Evolutionary Genetic Analysis of an Invasive Population of Sculpins in the Lower Rhine
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Evolutionary genetic analysis of an invasive population of sculpins in the Lower Rhine I n a u g u r a l - D i s s e r t a t i o n zur Erlangung des Doktorgrades der Mathematisch-Naturwissenschaftlichen Fakultät der Universität zu Köln vorgelegt von Arne W. Nolte aus Oldenburg Köln, 2005 Berichterstatter: Prof. Dr. D. Tautz Prof. Dr. H. Arndt Prof. Dr. A. Meyer Tag der letzten mündlichen Prüfung: Freitag der 9. Juli 2005 Acknowledgements I thank Prof. Dr. D. Tautz for his continuous interest in sculpin biology. This has not only provided me with a fascinating project but also contributed significantly to the fact that sculpins are now among the genetically best- explored freshwater fishes in Europe. His inventive spirit and support have made it possible to put ambitious ideas into practice. Prof. Dr. H. Arndt and Prof. Dr. A. Meyer have kindly agreed to evaluate this thesis. I thank Dr. J. Freyhof, who made the initial discovery that invasive sculpins are “different” and introduced me to this problem during undergraduate times. Since then, he has been extremely helpful in all questions surrounding fishes and, with respect to this work, in providing insights into ecological aspects. The sculpin project was possible only with benevolent support and permissions from Dr. A. Mellin, T. Heilbronner, W. Fettweis, C. Bode, L. Jörgensen, L. Kroll, Dr. C. Köhler, W. Fricke, Dr. H. Arzbach and M. Kämmereit and with material or logistic support from Dr. F. Volckaert, Dr. B. Hänfling, Dr. D. Neely, Dr. L. Bervoets, Dr. G. Knaepkens, Dr. E. Winter, I. Steinmann, Dr. E. Korte, U. Weibel, C. Dümpelmann, Dr. W. Dönni, C. von Landwüst and Dr. A. Waterstraat as well as numerous local fishermen. As a newcomer to molecular biology I had to learn first how to produce data in the lab and at later stages how to make use of those data. I thank all current and former members of the Tautz Group for a pleasant, productive and helpful working environment, most of all Kathryn Stemshorn who joined the Cottus project in several ways.... As for the computer work, I acknowledge the persistent support of our specialists Chris Voolstra and Till Bayer. Dr. Röbbe Wünschiers has introduced me to the world of “Computational Biology” and Till Bayer and Dr. Tina Harr have helped me with extremely useful scripts to handle raw data. Many thanks to Susanne Kipp for help in careful phenotypic analyses that have been the second pillar of my work besides molecular data. Above all, I thank my parents, Dr. Helga Nolte and Karl Heinz Nolte, for allowing me to pursue and develop my interest in biology. Contents Contents Preface: Of sculpins and model organisms 3 Introduction 4 An invasion of the Lower Rhine .........................................................4 Ecological genetics and phylogeographic inference ..........................5 The study system: continuous bodies of water and leaky genepools 7 Aspects treated in this study..............................................................7 Literature: ..........................................................................................8 Declaration of collaborators contributions 10 Chapter 1: An invasive lineage of sculpins, Cottus sp. (Pisces, Teleostei) in the Rhine with new habitat adaptations has originated from hybridization between old phylogeographic groups 11 Abstract ...........................................................................................11 Introduction......................................................................................11 Methods:..........................................................................................13 Results:............................................................................................14 Discussion .......................................................................................21 Acknowledgements .........................................................................24 Literature .........................................................................................25 Appendix – Chapter 1......................................................................27 Chapter 2: Direct cloning of microsatellite loci from Cottus gobio through a simplified enrichment procedure 28 Abstract: ..........................................................................................28 Microsatellites from Sculpins ...........................................................28 Acknowledgements: ........................................................................37 Literature .........................................................................................38 Chapter 3: A Genetic Map of Cottus gobio (Pisces, Teleostei) based on microsatellites can be linked to the Physical Map of Tetraodon nigroviridis 39 Abstract: ..........................................................................................39 Introduction......................................................................................39 Methods...........................................................................................40 Results:............................................................................................42 Discussion: ......................................................................................45 Acknowledgements .........................................................................47 Literature .........................................................................................47 Chapter 4: Rapid moulding of nascent hybrid zones results from differential adaptation of two lineages of sculpins 50 Abstract: ..........................................................................................50 Introduction:.....................................................................................50 1 Contents Methods:..........................................................................................51 Results:............................................................................................55 Discussion: ......................................................................................57 Acknowledgements: ........................................................................60 Literature: ........................................................................................60 Appendix – Chapter 4......................................................................61 Chapter 5: Shape based assignment tests reveal transgressive phenotypes in natural sculpin hybrids (Teleostei, Scorpaeniformes, Cottidae) 62 Abstract ...........................................................................................62 Introduction......................................................................................62 Methods...........................................................................................64 Results.............................................................................................69 Discussion .......................................................................................73 Acknowledgements .........................................................................76 Literature .........................................................................................76 Appendix – Chapter 5......................................................................78 Chapter 6: The distribution of genomic regions associated with habitat and divergent morphology across sculpin hybrid zones 79 Abstract: ..........................................................................................79 Introduction:.....................................................................................79 Methods:..........................................................................................81 Results.............................................................................................86 Discussion .......................................................................................89 Acknowledgements: ........................................................................92 Literature: ........................................................................................92 Appendix – Chapter 6......................................................................94 Abstract 95 Zusammenfassung 96 Erklärung 98 Teilpublikationen..............................................................................98 Lebenslauf 99 2 Preface Preface: Of sculpins and model organisms A straightforward approach to study biological phenomena is to start with theory and test predictions. Proceeding this way allows one to choose beforehand, which study organism best suits the needs. Most likely, the choice would be among the so-called model organisms for which an overwhelming wealth of background information is available. Admittedly, the increase of knowledge in all disciplines of biology reflects the tremendous success and utility of this approach. My motivation for this work stems less from initial theoretical considerations but was borne out of an interest in natural history of fishes. I have been intrigued by simple and yet open questions regarding the appearance of sculpins where nobody expected them to be. At a glance, finding answers on where sculpins may come from and what has permitted them to appear in the first place seems to be a minor detail. Yet, careful analyses of “experiments” conducted by nature will reveal novel aspects and approach limits of our knowledge, most likely from a unique perspective. Most importantly, to unravel a complex situation as found in