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Evolution in Northern Neotropical Catfishes – Integrating Genomics and Morphometrics Zurich Open Repository and Archive University of Zurich Main Library Strickhofstrasse 39 CH-8057 Zurich www.zora.uzh.ch Year: 2017 Evolution in Northern Neotropical Catfishes – Integrating Genomics and Morphometrics Stange, Madlen Abstract: Acknowledgements This dissertation would not have been written if it were not for the curiosity of my supervisor Marcelo R. Sánchez-Villagra. Thankfully, he got bored (just a little) with terrestrial vertebrates and became curious about aquatic species diversity. I was lucky enough that he hired me to do the job. I thank Marcelo for his intellectual guidance and financial support as well as his efforts to advance women in science. I want to thank Sandra Schwarte for teaching me how to work thoroughly, thoughtful, and conceptual. I am so glad for having been your student assistant and your friend. You made me the scientist I am today. I thank Michael Lenhard for being the most inspiring and passionate professor I have met during my undergraduate and graduate studies. Thank you for actually caring for your students. I thank Stefanie Hartmann and Detlef Groth for realizing how important R will be for any biologist and for teaching it so well and patiently to us ignorant.I thank all the heads and members of the different working groups I had the honor to be a temporary part of, for the inspiring discussions, support, and fun obviously: the group of Ralph Tiedemann (Uni Potsdam), Michael Lehnhard (Uni Potsdam), Walter Salzburger (Uni Basel), and Marcelo R. Sánchez-Villagra (UZH). I want to thank Walter for allowing me to do my Master thesis at his lab. It started a series of events for which I am very grateful today. Huge thanks go to my many co-authors and collaborators from Switzerland, Panama, and Venezuela, in particular Jorge Domingo Carrillo Briceño (UZH), Richard G. Cooke from the Smithsonian Tropical Research Institute, and Cathy Villalba and Gloria Sánchez from Venezuela. Fieldwork requires the help of many and I want to state that I would be nowhere close the achieved sample size without the support of the many helpers. Finally, I thank my family and friends for their support during this very long educational process: Stefan, Alex, Laura, and Astrid, you are the best! Other titles: Dissertation zur Erlangung der naturwissenschaftlichen Doktorwürde (Dr. sc. nat.) vorgelegt der Mathematisch-naturwissenschaftlichen Fakultät der Universität Zürich von Madlen Stange aus Deutsch- land Promotionskommission Prof. Dr. Marcelo Sánchez-Villagra (Vorsitz und Leitung der Dissertation) Prof. Dr. Walter Salzburger Prof. Dr. Lukas Keller Dr. Juan Ignacio Montoya-Burgos (Gutachter) Zürich, 2017 Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-149810 Dissertation Published Version Originally published at: Stange, Madlen. Evolution in Northern Neotropical Catfishes – Integrating Genomics and Morphometrics. 2017, University of Zurich, Faculty of Science. Evolution in Northern Neotropical Catfishes – Integrating Genomics and Morphometrics Dissertation zur Erlangung der naturwissenschaftlichen Doktorwürde (Dr. sc. nat.) vorgelegt der Mathematisch-naturwissenschaftlichen Fakultät der Universität Zürich von Madlen Stange aus Deutschland Promotionskommission Prof. Dr. Marcelo Sánchez-Villagra (Vorsitz und Leitung der Dissertation) Prof. Dr. Walter Salzburger Prof. Dr. Lukas Keller Dr. Juan Ignacio Montoya-Burgos (Gutachter) Zürich, 2017 Dissertation Evolution in Northern Neotropical Catfishes – Integrating Genomics and Morphometrics 4 Content 5 Content Acknowledgements 7 Summary 9 Zusammenfassung 11 Introduction 13 Chapter 1 Evolution of opercle bone shape along a macrohabitat gradient: species identification using mtDNA and geometric morphometric analyses in Neotropical sea catfishes (Ariidae) 25 Supplementary material 43 Chapter 2 Bayesian divergence-time estimation with genome-wide SNP data of sea catfishes (Ariidae) supports Miocene closure of the Panamanian Isthmus 59 Supplememtary material 119 Chapter 3 Phylomorphospace and morphological diversity of northern Neotropical Ariidae reveals conservatisms among genera despite habitat transitions 135 Supplementary material 161 Conclusion 169 Author contributions 175 Co-authored publication linked to this dissertation (abstract) 177 Curriculum Vitae 179 6 Acknowledgements 7 Acknowledgements This dissertation would not have been written if it were not for the curiosity of my supervisor Marcelo R. Sánchez-Villagra. Thankfully, he got bored (just a little) with terrestrial vertebrates and became curious about aquatic species diversity. I was lucky enough that he hired me to do the job. I thank Marcelo for his intellectual guidance and financial support as well as his efforts to advance women in science. I want to thank Sandra Schwarte for teaching me how to work thoroughly, thoughtful, and conceptual. I am so glad for having been your student assistant and your friend. You made me the scientist I am today. I thank Michael Lenhard for being the most inspiring and passionate professor I have met during my undergraduate and graduate studies. Thank you for actually caring for your students. I thank Stefanie Hartmann and Detlef Groth for realizing how important R will be for any biologist and for teaching it so well and patiently to us ignorant. I thank all the heads and members of the different working groups I had the honor to be a temporary part of, for the inspiring discussions, support, and fun obviously: the group of Ralph Tiedemann (Uni Potsdam), Michael Lehnhard (Uni Potsdam), Walter Salzburger (Uni Basel), and Marcelo R. Sánchez-Villagra (UZH). I want to thank Walter for allowing me to do my Master thesis at his lab. It started a series of events for which I am very grateful today. Huge thanks go to my many co-authors and collaborators from Switzerland, Panama, and Venezuela, in particular Jorge Domingo Carrillo Briceño (UZH), Richard G. Cooke from the Smithsonian Tropical Research Institute, and Cathy Villalba and Gloria Sánchez from Venezuela. Fieldwork requires the help of many and I want to state that I would be nowhere close the achieved sample size without the support of the many helpers. Finally, I thank my family and friends for their support during this very long educational process: Stefan, Alex, Laura, and Astrid, you are the best! 8 Summary 9 Summary Transitions between the marine and freshwater macrohabitat have occurred repeatedly in the evolution of teleost fishes. In this PhD thesis five genera of northern Neotropical sea catfish (Ariidae), a marine teleost lineage that repeatedly adapted to freshwater habitats, was investigated with regard to shape changes in relation to macrohabitat transition. An underlying fundamental assumption is that many morphological changes are adaptive in nature and it was examined here whether similar morphological changes occurred with each freshwater transition. Two skeletal features, the opercle bone, that has been shown to be a good marker for habitat adaptation in teleost fishes, and the skull, a commonly used marker for habitat adaptation in terrestrial vertebrates, were investigated applying 2D and 3D geometric morphometrics, respectively. The resulting shape data was analysed using phylogenetically informed multivariate statistics. The application of a mitochondrial DNA marker helped to verify species identities. The distribution of the investigated group makes it a rich subject to address the fundamental question on faunal evolution in the northern Neotropics. Another section of this thesis concerns the investigation of the dating of lineage splitting events among Caribbean and Eastern Pacific ariid species, solving questions on the taxonomy and phylogeny of the group but also testing conflicting hypotheses on the timing of the rise of the Panamanian Isthmus. To do so, a novel approach using Bayesian divergence time estimation was developed that constructs time-calibrated phylogenetic hypotheses from single-nucleotide polymorphisms and fossils for internal-node calibration. In the course of this study new species and freshwater populations of brackish/marine species were found and partially validated by mtDNA, nuclear DNA, or shape analysis, or all of the above together. Comprehensive morphometric analyses showed that habitat has a larger effect on opercle shape than on skull shape, but phylogenetic relationships largely determine the position of species in morphospace for both features. Freshwater species occupy a smaller area in morphospace than brackish and marine species. The Bayesian divergence time estimation revealed that most lineage splitting events among species from the two oceans happened during the Miocene, thus supporting findings for a longer and more complex formation history of the Panamanian Isthmus. 10 Zusammenfassung 11 Zusammenfassung Während der Evolution der echten Knochenfische (Teleostei) kam es häufig zu Transitionen zwischen den Makrohabitaten Salz- und Süßwasser. In der vorliegenden Doktorarbeit wurden fünf Gattungen der im salzwasserlebenden Ariidae (Kreuzwelse) aus den nördlichen Neotropen untersucht. Sie zeichnen sich dadurch aus, dass Mitglieder der einzelnen Gattungen sich wiederholt an Süßwasserhabitate angepasst haben. Die zugrundeliegende Hypothese ist, dass a) Formveränderungen der jeweiligen Art auf Grund von Anpassung an das neue Habitat auftreten können, und b) im gleichen Habitat die immer gleiche Form begünstigt werden könnte. Zwei Kapitel der vorliegenden Arbeit befassen sich mit den Formveränderungen,
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