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Population History and Evolutionary Processes In Phylogeography, phylogenetics and evolution of the redfins (Teleostei, Cyprinidae, Pseudobarbus) in southern Africa by Ernst Roelof Swartz Submitted in partial fulfilment of the requirements for the degree Doctor of Philosophy Department of Genetics Faculty of Natural and Agricultural Science University of Pretoria Pretoria Supervisors: Prof. Paulette Bloomer (Department of Genetics, University of Pretoria) Prof. Paul H. Skelton (South African Institute for Aquatic Biodiversity) July 2005 © University of Pretoria Declaration: I, the undersigned, hereby declare that the work contained in this thesis is my own original work and that I have not previously in its entirety or in part submitted it at any university for a degree. Signature: uuuuuuuuuuuuuuuuuuuuuuuuuuuuuu Date: uuuuuuuuuuuuuuuuuuuuuuuuuuuuuuuuuuu ii Thesis summary The present thesis concerns the population history, evolutionary processes and phylogenetic relationships of lineages of the redfin minnow genus Pseudobarbus. First, the population history and evolutionary processes within P. quathlambae were determined, mainly to decide the conservation value of the Mohale population. The Mohale dam threatens its survival. A divergence in mitochondrial control region and cytochrome b sequences and frequency differences in the distribution of major histocompatibility alleles were found between the Mohale population and an “Eastern” lineage. The Mohale population has therefore been historically isolated and was deemed indispensable for the conservation of P. quathlambae. Differentiation among populations of the P. afer and P. phlegethon complex were investigated, in relation to geological and climatic processes. Sea levels were about – 130 m below present levels during the last glacial maximum, about 18 000 years ago. Five historically isolated lineages were identified through analysis of mitochondrial control region sequences. The four P. afer lineages showed a strong association with proposed palaeoriver systems. A “Forest” lineage, however, reaches across two proposed palaeoriver systems. Surprisingly, this lineage is closely related to P. phlegethon. Pseudobarbus asper and P. tenuis were analysed together, because of their close phylogenetic relationship and because they occur in sympatry in the Gourits River system. Pseudobarbus tenuis showed divergence in mitochondrial control region only between the Keurbooms and Bitou River systems compared to the Gourits River system. Within P. asper, divergence was low, suggesting recent inland exchange opportunities between populations of the Gourits and Gamtoos River systems. River capture of south-eastern tributaries of the Gourits River system by the Keurbooms River would have resulted in unidirectional colonization, suggesting that speciation between P. asper and P. tenuis occurred within the Gourits River system with or iii without the Gamtoos River system being involved. Lower sea levels during the last glacial maximum also played an important role in the population history of P. burchelli. Differentiation in P. burchelli did not occur between two proposed palaeoriver systems, but rather within a western palaeoriver system. Divergence in mitochondrial control region and cytochrome b sequences showed that the “Breede” and “Tradou” lineages diverged within the Breede River system, before the “Heuningnes” lineage became isolated in the Heuningnes River system. Fifteen historically isolated Pseudobarbus lineages were included in a phylogenetic analysis on which biogeographic hypotheses were based. Phylogenetic relationships based on mitochondrial control region, cytochrome b and 16S and a combined dataset of all these were compared to relationships recovered from a previous morphological dataset. Conflicts between the molecular and morphological analyses, suggests that several morphological characters evolved in a complex manner. The molecular phylogenies suggest that the earliest divergence in the Pseudobarbus was between P. quathlambae in the Orange River system and the other species that occur in the Cape Foristic Region. Pseudobarbus lineages with two pairs of barbels and those with a single pair of barbels (excluding P. quathlambae) grouped together. In terms of currently described species, only the two lineages of P. quathlambae and the three lineages of P. burchelli were clearly monophyletic. iv This thesis is dedicated to my parents Doempie and Hilda for their unconditional love and support throughout my studies and my brothers Juan-Francois and Ruan for their friendship… …and to the plight of the redfins and those who dedicate time and effort towards their conservation. v Thesis acknowledgements My research on the redfins was funded and supported by WWF-SA (Table Mountain Fund), Lesotho Highlands Developmental Authority (LHDA), the Mazda Wildlife Fund, Cape Nature and the National Research Foundation (NRF). I thank my supervisors Paulette Bloomer and Paul Skelton for their time, encouragement and invaluable advice throughout my research career thus far. Thanks for walking the extra mile and for giving me so many opportunities and financial support to do field surveys, extra lab work and to attend conferences and workshops. Without your support and mentorship this thesis would not have been possible. Michael Cunningham has been an inspirational colleague throughout my post-graduate studies. He provided analytical advice, edited papers and assisted on many field surveys, but perhaps it was our general discussions that has helped me develop as a scientist the most. Roger Bills has had a similar influence on my research, and has helped to spark in me a deep interest in African freshwater fishes. Both Roger (and his family Daksha and Veer) and Michael also helped with accommodation to ease financial strains. My sincere appreciation also goes to Johan Rall whose passion for the conservation of freshwater fish in general, and the Maloti Minnow in particular, was inspirational. Thanks for all the opportunities to study this enigmatic species and for contributing so many ideas towards my research. This thesis would have lacked a significant part of the “redfin story” if it was not for your contribution. I’m hoping for many more years of fruitful discussions with these fine scientists. vi Heidi Roos often helped out in the lab especially during the LHDA contract. However, it was her help and companionship on long field surveys under often very testing conditions that was crucial to the success of our WWF freshwater fish project. Thanks for your support and encouragement throughout my PhD. Our field surveys would not have been as productive as it was, if it were not for several individuals that went out of their way to help. Tom Barry introduced me the Gourits River system and helped on several field surveys. It’s a testament to his enthusiasm for conservation that I was able to get such a good sampling coverage of this vast river system. He also provided us with accommodation during these surveys. Hilton Herd’s local knowledge of the Gouna Forest and surrounding areas was invaluable to our exploration efforts and he also helped with the surveys. Thanks also to the other members of the Herd family for hosting us. Ian Russell not only led field surveys in the Wilderness Lakes region for our benefit, but also provided the important slender redfin samples from the Keurbooms River system. Likewise, John Grigg provided genetic samples of the unique Tradou population of Burchell’s redfin with Dean Impson and assisted us in our surveys of the Breede River system. Gail Cleaver and her staff assisted in the field in the Kammanassie area. Dean Impson and Jim Cambray have supported my research for several years now. They gave me invaluable advice on where to sample throughout my project and provided samples themselves. I also received assistance in the field from Amanda Curtin, Gideon Kempen, Gavin Gouws, Savel Daniels, Fawzia Gordon, Kate Henderson, Denis Tweddle, Johnnie de Jaar and Roelien van Niekerk and samples from Denis Tweddle, Mokitinyane Nthimo, Anton Bok and Daksha Naran. vii During our field surveys we encountered true hospitality in rural South Africa and Lesotho. My sincere appreciation goes out to all the farmers of the Western Cape Province whom allowed us to collect fish on their properties and provided us with accommodation. I also appreciate the assistance we received from several conservation managers in the Western and Eastern Cape Provinces. Thanks to everyone that hosted us during the Maloti Minnow surveys at the Pony Trekking Centre on God Help Me Pass and in Polateng village outside Semonkong in Lesotho. Thanks also to everyone who contributed indirectly to my research associated with the Lesotho projects through the contracts under the guidance of Paul Skelton (South African Institute for Aquatic Biodiversity) and Johan Rall (ECOSUN). I would not have survived the late nights of lab work if it were not for the friendship and support of my fellow post-graduate students in the Molecular Ecology and Evolution Programme (Department of Genetics, University of Pretoria). Wayne Delport was the lab’s “clever guy” and assisted with lab work during the LHDA contract and gave analytical advice on several chapters of this thesis. Tyron Grant assisted in the lab and was central to the healthy social life we enjoyed in Pretoria. Thanks also to Lisel Solms, Marina Alais, Carel Oosthuizen, Ute Kryger, Shaun Forgi, Cathi Lehn, Keith Barnes, James Sakwa and other “MEEP” members for companionship in the lab. Outside our lab,
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