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Diss 5.3 for Server Convergence and plasticity in the adaptive radiation of cichlid fishes Inauguraldissertation zur Erlangung der Würde eines Doktors der Philosophie vorgelegt der Philosophisch-Naturwissenschaftlichen Fakultät der Universität Basel von Moritz Muschick aus Wolfenbüttel, Deutschland Basel, 2013 1 Genehmigt von der Philosophisch-Naturwissenschaftlichen Fakultät auf Antrag von Prof. Dr. Walter Salzburger (Departement Umweltwissenschaften, Universität Basel) und Prof. Dr. Patrik Nosil (Department of Ecology & Evolutionary Biology, University of Colorado at Boulder) Basel, den 15. November 2011 Prof. Dr. Martin Spiess (Dekan) Originaldokument gespeichert auf dem Dokumentenserver der Universität Basel edoc.unibas.ch Dieses Werk ist unter dem Vertrag „Creative Commons Namensnennung-Keine kommerzielle Nutzung-Keine Bearbeitung 2.5 Schweiz“ lizenziert. Die vollständige Lizenz kann unter creativecommons.org/licences/by-nc-nd/2.5/ch eingesehen werden. 2 Namensnennung-Keine kommerzielle Nutzung-Keine Bearbeitung 2.5 Schweiz Sie dürfen: das Werk vervielfältigen, verbreiten und öffentlich zugänglich machen Zu den folgenden Bedingungen: Namensnennung. Sie müssen den Namen des Autors/Rechteinhabers in der von ihm festgelegten Weise nennen (wodurch aber nicht der Eindruck entstehen darf, Sie oder die Nutzung des Werkes durch Sie würden entlohnt). Keine kommerzielle Nutzung. Dieses Werk darf nicht für kommerzielle Zwecke verwendet werden. Keine Bearbeitung. Dieses Werk darf nicht bearbeitet oder in anderer Weise verändert werden. • Im Falle einer Verbreitung müssen Sie anderen die Lizenzbedingungen, unter welche dieses Werk fällt, mitteilen. 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Quelle: http://creativecommons.org/licenses/by-nc-nd/2.5/ch/ Datum: 3.4.2009 3 Contents Preface ....................................................................................................5 Acknowledgments .............................................................................6 Introduction .........................................................................................7 Chapter 1 ............................................................................................12 Pharyngeal jaws and their evolutionary, ecological and behavioural significance ...................................................12 Chapter 2 ............................................................................................38 Adaptive phenotypic plasticity in the Midas cichlid fish pharyngeal jaw and its relevance in adaptive radiation ......38 Chapter 3 ............................................................................................51 Convergent evolution within an adaptive radiation of cichlid fishes .......................................................................51 Supplemental information for chapter 3 ...............................................................................................................59 Chapter 4 ............................................................................................80 Parallel ecological diversification in Antarctic notothenioid fishes as evidence for adaptive radiation .....................80 Supplemental information for chapter 4 ...............................................................................................................96 Curriculum vitae ............................................................................110 4 Preface “It would seem that here we have an experiment being conducted before our eyes on a scale unapproachable by man. Let one of the "new" biologists leave his laboratory and apply his methods to the fishes of Lanao; perhaps he might then make a real contribution to the study of evolution. By spending six months on the shores of the lake he could obtain with great ease all the material he could handle, as the Marinao fishermen bring in thousands of fish on market day, often many canoe loads of each of the commoner species. By studying several thousand fresh specimens of each of the ten most abundant species, and studying all the specimens obtainable of the rarer species and all the anomalous individuals, he could do much toward unravelling the phylogeny of the more puzzling forms and could perhaps place in their proper sequence the doubtful cases and those forms which seem to be examples of hybridism. With the foundation indicated, his statistical analysis of species would have real value and would throw light upon the evolution of so many species from one parent species.” Albert W.C.T. Herre In 1933, Albert Herre discussed the evolution of the cyprinid species flock of Lake Lanao in Indonesia, now basically extinct (Herre 1933). His main point, to which he refers to as “a problem in evolution”, is the question how one species can diversify into several ecologically differentiated species in the course of an adaptive radiation. Herre did not find a satisfying solution then, nor do we have a definite answer today, but considerable progress has been made in the last 80 years, and continues to be made. With this thesis, I hope to make a contribution to our understanding of the evolutionary processes involved in adaptive radiation. Although I learned of Herre’s article long after I started working on this topic, I basically took the approach he outlines in his closing paragraph: I spend about six month collecting fish at Lake Tanganyika, sifting through canoe loads of fish in search of rare species, studied more than a thousand specimens and am now hoping that my statistical analyses have real value and throw light upon the evolution of so many species from one parent species. Moritz Muschick Basel, October 2011 5 Acknowledgments This work would not have been possible without the help and guidance I received from many people. For this I am grateful and I would like to thank them here. My family has supported me from my very early days on in the pursuit of a life as a biologist. To them this thesis is dedicated. Most influential in the scientific work presented here was my supervisor and friend Walter Salzburger, who granted me utmost freedom in my work, but was there to help and motivate whenever needed. I think his way of supervision fitted me perfectly and helped me to become, finally, a scientist. Michael Matschiner has been a great companion during the Ph.D. time and was always there for insightful discussions about all things science. My friends in the WalterLab, with who I spend most amazing times in Basel and during fieldwork at Lake Tanganyika and in Nicaragua, I would like to thank for their company, friendship and support. Patrik Nosil took the burden on himself to critically examine this thesis, in spite of his immense workload at the time this evaluation was due. Fieldwork at Lake Tanganyika would have been impossible without the help of Lawrence Makasa, Gilbert Sheltons, Ruben Shapola and Charity Muwene. And I would never have arrived there without the people who encouraged me along the way: Marta Barluenga, Birgit Dörges, Jürgen Heucke, Axel Meyer, Volker Petschik, Kathrin Lampert, Moritz Hilbrandt, Klaus Hantelmann and Harald Runte. I also would like to acknowledge the funding agencies and foundations that made my doctoral studies possible: University of Basel, European Research Council, Swiss National Science Fund, National Geographic Society, Freiwillige Akademische Gesellschaft Basel and European Science Foundation. 6 Introduction Investigation of speciation and the formation of biodiversity is central to evolutionary biology, which itself can be considered as the uniting discipline of life sciences. Ever since Charles Darwin and Alfred Wallace (1858) propelled our understanding about the importance of natural selection in the transformation of species, researchers endeavoured to use this intellectual foundation to explain larger patterns of biodiversity. One pattern emerging from the observation of phylogenetic relationships and ecological adaptations of species is the abundance of lineages, which are apparently rapidly diversifying, resulting in ecologically diverse clades of species (Schluter 2000). Most of the biodiversity we know is made up by such clades, being the result of so-called adaptive radiations. Phenotypic diversification and lineage accumulation in adaptive radiations have received considerable attention and great progress has been made in understanding these aspects (e.g. Glor 2010). Several groups of organisms played especially prominent in this research, including: Darwin’s finches (Grant and Grant 2007), the replicated sets of ecomorphs of Anolis lizards on Caribbean islands (Losos 2009) or benthic-limnetic species pairs of threespine
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