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Alcolapia Grahami) Evolution of Fish in Extreme Environments: Insights from the Magadi tilapia (Alcolapia grahami) Dissertation submitted for the degree of Doctor of Natural Sciences (Dr. rer. Nat) Presented by Geraldine Dorcas Kavembe at the Faculty of Sciences Department of Biology Konstanz, 2015 Konstanzer Online-Publikations-System (KOPS) URL: http://nbn-resolving.de/urn:nbn:de:bsz:352-0-290866 ACKNOWLEDGEMENTS The University of Konstanz is a wonderful place to study fish biology. It is strategically located at the heart of Lake Constance (the Bodensee) and at the mouth of River Rhine. Even more fascinating, I have been very fortunate to pursue my PhD studies surrounded by an inspiring group of budding and accomplished evolutionary biologists, who define the Meyer lab. I must admit it is impossible to acknowledge all individuals who in one way or another contributed to the completion of this thesis, but I would like to acknowledge some key individuals and institutions for their significant contributions. First, I thank my supervisors: Prof. Dr. Axel Meyer and Prof Dr. Chris Wood for accepting to mentor and walk with me during my PhD research. The great discussions, immense support and your patience with me gave me the impetus to carry on even when everything seemed impossible. Axel and Chris, thank you for believing and investing your time and resources in me. I thank Prof. Dr. Mark van Kleunen for accepting to serve in my defense committee. I am grateful to Dr. Gonzalo Machado-Schiaffino who despite constantly reminding me that he was not my supervisor has been my undercover mentor throughout all my projects. I thank all the co-authors in the presented manuscripts for their great team spirit. Special thanks to my colleagues at Meyer lab and especially to Maggie Sefton for keenly reading through my chapters, and to Andreas Kautt and Ralf Schneider for helping with the German translation of my summary. Ingrid Bader, Christiane Harmsen, Alexandra Frasch and the Welcome Center team provided important logistical support during my studies. I express my greatest appreciation to the Lake Magadi Collaborative Research Team for the wonderful sampling expeditions. I thank the Tata Magadi Company and the Magadi secondary school for their hospitality and support during all the sampling expeditions. The National Commission for Science, Technology and innovation, Kenya (NACOSTI) and the Fisheries Department under the Ministry of Livestock and Fisheries Development granted permissions to acquire and transport my samples, for which I am sincerely grateful. This work was supported by a collaborative PhD grant by the Ministry of Education, Science and Technology (MOEST - Kenya), the Deutsche Akademischer Austausch Dienst (DAAD-Germany) and by the University of Konstanz. The sampling expeditions were supported by various grants to Chris Wood (Natural Sciences and Engineering Research iii Acknoweldgements Council of Canada (NSERC) Discovery grant), John Maina (National Research Foundation (NRF) grant of South Africa), and Adalto Bianchini (International Canada Research Chair Program for the International Development Research Centre-IDRC grant). I am grateful for the support I received from my employer, South Eastern Kenya University (SEKU). Finally, I wish to thank my family and friends for their love and encouragement throughout my schooling. Special thanks go to my husband Ben and to our beloved daughters, Beatrice and Lenah, for enduring my long physical absence during my stay in Germany. I am grateful to my parents and siblings for their support throughout my school life. My studies would not have been complete without a “gang of crazy” characters around me: Ayub, Msafiri, Kelvin, Bihemo, Alpha, Esther, Mialy, Elizabeth, Mugambi, among many others who provided me a life outside the lab. iv SUMMARY Extreme environments such as soda lakes are largely unexplored habitats where a surprising number of often endemic species thrive regardless of multiple co-occurring abiotic stresses, depleted food resources and restricted dispersal abilities. Their distinct geochemistry, ecological boundaries, simplified biota and high levels of endemism strikingly resemble the features found on islands that have long been used for evolutionary studies. Extreme environments thus represent prime natural laboratories to test various hypotheses related to the evolutionary processes shaping the origin and distribution of biodiversity. In this thesis, I used a multidisciplinary approach to examine how extreme aquatic habitats shape the evolutionary trajectories of their fish populations, using the Magadi tilapia (Alcolapia grahami) as a model species. This small-bodied cichlid fish has evolved to tolerate extreme water conditions (salinity: ~60% seawater, pH above 10, titration alkalinity > 300 mM, osmolality = 525 mOsm, and temperatures often exceeding 40 °C) in the Lake Magadi basin, Kenya. In the first part of my research project (Chapter three), I used neutral markers to characterize five populations of Magadi tilapia representing the entire species range, and to infer the phylogenetic position of the species. With the exception of a single population that is isolated by a land barrier, all the other populations are isolated by trona (expansive layers of floating solidified sodium carbonate salts). The results suggest high genetic diversity and strong genetic structuring of Magadi tilapia populations into three distinct clusters: Little Magadi, Fish Spring Lagoon, and Rest of Magadi. The physically isolated Little Magadi population was the most genetically distinct, whereas three populations separated by trona were genetically indistinguishable (these constitute the Rest of Magadi cluster). Interestingly, one population (Fish Spring Lagoon), which is also isolated from the populations within Lake Magadi by trona, displayed clear genetic differentiation suggesting that trona may play a key role in shaping the genetic structure of Magadi tilapia populations. Phylogenetically, Magadi tilapia grouped closely to a freshwater tilapiine cichlid, Oreochromis variabilis, from Lake Victoria. This is consistent with previous suggestions that the Alcolapia, the genus of which Magadi is a member of, is descended from a freshwater ancestor. In the second part of my research project, building on the results of the first study, I examined the potential occurrence of eco-morphological differentiation among Magadi tilapia populations, taking their past demographic history into account (Chapter four). To achieve this, I integrated data from population genomics, geometric morphometrics, stable v Summary isotopes, and demographic analyses. The results again suggested that the physically isolated Little Magadi population is the most genetically distinct. It has a narrow niche breadth and a characteristically upturned mouth, which is likely an adaptation to feeding on prey suspended on the water surface. Subtle ecomorphological differences exist between the populations within Lake Magadi. Notably, the results suggest that the three genetically distinct populations of Magadi tilapia diverged simultaneously rather recently about 1 100 generations ago. In the third component of my research project (Chapter five), I examined gene expression responses of Magadi tilapia to contrasting water conditions (its natural hypersaline water vs. freshwater) and against its closely related freshwater species, Oreochromis leucostictus. A high level of gene expression variation was observed especially between Magadi tilapia and its freshwater relative. Significant expression differences were also observed between wild and freshwater-acclimated samples of Magadi tilapia in genes related to metabolism, osmoregulation and chemical detoxification. This suggests that changes in gene expression may play a role in the adaptation of Magadi tilapia to the extreme environment. Additionally, a set of genes with physiological functions related to responses to water stress and which were surprisingly not differentially expressed were found to be under positive selection in Magadi tilapia. This suggests that evolution of stress tolerance in Magadi tilapia may be driven by both alteration in gene expression and coding sequences. Importantly, I found for the first time, the expression of the complete set of genes in the pathway responsible for urea synthesis in the gills of a teleost fish. This may represent a major physiological adaptation in Magadi tilapia to increase the rate of urea excretion to avoid accumulation of ammonia, which is lethal given its highly alkaline habitat. The differentially expressed genes and the genes showing positive signatures of selection are promising candidate genes for future studies on the genetic adaptations of Magadi tilapia. Taken together, the results of my PhD research revealed strong patterns of population structuring and rapid ecomorphological diversification in an evolutionarily young cichlid lineage as well as important insights into the genomic responses involved in fish adaptation to multiple stressful conditions. Conservation of the Magadi tilapia populations should focus on maintaining the integrity of the unique gene pools identified in this phenotypically distinct group of cichlid fishes. vi ZUSAMMENFASSUNG Extreme Umgebungen, wie Soda-Seen, sind größtenteils unerforschte Habitate, in denen eine überraschende Anzahl an oftmals endemischen Arten trotz verschiedener abiotischer Stressfaktoren, knapper Nahrungsressourcen und eingeschränkter Möglichkeiten zur Ausbreitung, gedeihen. Ihre
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