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Evolutionary Pattern and Process Transitions Between Marine and Freshwaters in Fishes: Evolutionary Pattern and Process by Devin D. Bloom A thesis submitted in conformity with the requirements for the degree of Doctorate of Philosophy Department of Ecology and Evolutionary Biology University of Toronto © Copyright by Devin D. Bloom 2013 ii Transitions Between Marine and Freshwaters in Fishes: Evolutionary Pattern and Process Devin D. Bloom Doctorate of Philosophy Department of Ecology and Evolutionary Biology University of Toronto 2013 Abstract Evolutionary transitions between marine and freshwater habitats are rare events that can have profound impacts on aquatic biodiversity. The main goal of my thesis is determining the processes involved in transitions between marine and freshwater biomes, and the resulting patterns of diversity using phylogenetic approaches. To test hypotheses regarding the geography, timing, frequency, and mechanisms regulating biome transitions I generated multi-locus time- calibrated molecular phylogenies for groups of fishes that include both exclusively marine and freshwater species. My analysis of anchovies demonstrated that Neotropical freshwater anchovies represent a monophyletic radiation with a single origin in South American freshwaters. I used a phylogeny of herring and allies (Clupeiformes) to investigate the evolution of diadromy, a migratory behavior in which individuals move between oceans and freshwater habitats for reproduction and feeding. These analyses do not support the hypothesis that differences in productivity between marine and freshwater explain the origins of diadromous lineages. Diadromy has been considered an evolutionary pathway for permanent biome transitions, however I found that diadromy almost never produces a fully marine or freshwater clade. Marine lineages often invade continental freshwaters during episodes of marine incursion. In South America, the rich diversity of marine derived fish lineages invaded during Eocene marine incursions from either the Pacific or the Caribbean, and Oligocene marine incursions from the Caribbean. I falsified the highly cited Miocene marine incursion hypothesis, but found that the Pebas Mega-Wetland catalyzed diversification in some marine derived lineages. Using diversification analyses, I investigated the evolutionary processes that have generated disparate ii iii patterns of diversity between continents and oceans. I found that freshwater silversides have higher speciation and extinction rates than marine silversides. Lineages accumulation plots suggest ecological limits are not regulating clade growth in either marine or freshwater biomes. Overall, biome conservatism is a widespread pattern among fishes, and this pattern is largely driven by competition in clades that are physiologically capable of biome transitions. Biome transitions are facilitated by rare paleogeographic events, such as marine incursions. Finally, a difference in net diversification rate is the macroevolutionary mechanism that best explains the difference in diversity between continents and oceans. iii iv This thesis is dedicated to the memories of Dr. Irwin and Lisa Bloom—whose unwavering devotion to education and the pursuit of knowledge started it all. iv v Acknowledgments Over the course of past five years I have been the beneficiary of an amazing support system— from friends, family, colleagues, and mentors. Many people fall into multiple categories. There were far too many people that had an important influence on my young career to mention here. I would like to acknowledge those that played integral roles. First and foremost, thanks go to my advisor Dr. Nathan (Nate) Lovejoy. Nate was everything I needed in an advisor. He granted me the autonomy necessary to become an independent researcher, but was always available as a sounding board for ideas. When the University of Toronto and EEB decided to no longer fund PhD students past four years, Nate didn’t hesitate to provide financial support. Nate patiently taught me the art of crafting a well-written manuscript and developing my ideas in a broad scientific context. There is no doubt I am a far better scientist thanks to his guidance. It was also fortuitous and a joy to work with someone that enjoys sarcasm as much as I do! But perhaps I am most grateful that Nate cared deeply about his students as people, and would do everything in his power to see them succeed. I would like to thank my advisory committee: Allan Baker, Belinda Chang, and Hernán López- Fernández. Their collective expertise, critical feedback and often animated discussion improved my research considerably. Dr. Phil Cochran from Saint Mary’s University is thanked for recognizing and cultivating the enthusiasm of a young ichthyologist. Dr. C opened the door to the amazing world of scientific research. His endless pranks (fishing lures in my shoes, frozen rattlesnakes in the biology building parking lot) were a reminder to have fun along the way. I would like to thank Dr. Kyle Piller for an immensely rewarding collaboration. As my master’s advisor, Kyle introduced me to Silversides, phylogenetics, DNA sequencing, international field and so much more. Kyle gave me an opportunity to go to graduate school when few others would. This is not something I will ever forget. Dr. Hernán López-Fernández (Royal Ontario Museum) graciously took me on my first collecting expedition to South America (perhaps foolishly). This was the starting point of a friendship and v vi collaboration that I certainly hope lasts the remainder of my career. The hours spent discussing science, fishes, and life over good food, beer, and scotch are some of favorite moments of the past five years. Dr. Brian Sidlauskas (Oregon State University) brought me on a collecting trip to the Cuyuni River in Guyana. This not only was a great adventure and collecting opportunity, but started a collaboration that will expand my entire research program. I had the great pleasure to share the Lovejoy lab with some awesome people: Eric Lewallen, Javiar Maldonado-Ocampo, Kristen Brochu, Megan McCusker, and Shawna Kjartanson. There were far to many undergraduates that helped out to name, but their contributions are not overlooked. Fellow graduate students in the department made my time here much more enjoyable, particularly, Emily MacLeod, Maria Modanu, Caroline Tucker, Julie Helson, and Catherine Febria. My nest of newfies (and honorary newfies) were the best friends I could possibly ask for. Stephen Pynn, David Andrews, Luke Barry, and Danielle Rhode are simply amazing people and no words here will convey my gratitude for these friendships. Boys, I will miss the ice and the locker room. Finally, I owe the biggest thanks to Tiffany Anne Schriever and Tiktaalik (Teek) Bloom. I am eternally grateful that you are in my life. The contributions to each individual study are acknowledged at the end of each data chapter. vi vii Table of Contents Acknowledgments ......................................................................................................................... v Table of Contents ........................................................................................................................ vii List of Tables ................................................................................................................................. x List of Figures .............................................................................................................................. xii List of Appendices ...................................................................................................................... xiv 1 General Introduction .............................................................................................................. 1 2 Molecular phylogenetics reveals a pattern of biome conservatism in New World Anchovies (Family Engraulidae) ................................................................................................. 5 2.1 Abstract ........................................................................................................................................... 5 2.2 Introduction .................................................................................................................................... 5 2.3 Methods ........................................................................................................................................... 9 2.3.1 Taxon sampling ........................................................................................................................ 9 2.3.2 DNA extraction, PCR, sequence acquisition .......................................................................... 10 2.3.3 Alignment ............................................................................................................................... 11 2.3.4 Data analysis ........................................................................................................................... 11 2.3.5 Habitat reconstruction ............................................................................................................ 13 2.4 Results ........................................................................................................................................... 14 2.4.1 Molecular data ........................................................................................................................ 14 2.4.2 Phylogenetic relationships .....................................................................................................
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