Patterns of Evolution in Gobies (Teleostei: Gobiidae): a Multi-Scale Phylogenetic Investigation

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Patterns of Evolution in Gobies (Teleostei: Gobiidae): a Multi-Scale Phylogenetic Investigation PATTERNS OF EVOLUTION IN GOBIES (TELEOSTEI: GOBIIDAE): A MULTI-SCALE PHYLOGENETIC INVESTIGATION A Dissertation by LUKE MICHAEL TORNABENE BS, Hofstra University, 2007 MS, Texas A&M University-Corpus Christi, 2010 Submitted in Partial Fulfillment of the Requirements for the Degree of DOCTOR OF PHILOSOPHY in MARINE BIOLOGY Texas A&M University-Corpus Christi Corpus Christi, Texas December 2014 © Luke Michael Tornabene All Rights Reserved December 2014 PATTERNS OF EVOLUTION IN GOBIES (TELEOSTEI: GOBIIDAE): A MULTI-SCALE PHYLOGENETIC INVESTIGATION A Dissertation by LUKE MICHAEL TORNABENE This dissertation meets the standards for scope and quality of Texas A&M University-Corpus Christi and is hereby approved. Frank L. Pezold, PhD Chris Bird, PhD Chair Committee Member Kevin W. Conway, PhD James D. Hogan, PhD Committee Member Committee Member Lea-Der Chen, PhD Graduate Faculty Representative December 2014 ABSTRACT The family of fishes commonly known as gobies (Teleostei: Gobiidae) is one of the most diverse lineages of vertebrates in the world. With more than 1700 species of gobies spread among more than 200 genera, gobies are the most species-rich family of marine fishes. Gobies can be found in nearly every aquatic habitat on earth, and are often the most diverse and numerically abundant fishes in tropical and subtropical habitats, especially coral reefs. Their remarkable taxonomic, morphological and ecological diversity make them an ideal model group for studying the processes driving taxonomic and phenotypic diversification in aquatic vertebrates. Unfortunately the phylogenetic relationships of many groups of gobies are poorly resolved, obscuring our understanding of the evolution of their ecological diversity. This dissertation is a multi-scale phylogenetic study that aims to clarify phylogenetic relationships across the Gobiidae and demonstrate the utility of this family for studies of macroevolution and speciation at multiple evolutionary timescales. In the first chapter, I present a DNA sequence matrix derived from two nuclear genes to help resolve intergeneric level phylogenetic relationships with the Gobiidae. My study is the first to use data from conserved nuclear loci to infer relationships across the Gobioidei, and the results provide strong support for the monophyly of, and interrelationships between, several ecologically divergent clades. Specifically, I show that gobies are asymmetrically divided into two clades, one of which contains primarily marine species and the other comprises mostly estuarine or freshwater taxa. In the second chapter, I focus on the evolution of microhabitat association and morphology in one of the most diverse lineages of gobies, the reef-associated genus Eviota. Eviota species v have invaded novel microhabitats multiple times throughout their evolutionary history, often occurring independently of diagnostic morphological changes in pectoral-fin ray branching and arrangement of sensory cephalic lateralis pores. The combination of historical ecological flexibility coupled with resilience to local extinction events may explain the elevated extant biodiversity in Eviota. Lastly, in my third chapter, I use Eviota as a model for studying fine-scale speciation in the Coral Triangle, a marine biodiversity hotspot in the Western Pacific Ocean. A phylogeographic analysis of two species complexes that have diverged within the Coral Triangle provides strong support for the hypothesis that the Coral Triangle serves as a ‘center of origin’ or cradle of new species. Specifically, I demonstrate that a combination of biotic and abiotic factors may be contributing to rapid speciation both in allopatry and sympatry within the last 1.5 million years. The presence of recently diverged cryptic species in the Coral Triangle implies that our current estimates of biodiversity in this marine hotspot are severely underestimated. Ultimately, this dissertation demonstrates that gobies and other ecologically diverse clades of fishes serve as excellent model groups for studying the processes driving taxonomic and phenotypic diversification in marine species at a variety of spatial and temporal scales. This project will serve as a foundation for future studies that aim to use more comprehensive genomic datasets to address questions regarding drivers of speciation and ecological diversification in gobiid fishes. vi DEDICATION I dedicate this dissertation to my parents Elizabeth M. Tornabene and Michael F. Tornabene. My mother has been a lifeline in times of struggle and a guiding light when I am lost at sea. My father has been an endless source of encouragement, and the unforgettable times we shared on the ocean led to my infatuation with the sea and the mysteries that lie beneath its surface. None of my successes in life would be possible without their love and encouragement. vii ACKNOWLEDGMENTS This dissertation could not have been completed without the encouragement and support of many amazing relatives, friends, and faculty members. I sincerely thank my adviser, mentor, and dear friend Dr. Frank Pezold. Dr. Pezold and I met in 2006 when I was undergraduate attending a conference in New Orleans. We immediately began chatting about goby systematics and after eight years the topics of our conversations haven’t changed much. Dr. Pezold has educated, motivated, supported and directed me as I wandered through the maze of academia, and I am incredibly grateful for his wisdom and guidance. I also thank my committee members Drs. Chris Bird, Derek Hogan and Kevin Conway for their support and insight throughout the program. I am extremely grateful for the countless individuals outside of Texas A&M system that helped make this dissertation possible. I thank my former mentor and good friend Dr. James Van Tassell, who spent many hours each winter and summer pushing me to achieve my goals. Drs. Mark Erdmann, Carole Baldwin, and Chenhong Li have also contributed to my success at TAMUCC and for that I am in their debt. My dear friends and colleagues Ryan Chabarria and Sharon Furriness contributed not only scientific expertise but also their friendship and encouragement. I thank Dr. Gabby Ahmadia, David Boseto, Samantha Valdez and Dr. Yongjiu Chen for their major contributions to various chapters of this dissertation. I also thank all of the current and former members of the Fish Systematics and Conservation Lab for creating an incredible research environment. I am thankful for the brotherhood of my dear friends Judd Curtis, Keith Johnson, Matthew Magnusson, Scott Large, Frank Kelly, Jon Anderson and Tom Jerhada, who helped me through these final years. I am incredibly grateful for my loving family. My parents Elizabeth and Michael have viii been my biggest supporters through this journey and I could not ask for more loving, selfless parents. My brother Paul and sister Robyn have been caring and loving siblings and have taught me much about perseverance and overcoming adversity. Lastly, my support network of family in New York and Florida consists of over a dozen aunts and uncles, cousins, grandparents and nephews, all of which are excited to see me accomplish this great achievement. Funding for many aspects of my research was provided by NSF-OISE 0080699 and OISE- 0553910 to Frank Pezold. I also received two Lerner Gray Awards from the American Museum of Natural History, two grants from the Smithsonian Institute Schultz Fund for Ichthyological Research, and several scholarships and grants from Texas A&M University – Corpus Christi that helped make this research possible. The three chapters here have been adapted for this dissertation with permission from publishers of the journals Molecular Phylogenetics & Evolution and Systematics & Biodiversity. ix TABLE OF CONTENTS CONTENTS PAGE ABSTRACT .................................................................................................................................... v DEDICATION .............................................................................................................................. vii ACKNOWLEDGMENTS ........................................................................................................... viii TABLE OF CONTENTS ................................................................................................................ x LIST OF FIGURES ..................................................................................................................... xiv LIST OF TABLES ........................................................................................................................ xv INTRODUCTION .......................................................................................................................... 1 CHAPTER I: Gobies are deeply divided: phylogenetic evidence from nuclear DNA (Teleostei: Gobioidei: Gobiidae) ...................................................................................................................... 7 Abstract ........................................................................................................................................7 1. Introduction ..............................................................................................................................8 2. Materials and methods ...........................................................................................................16 3. Results ....................................................................................................................................20 3. 1 Gobiidae
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