieae of the Asclepiadoideae (Apocynaceae), on the * other hand, has been settled by molecular phylogenetic Corresponding author. Present address: Department of Botany, studies (e.g., Meve and Liede, 2004; Potgieter and Albert, Stockholm University, Lilla Frescativ. 5, SE-10691 Stockholm, Sweden. Fax: +46 8 162268. 2001; Sennblad and Bremer, 2002). Molecular work has E-mail address: [email protected] (L. Wanntorp). also begun to test the monophyly of Hoya (Wanntorp 1055-7903/$ - see front matter © 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2006.01.022 L. Wanntorp et al. / Molecular Phylogenetics and Evolution 39 (2006) 722–733 723 Fig. 1. Geographical distribution of Hoya. genera Absolmsia, Micholitzia, and Madangia (Wanntorp et al., in press). Although identifying some major clades within Hoya, the information from the chloroplast data obtained to date is, insuYcient to resolve species relation- ships within the genus (Fig. 3). To better resolve the infrageneric structure of Hoya, we resorted to the internal transcribed spacer of nuclear ribo- somal DNA (nrDNA), which is part of the rDNA cistron comprising 18S, ITS1, 5.8S, ITS2, and 26S. Most eukaryotes have several hundred copies of this cistron, with the copies usually undergoing concerted evolution through unequal crossing over and gene conversion, resulting in their homog- enization within individuals, populations, and species (Dover and Tautz, 1986). Studies involving cloning of ITS over the past few years, however, have revealed that incom- pletely homogenized paralogous copies can persist within species or individuals. Biological phenomena explaining the presence of paralogous copies include polyploid genomes (Muir et al., 2001; Volkov et al., 1999; Wendel et al., 1995), multiple nucleolar organizer regions (Bobola et al., 1992; Karvonen and Savolainen, 1993), and highly divergent ITS pseudogenes no longer capable of undergoing normal con- certed evolution (Buckler et al., 1997; Muir et al., 2001; Raz- aWmandimbison et al., 2004). When multiple copies are detected, the ITS region often cannot be used for phyloge- netic purposes unless it can be demonstrated that paralo- gous ITS copies coalesce within species rather than persist Fig. 2. Schematic drawing of Hoya multiXora. (A) Lateral view of Xower. through speciation events (e.g., Bellarosa et al., 2005; Buck- (B) Corona lobe and anther from the inside. (C) Lateral view of corona ler et al., 1997; RazaWmandimbison et al., 2004; Won and and gynostegium (two anthers removed). (D) Pollinarium. 1, corolla; 2, outer corona lobe; 3, inner corona lobe; 4, column; 5, anther wing; 6, Renner, 2005). When facing evidence of polymorphic ITS in anther appendage; 7, style head; 8, pollinium; 9, Caudicle; 10, Retinacu- Hoya, we decided to assess the level of intra-species poly- lum; 11, Pellucid margin. Drawn by H-E. Wanntorp. morphism by cloning the ITS1/5.8S/ITS2 region from about a third of the included accessions. We then analyzed these et al., in press) and Dischidia, one of its closest relatives sequences together with the remaining directly obtained ITS (Livshultz, 2000, 2003). Results for Hoya so far show that sequences and the available chloroplast DNA sequences the genus is paraphyletic unless it includes the monotypic using phylogenetic methods. 724 L. Wanntorp et al. / Molecular Phylogenetics and Evolution 39 (2006) 722–733 Fig. 3. Phylogram showing a 50% majority rule consensus obtained from the Bayesian analysis, based on the trnL region and the atpB-rbcL spacer with bootstrap support >75% shown above branches, and Bayesian posterior probabilities >0.97 below branches. Geographic occurrences are abbreviated as follows: Amb, Ambon; Au, Australia; Bor, Borneo; Br, Brazil; Bu, Burma; Ch, China; Him, Himalaya; In, India; Indo, Indochina; Ja, Japan; Jav, Java; Ma, Malaysia; Mol, Moluccas; NG, New Guinea; Nic, Nicobar; Ph, Philippines; Sam, Samoa; Sol, Solomon Islands; Sri, Sri Lanka; Su, Sumatra; Sul, Sulawesi; Tai, Taiwan; Th, Thailand; Tim, Timor; Van, Vanuatu. (ModiWed from Wanntorp et al., in press.) Morphological adaptations for ant-symbioses occur in press) and covers most of the geographic range and Xower several species of Hoya and Dischidia (Beccari, 1884; Jan- morphological variation on which sections have been based zen, 1974; Livshultz et al., 2005; Treseder et al., 1995). In the (Burton, 1985, 1995, 1996; Hooker, 1885; Kloppenburg, case of Dischidia, Livshultz et al. (2005) has suggested that 1993, 2001a; Schlechter, 1913, 1916). In addition to 35 myrmecophytism may be plesiomorphic, and we were species of Hoya, we included Absolmsia spartioides, Dischi- therefore interested in inferring how many times occupa- dia hirsuta, D. astephana, D. bengalensis, Gunnessia pepo, tion by ants may have arisen in Hoya. The principal goals Madangia inXata, and Micholitzia obcordata (all Mars- of this study were to further clarify intrageneric relation- denieae). Trees were rooted with Marsdenia carvalhoi based ships in Hoya, based on nuclear sequences, and to use the on earlier results (Wanntorp et al., in press). resulting phylogeny to examine the evolution of morpho- Genomic DNA was isolated from fresh or silica gel- logical characters, and of the symbiosis between ants and dried young leaves using DNeasy Plant kits according to species of Hoya. the manufacturer’s protocol (QIAGEN, Valencia, CA, USA). Polymerase change reactions (PCRs) were per- 2. Materials and methods formed with 10 M primers in 25-L reactions using “ready to go” PCR beads from Amersham-Pharmacia Biotech 2.1. Taxon sampling, DNA isolation, ampliWcation and (Uppsala, Sweden). PCRs were set at an initial denatur- sequencing ation for 5 min at 95 °C, followed by 30 cycles of 95 °C for 30 s, 50 °C for 30 s for primer annealing, 72 °C for 2 min for A list of material with voucher information and Gen- primer extension, and 72 °C for 8 min for completion of Bank Accession Nos. is presented in Table 1. The species primer extension, using the primers 18SF (Rydin et al., sample used here is the same as that of Wanntorp et al. (in 2004) and C26A (Yokota et al., 1989). Alternative settings L. Wanntorp et al. / Molecular Phylogenetics and Evolution 39
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