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A Molecular Phylogeny Reveals Widespread Floral Molecular Phylogenetics and Evolution 51 (2009) 100–110 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Pollinators underestimated: A molecular phylogeny reveals widespread floral convergence in oil-secreting orchids (sub-tribe Coryciinae) of the Cape of South Africa Richard J. Waterman a,b,*, Anton Pauw c, Timothy G. Barraclough a, Vincent Savolainen a,b a Division of Biology, Imperial College London, Silwood Park Campus, Ascot, Berkshire SL5 7PY, UK b Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3DS, UK c Department of Botany and Zoology, Stellenbosch University, Private Bag X1, Matieland 7602, South Africa article info abstract Article history: The oil-secreting orchids of southern Africa belong to the sub-tribe Coryciinae within Diseae. A phylogeny Received 18 December 2007 of Diseae is inferred using sequence data from all genera in the tribe, with an emphasis on resolving gen- Revised 2 May 2008 eric classifications within Coryciinae. Nuclear (ITS) and plastid (trnLF and matK) gene region sequences Accepted 13 May 2008 were analysed for 79 ingroup taxa and three outgroup taxa. Coryciinae is confirmed to be diphyletic, with Available online 24 May 2008 Disperis and Coryciinae sensu stricto (s.s.) forming separate monophyletic clades. The current genera Cory- cium and Pterygodium are not monophyletic according to our analysis and we propose a subdivision of Keywords: Coryciinae s.s. into 10 monophyletic clades including three monotypic groups. Previous generic classifi- Ceratandra cations of Coryciinae s.s. have been hampered by convergent evolution of floral parts, a consequence of Convergent evolution Corycium few pollinator species and limited pollinia attachment sites in the oil-bee pollination system common Disperis to this group. Evotella Ó 2008 Elsevier Inc. All rights reserved. ITS matK Oil-secretion Pollination Pterygodium trnLF 1. Introduction ough sampling of Coryciinae has taken place for the purpose of a molecular phylogeny, despite initial molecular studies recognising Made up of five genera and about 112 species, the orchid sub- that Coryciinae ‘‘appears as the keystone sub-tribe in understand- tribe Coryciinae is remarkable for its morphologically complex ing the evolution of Diseae and Orchideae” (Douzery et al., 1999,p. flowers and specialised pollinations systems. Members of Corycii- 897). nae are widespread in the Cape of South Africa and surrounding The sub-tribe was first recognized as the Corycieae by Bentham areas, and together with the other sub-tribes of Diseae account and Hooker (1883). Since then there have been various adjust- for over half of all orchids endemic to southern Africa (Bellstedt ments to the delimitation of the genera (Table 1), but the sub-tribal et al., 2001). Diseae includes five sub-tribes: Coryciinae (112 spe- classification has remained largely undisputed. All previous classi- cies), Disinae (176 species), Satyriinae (91 Species) and the small fications have been heavily reliant on floral morphology—it has of- mono-generic sub-tribes Brownleeinae (7 species) and Huttonaei- ten been considered that the defining feature of the Coryciinae is nae (5 species) (Linder and Kurzweil, 1999; Kurzweil and Manning, the presence of a ‘‘lip appendage” attached to a lip basally fused 2005; Bytebier et al., 2007). Recent molecular phylogenetic trees to the front of the gynostemium (Dressler, 1981; Rolfe, 1913). have been published featuring high proportions of species from However, until relatively recently, the floral morphology was Disinae (Bytebier et al., 2007) and Satyriinae (Van der Niet et al., poorly understood and the function of the lip appendage unknown. 2005; Van der Niet and Linder, 2008). However, to date no thor- In 1989 it was first demonstrated that many Coryciinae produce oil as a floral reward and are pollinated by Rediviva bees (Steiner, 1989). With few exceptions, oil is secreted from the tip of the lip appendage, where it is collected by female Rediviva bees, probably * Corresponding author. Address: Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AB, UK. for use as larval provisions. The diversity of lip appendages is E-mail address: [email protected] (R.J. Waterman). extensive, and the homology of this complex structure remains dif- 1055-7903/$ - see front matter Ó 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2008.05.020 Table 1 Taxa used in this analysis, voucher information and Genbank accession numbers for DNA sequences Taxon Previous taxonomic placement Voucher information GenBank Accession Number Schlechter Rolfe (1913) Stewart et al. trnLF matK ITS (1898) (1982) Outgroups Codonorchis lessonii (d’Urv.) Lindl. Rudall P (1997); Kew DNA Bank DQ415136 DQ414993 0–1398 Ryan A 2 (K) AF348005 Pachyplectron arifolium Schltr. Ziesing 22 (CBG) AJ409434 AJ310051 AF348049 Pterostylis curta R.Br. Chase 572 (K) AJ544507 AJ543951 AJ539526 Brownleeinae Brownleea macroceras Sond. Bytebier B 2293 (NBG, BR, K, NU) DQ415138 DQ414995 DQ414852 Brownleea parviflora Harv. ex. Lindl. Kurzweil, 1972 (MAL, UZL, SRGH) DQ415137 DQ414994 DQ414851 Coryciinae Ceratandra (5 of 6) Ceratandra atrata T. Durand & Schinz Ceratandra Ceratandra Ceratandra Pauw A 25 (BOL) EU301582 EU301529 EU301476 R.J. Waterman et al. / Molecular Phylogenetics and Evolution 51 (2009) 100–110 Ceratandra bicolor Sond. ex. Bolus Ceratandra Evota Evota Pauw A 2 (BOL) EU301594 EU301541 EU301488 Ceratandra globosa Lindl. Ceratandra Ceratandropsis Ceratandra Bytebier B 2451 (BR, NBG) EU301571 EU301518 EU301465 Ceratandra grandiflora Lindl. Ceratandra Ceratandropsis Ceratandra Pauw & Liltved 49 (BOL) EU687540 EU687535 EU687530 Ceratandra harveyana Lindl. Ceratandra Evota Evota Pauw A 6 (BOL) EU301574 EU301521 EU301468 Corycium (11 of 14) Corycium bicolorum (Thunb.) Sw. Pterygodium Corycium Corycium Bytebier B 2725 (NBG) EU301560 EU301507 EU301454 Corycium carnosum (Lindl.) Rolfe Pterygodium Corycium Corycium Pauw A 30 (BOL) EU301577 EU301524 EU301471 Corycium crispum (Thunb.) Sw. Pterygodium Corycium Corycium Pauw A DNA:186 (no voucher) EU301553 EU301500 EU301447 Corycium deflexum (Bolus) Rolfe Corycium Pauw A 32 (BOL) EU301559 EU301506 EU301453 Corycium Corycium dracomontanum Corycium Bytebier B 2302 (BR, GRA, NBG) EU301566 EU301513 EU301460 Parkman & Schelpe Corycium excisum Lindl. Pterygodium Corycium Corycium Pauw A 15 (BOL) EU301587 EU301534 EU301481 Corycium flanaganii (Bolus) Pterygodium Anochilus Anochilus Bytebier B 2466 (NBG, BR, EU301570 EU301517 EU301464 Kurzweil & H.P. Linder GRA, K) Corycium ingeanum E.G.H. Oliver Pauw A 11 (BOL) EU301552 EU301499 EU301446 Corycium microglossum Lindl. Pterygodium Corycium Corycium Pauw A 16 (BOL) EU301579 EU301526 EU301473 Corycium orobanchoides (L. f.) Sw. Pterygodium Corycium Corycium Pauw A 47 (BOL) EU301581 EU301528 EU301475 Corycium nigrescens Sond. Pterygodium Corycium Corycium Bytebier B 2219 (BR, GRA, NBG) EU301567 EU301514 EU301461 Disperis (22 of 74) Disperis anthoceros Rchb. f. Bellstedt 982 EU301573 EU301520 EU301467 Disperis bodkinii Bolus Liltved WR (Compton) EU301576 EU301523 EU301470 Disperis bolusiana subsp. bolusiana Schltr. Bytebier B 2380 (BR, NBG) EU301563 EU301510 EU301457 ex Bolus Disperis bolusiana subsp. macrocorys Rolfe Pauw A DNA:173 (BOL) EU301550 EU301497 EU301444 Disperis capensis var. brevicaudata Rolfe Oliver & Liltved 12443 (NBG) EU687541 EU687536 EU687531 Disperis capensis var. capensis (L. f.) Sw. Pauw A 44 (BOL) EU301593 EU301540 EU301487 Disperis cardiophora Harv. Bytebier B 2278 (BR, NBG) EU301565 EU301512 EU301459 Disperis circumflexa subsp. aemula Pauw A 38 (BOL) EU301556 EU301503 EU301450 (Schltr.) J.C. Manning Disperis circumflexa subsp. circumflexa (L.) Pauw A 41 (BOL) EU301589 EU301536 EU301483 T. Durand & Schinz Disperis concinna Schltr. Ellis A 4 (BOL) EU301597 EU301544 EU301491 Disperis cucullata Sw. Pauw A 40 (BOL) EU301554 EU301501 EU301448 Disperis dicerochila Summerh. Kurzweil, 1983 (MAL, UZL) DQ415139 DQ414996 DQ414853 Disperis fanniniae Harv. Pauw A 50 (BOL) EU687542 EU687537 EU687532 Disperis lindleyana Rchb. f. Kurzweil, 1827 (NBG); Kew DNA EU301601 AY370652 AJ000129 bank 0–696 Disperis macowanii Bolus Pauw A 18 (BOL) EU301575 EU301522 EU301469 Disperis oppositifolia Sm. Sm. MWC (no voucher); Kew EU301602 EU301548 EU301495 DNA bank 23717 Disperis oxyglossa Bolus Ellis A 5 (BOL) EU301600 EU301547 EU301494 Disperis paludosa Harv. ex Lindl. Pauw A 17 (BOL) EU301562 EU301509 EU301456 (continued on next page) 101 Table 1 (continued) 102 Taxon Previous taxonomic placement Voucher information GenBank Accession Number Schlechter Rolfe (1913) Stewart et al. trnLF matK ITS (1898) (1982) Disperis purpurata subsp. Pauw A 26 (BOL) EU301558 EU301505 EU301452 purpurata Rchb. f. Disperis renibractea Schltr. Bytebier B 2251 (BR, K, NBG) EU301564 EU301511 EU301458 Disperis stenoplectron Rchb. f. Edwards & Bellstedt 2308 (NU) DQ415140 DQ414997 DQ414854 Disperis tripetaloides (Thouars) Lindl. RII 593; Kew DNA bank 30985 EU687543 EU687538 EU687533 Disperis tysonii Bolus Ellis A 3 (BOL) EU301599 EU301546 EU301493 Disperis villosa (L.f.) Sw. Pauw A 37 (BOL) EU301588 EU301535 EU301482 Disperis wealei Rchb. f. Ellis A 2 (BOL) EU301598 EU301545 EU301492 Evotella (1 of 1) Evotella rubiginosa (Sond. ex Bolus) Pterygodium Corycium Corycium Pauw A 4 (BOL) EU301561 EU301508 EU301455 Kurzweil & H.P. Linder Pterygodium (16 of 19) Pterygodium acutifolium Lindl. Pterygodium Pterygodium Pterygodium Pauw A 45 (BOL) EU301583 EU301530
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