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Phylogeny and Taxonomy of the Complex Thalloid Liverwort Family Cleveaceae Cavers

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Phylogeny and Taxonomy of the Complex Thalloid Liverwort Family Cleveaceae Cavers Phylogeny and Taxonomy of the Complex Thalloid Liverwort family Cleveaceae Cavers Sumudu Chandima Kumari Rubasinghe Doctor of Philosophy University of Edinburgh Royal Botanic Garden Edinburgh 2011 DECLARATION I hearby declare that the work contained in this thesis is my own, unless otherwise acknowledged and cited. This thesis has not in whole or part been previously presented for any degree. Sumudu Chandima Kumari Rubasinghe Edinburgh May 2011 i ABSTRACT Liverworts (Phylum Marchantiophyta) form the earliest diverging lineage of extant land plants and hold a key position in the evolutionary history of land plants. The family Cleveaceae, first defined in 1881 by Leitgeb by its complex thallus anatomy and star-shaped epidermal pores with strongly thickened radial walls, is now included within Marchantiopsida (Complex Thalloid Liverworts). The family is widely distributed in warm temperate to arctic regions throughout the Northern Hemisphere, but very rare in South America and absent from Australia and New Zealand. Since Cleveaceae was described, the number and names of genera and species recognized within the family have changed many times, with three genera currently accepted: Athalamia (12 to 15 species), Sauteria (2 to 5 species) and Peltolepis (1 or 2 species). However, no robust phylogenetic frame work or taxonomic monographs of the family have previously been undertaken and the species diversity within the genera remains uncertain. The study presents the first robust phylogenetic framework for the family, based on three chloroplast genes (psbA, rpoC1 and rps4) and one nuclear ribosomal region (26S) sequenced for 54 ingroup accessions representing a substantial part of the geographic range of the family (except South America) and a large part of its morphological diversity. Samples sequenced include the type species of the three currently accepted genera as well as those of previously synonymised genera; Clevea, Spathysia, Gollaniella and Sauchia. The current circumscription and relationships of the genera were tested using Maximum Parsimony, Bayesian and Likelihood inferences. Cleveaceae was strongly supported as monophyletic with four main lineages resolved within the family, two corresponding to Peltolepis and Sauteria and two composing a polyphyletic Athalamia. The latter is therefore divided into a more narrowly defined Athalamia and a fourth genus, for which Clevea is the earliest published name. ii Inferred evolutions of twelve morphological characters, that are useful or have been used in classifications of Cleveaceae, were reconstructed using maximum parsimony and maximum likelihood methods. The misleading influence of homoplasy on past morphological classifications and phylogenies is discussed. The study also presents the first worldwide taxonomic revision of Cleveaceae based on around 2300 specimens studied, including all available type specimens. The monographic work is based on morphological and anatomical characters reviewed using dissecting, compound and scanning electron microscopes including both herbarium and fresh material collected on field excursions during the study. Ventral scale morphology, position and aggregation of androecia and shape of receptacle were found to be valuable characters in generic and species delimitation. The traditional definition of genera of Cleveaceae based mainly on two characters (carpocephalum stalk position and anatomy) was rejected. A total of seven species were recognized from 25 formerly described names including one new necessary combination: Clevea hyalina (Sommerf.) Lindb., C. spathysii (Lindenb.) Müll.Frib., C. pusilla (Steph.) Rubasinghe & D.G.Long comb. nov., Athalamia pinguis Falc., Sauteria alpina (Nees) Nees, S. spongiosa (Kashyap) S.Hatt., and Peltolepis quadrata (Saut.) Müll.Frib. Nine excluded and doubtful species are listed along with reasons for their exclusion. Generic and species keys are presented based on vegetative, reproductive and spore morphological characters. For each genus and species, descriptions, illustrations, and distribution maps are given along with ecological, taxonomic and nomenclatural notes. iii ACKNOWLEDGEMENTS Venturing into the world of bryophytes was a new and challenging experience. The study of this group has enabled me to visit some wonderful places in the world and also to develop several great friendships. Most importantly, I am indebted to David Long; my principal supervisor for his invaluable guidance, advice, unsurpassed knowledge of bryophytes, patience, friendship and immense support given throughout. I am extremely grateful to my second supervisor Richard Milne, for his invaluable support, encouragement, enthusiasm, advice, and friendship. I extend my sincere thanks to Laura Forrest, for training me in the molecular lab, making time to discuss my ideas and queries, reading and improving my phylogeny chapter and for being supportive all throughout. I am also grateful to Michael Möller for his invaluable discussions on phylogenetic analyses. It would have been next to impossible to write this thesis without their help and guidance. I am immensely grateful to the Darwin Trust of Edinburgh for funding and making this doctoral research project a reality. I am very grateful to the Davis Expedition Fund of the University of Edinburgh, Oleg Polunin Memorial Fund and the Bequest Fund of the British Bryological Society for financial support for field work. The FfWG (Funds for Women Graduates) is greatly acknowledged for funding the last lap of the write-up period. It was a genuine privilege to work in such a dynamic and international environment at the Royal Botanic Garden Edinburgh, and I am grateful to all members of staff who have been extremely helpful and friendly. I am very thankful to the staff of the University of Edinburgh especially Caroline Proctor and Ellen Glendinning for their support, guidance and encouragement. Carrying out field work in different parts of the world enriched my knowledge of bryophytes and it also enabled me to collect specimens to produce an almost a complete phylogeny of my study group. Thanks to Elizabeth Kungu and David Chamberlain for sharing their expertise, advice and guidance on field work and for all the discussions and encouragement. I am very grateful to Rosa Maria Ros iv of the University of Murcia for help with the permits and field work in Spain. Thanks also to Gordon Rothero, Ariane Cailliau and Eva Maier for accompanying me in field work in Switzerland; climbing 3000m would have been next impossible without their support and company. Support and expert advice in the lab at RBGE from Alexandra Clark, Michelle Hollingsworth, James Tosh and Ruth McGregor is much appreciated. A special thanks to Frieda Christie for her expert advice and assistance in SEM and microscopy work. Thanks are also due to Hans Sluiman for providing me with technical support and Robert Mill for the helping with translations. Thanks to Helen Hoy, Sally Ray and Adele Smith who dealt with my loans and herbarium specimens. I would like to warmly thank all the curators who lent me specimen loans and granted me permission to study their specimens. Tomoyuki Katagiri of the Hiroshima University is greatly acknowledged for sending Japanese specimens for the molecular study. I would like to thank the Library staff at the RBGE for their kind cooperation and helping with my countless requests in finding obscure literature. Graham Hardy is specially acknowledged for providing assistance in obtaining extensive interlibrary loans. Special thanks are due to Nicola Harrison-Burton, Kaylene Bransgrove and Carmen Puglisi for helping me with field work in Scotland; Daniel Thomas, Daniela Schill, Tobias Marczweski for helping me with difficult German translations. A big thankyou to Alex Twyford, Bhaskar Adhikari, Tiina Sarkinen, Steven Wrigley and Carmen Puglisi for the discussions and sharing knowledge on subject and also for providing technical and moral support. I would like to make a special reference to Ikuyo Ishikawa who helped me with Japanese translations. Thanks to all my fellow PhD students for providing moral support and keeping me company: Kate Armstrong, Rhiannon Chrichton, Chantel Davis, Jane Droop, Emma Goodyer, Paulina Hechenleitner, Maria-Camila Gomez, Camila Martinez, Mobina Shaukat Ali Zoë Goodwin, and Faten Filimban. v Special thanks to Jean Long, Siobhan, Kathleen and Nina Long, Vita and Max Allan, and Fiona and Richard Forsyth, for their support and friendship during my stay in Edinburgh. They all made me feel at home and made my stay an extremely pleasurable experience. Last but not least, a very affectionate thank to my parents and immediate family for giving me everything, constant support, courage, love, and belief; I would have not had the strength to complete this doctoral study without them. Please vi TABLE OF CONTENTS Declaration ................................................................................................................i Abstract ................................................................................................................... ii Acknowledgements.................................................................................................iv List of figures ..........................................................................................................ix List of tables........................................................................................................... xi List of Appendices .. ...............................................................................................xi
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