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Molecular Phylogenetic Relationships Within the Subtribe Disinae (Orchidaceae) and Their Taxonomic, Phytogeographic and Evolutionary Implications

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Molecular Phylogenetic Relationships Within the Subtribe Disinae (Orchidaceae) and Their Taxonomic, Phytogeographic and Evolutionary Implications Molecular phylogenetic relationships within the subtribe Disinae (Orchidaceae) and their taxonomic, phytogeographic and evolutionary implications Benny Bytebier Dissertation presented for the degree of Doctor of Philosophy (Biochemistry) at Stellenbosch University Supervisors: Prof. Dirk U. Bellstedt, Stellenbosch University Prof. H. Peter Linder, University of Zurich Department of Biochemistry Stellenbosch University March 2007 Declaration I, the undersigned, hereby declare that the work contained in this dissertation is my own original work and that I have not previously in its entirity or in part submitted it at any university for a degree ………………………… …………………… Signature Date ii Abstract Twenty five years after the last major morphological revision, phylogenetic relationships were inferred on the basis of a new DNA dataset for the African orchid subtribe Disinae, which includes the large genus Disa and the small genus Schizodium. One nuclear gene region (ITS) and two plastid gene regions (trnLF and matK) were sequenced for 136 ingroup, representing 70% of all known Disinae species, as well as for 7 outgroup taxa. The combined data matrix contained 4094 characters and was analysed using parsimony and Bayesian inference. The generic status of Schizodium can no longer be supported, as it is deeply embedded within the genus Disa. Furthermore, the currently recognised subgenera do not reflect the phylogenetic relationships. Several of the currently recognised sections are monophyletic, others contain misplaced elements, while some are polyphyletic. These results necessitate a re-classification of the Disinae. A monotypic subtribe Disinae and a subdvision of Disa into eighteen sections is formally proposed. These sections are monophyletic, well-supported, morphologically distinguishable and are delimited to maximize the congruence with the previous classification. All currently known species are enumerated and assigned to sections. Likelihood optimisation onto a dated molecular phylogeny is subsequently used to explore the historical biogeography of Disa, as well as of three other Cape lineages (Irideae p.p., the Pentaschistis clade and Restionaceae), to find out where these lineages originated and how they spread through the Afrotemperate region. Three hypotheses have been proposed: (i) a tropical origin with a southward migration towards the Cape; (ii) a Cape origin with a northward migration into tropical Africa and (iii) vicariance. None of these hypotheses, however, has been thoroughly tested. In all cases, tropical taxa are nested within a predominantly Cape clade and there is unidirectional migration from the Cape into the Drakensberg and from there northwards into tropical Africa. Dating estimates show that the migration into tropical East Africa has occurred in the last 17 million years, consistent with the Mio-Pliocene formation of the mountains in this area. iii The same technique is then utilised to reconstruct the temporal occurrence of ancestral ecological attributes of the genus Disa. The first appearance of species in the grassland and savanna biomes, as well as in the subalpine habitat, are in agreement with the existing, reliable geological and paleontological information. This suggests that phylogenies can be used to date events for which other information is lacking or inconclusive, such as the age of the fynbos biome and the start of the winter rainfall regime in southern Africa. The results indicate that these are much older than what is currently accepted and date back to at least the Oligocene. iv Opsomming Vyf-en-twintig jaar na die laaste groot morfologiese hersiening, is die filogenetiese verwantskappe van die Afrika orgideë subtribus Disinae, wat die groot genus Disa en die klein genus Schizodium insluit, in hierdie studie op grond van ‘n nuwe DNA datastel afgelei. Daar is van 136 binnegroep, wat 70% van alle bekende Disinae spesies verteenwoordig, sowel as sewe buitegroep taksa geenopeenvolgings van een nukleêre geen streek (ITS) en twee plastiedgeen streke (trnLF en matK) bepaal. Die gekombineerde data matriks het 4094 karakters bevat en is met die parsimonie en Bayesian metodes ontleed. Die generiese status van Schizodium kan nie hieruit ondersteun word nie, en is diep ingebed binne die genus Disa. Die huidiglik aanvaarde subgenera word ook nie deur hierdie filogenie ondersteun nie. Verskeie van die huidiglik herkende seksies is bevind om monofileties te wees, ander bevat verkeerd geplaasde spesies, terwyl ander polifileties blyk te wees. ’n Monotipiese subtribus Disinae en ’n onderverdeling van Disa in agtien seksies word formeel voorgestel. Dié seksies is monofilities, goed ondersteun, morfologies onderskeibaar en omskryf om maksimaal ooreen te stem met die vorige klassifikasie. Alle huidiglik bekende spesies word gelys en toegewys aan seksies. Waarskynlikheidsoptimalisering op ’n gedateerde molekulêre filogenie is dan gebruik om die historiese biogeografie van Disa te ondersoek, tesame met drie ander Kaapse groepe (Irideae p.p., die Pentaschistis klade en Restionaceae), om te bepaal waar hierdie groepe hulle oorsprong gevind het en hoe hulle na die “Afrotemperate“ streek versprei het. Drie hipoteses word voorgestel: (i) ’n tropiese oorsprong met ’n suidwaartse migrasie na die Kaap; (ii) ’n Kaapse oorsprong met ’n noordwaartse migrasie na tropiese Afrika, en (iii) vikariansie. Geen van hierdie hipoteses is egter vantevore deeglik getoets nie. In alle gevalle is bevind dat die tropiese taksa oorwegend binne ’n Kaapse klade gesetel is, en dat daar ’n eenrigting migrasie is van die Kaap na die Drakensberge en van daar noordwaarts na tropiese Afrika. Dateringsskattings toon dat die migrasie na tropiese Oos-Afrika in die laaste 17 miljoen jaar plaasgevind het, ooreenstemmend met die Mio-Plioseen vorming van die berge in die area. v Dieselfde tegniek is daarna aangewend om die temporale voorkoms van voorvaderlike ekologiese eienskappe van die genus Disa te rekonstrueer. Die eerste voorkoms van die spesies in die grasveld en savanna biome, sowel as die subalpiene habitat, is in ooreenstemming met bestaande, betroubare geologiese en paleontologiese informasie. Dit suggereer dat filogenieë gebruik kan word om gebeurtenisse te dateer waarvoor daar informasie ontbreek of nie beslissend is nie, soos die ouderdom van die Fynbos bioom en die begin van die winterreënval stelsel in suider-Afrika. Die resultate dui daarop dat dit heelwat ouer is as wat tans aanvaar word en terugdateer na ten minste die Oligoseen. vi Acknowledgments I sincerely thank the following people and organisations who, in one way or another, have all contributed to the making of this thesis. My supervisors, Dirk Bellstedt and Peter Linder, for their unwavering support, unbridled enthusiasm, ceaseless encouragement and the contribution of ideas that have shaped this work. Rauri Bowie, Margaret de Villiers, Leanne Dreyer, Chloe Galley, Julie Hawkins, Eric Knox, Hubert Kurzweil, Muthama Muasya, Ted Oliver, Gail Reeves, Jane Sakwa, Timo van der Niet, Tony Verboom and many others for informative scientific discussions. Annelise Botes, Coral de Villiers and the Bellstedt lab for a stimulating work environment, as well as the Biochemistry Department for hosting me. Curators and staff of the BOL, BR, DSM, EA, GRA, MO, NBG, NU and PRE herbaria. Many people have helped me with fieldwork. With the risk of forgetting some I thank Bruce Anderson, Lalao Andriamahefarivo, Dirk Bellstedt, Mike Bingham, Clinton Carbutt, Jeremy Croudache, Hildegard Crous, Tim Davenport, Louise de Roubaix, Thys de Villiers, Willem de Vlam, Tony Dold, Marc and Caroll Duckitt, Bob Ducksworth, Rika du Plessis, Trevor Edwards, Werner Fibeck, Felix Forest, Berit Gehrke, Malcolm Gemmel, Chris Hardy, Steve Johnson, Mark Johns, Tjeerd Jongeling, Caroline Joubert, Eric Knox, Francois Krige, Hubert Kurzweil, Annelise le Roux, Bill Liltved, Peter Linder, Georgio Lombardi, Mervin Lotter, Quentin Luke, Heiner Lutzeyer, Tony Marshall, Frank Mbago, Cameron McMaster, Doug McMurtry, Philippe Moline, Shelah Morita, Louis Mostert, Muthama Muasya, Ingrid Nanni, Kenneth Oberlander, Ted Oliver, Tessa Oliver, Thierry Pailler, Anton Pauw, Pete Phillipson, Christina Potgieter, Domitilla Raimondo, C Rakotovao, Jane Sakwa, Annelise Schutte, Koos Steenkamp, Kim Steiner, Timo van der Niet, Gerrit van Ede, vii Jan Vlok, Johny Witbooi, Azieb Woldetinsae and various authorities, conservation bodies and land owners for permission to collect plants. I have benefitted greatly from attending several courses and workshops such as the Intensive Course in Molecular Systematics at the University of Reading (courtesy of the South African Big Genera Group), the course in Advanced Cladistics at the University of Cape Town; the Phylogenetics and Viral Molecular Evolution course at the University of the Western Cape, the course on Model Based Phylogenetics at Stellenbosch University, and from a study visit to the Insitute for Systematic Botany at the University of Zurich. I thank the Leopold III Fund for Nature Exploration and Conservation (Belgium), the Foundation for the Advancement of Scientific Research in Africa (Belgium), the New York Botanical Garden (USA), the Chicago Zoological Society (USA), the San Diego County Orchid Council (USA) for financial contributions to the field work; the National Research Foundation of South Africa and Stellenbosch University for financial support to the research(er). Last but not least, I thank my parents and family for their trust and Jane Sakwa for her precious love. viii
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