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A Hierarchical View of Vertebrate Systematics, with Emphasis on Turtles

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A Hierarchical View of Vertebrate Systematics, with Emphasis on Turtles A Hierarchical View of Vertebrate Systematics, with Emphasis on Turtles By Jonathan Julio Fong A dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Integrative Biology in the Graduate Division of the University of California, Berkeley Committee in charge: Professor Jimmy A. McGuire, co-Chair Professor Jeffrey L. Boore, co-Chair Professor Richard M. Harland Spring 2011 A Hierarchical View of Vertebrate Systematics, with Emphasis on Turtles © 2011 by Jonathan Julio Fong Abstract A Hierarchical View of Vertebrate Systematics, with Emphasis on Turtles by Jonathan Julio Fong Doctor of Philosophy in Integrative Biology University of California, Berkeley Professor Jimmy A. McGuire, co-Chair Professor Jeffrey L. Boore, co-Chair The focus of this research is phylogenetic relationships within vertebrates, with a special emphasis on turtles. Despite a substantial amount of previous research, there are still several outstanding questions regarding relationships within vertebrates. By studying the phylogeny at several hierarchical levels (class, order, family, species), we can begin to understand the processes that produce the biodiversity around us. In addition, turtles provide a good system for phylogenetics, as there is relatively low species diversity allowing for more complete sampling, a rich fossil record to calibrate the phylogeny, and applications to conservation. For this research, I take a genomics/bioinformatics approach to assess vertebrate phylogeny. Using a combination of expressed sequence tags (ESTs) and targeted amplification of cDNA, I developed 75 single-copy, nuclear markers conserved across vertebrates (Chapter 1). I also analyze the use of different data types for higher-level phylogenetics. Comparing NUCL (nucleotides), N12 (1st and 2nd codon positions), DEGEN1 (modified sequences to account for codon degeneracy), and AA (amino acids), I find that the NUCL data-type, due to the high level of phylogenetic signal, performs the best across all divergence times. The remaining three data-types (AA, N12, DEGEN1) are less subject to homoplasy, but have greatly reduced levels of phylogenetic signal relative to NUCL (Chapter 1). I use these molecular markers to build a vertebrate phylogeny to answer questions of relationships between and within major groups. In Chapter 2, I address the phylogenetic position of turtles within the amniote phylogeny. Despite over a century of morphological and molecular research, we still do not know where turtles reside in the vertebrate evolutionary tree. I also analyze different partitioning schemes, the effect of missing data, identifying unstable taxa in a phylogeny (rogue taxa), and the use of different data-types (Chapter 2). For the phylogenetic placement of turtles, different analyses and datasets produce different results. However, after performing topological and statistical tests, the weight of the evidence supports the grouping of turtles with archosaurs (birds and crocodiles), either with turtles being the sister group to Archosauria or Crocodylia. 1 The focus of Chapter 3 is the phylogenetic relationships within turtles, with divergence dating analyses. Within turtles, a basal Pleurodira-Cryptodira was recovered and within Cryptodira, a basal Trionychia (soft-shell turtles) was recovered, with Chelonioidea next (sea turtles). A novel relationship recovered is the sister relationship between Platysternon and Testuguria (Testudinidae and Geoemydidae). Divergence dating analyses using new fossil evidence re-classifying stem cryptodires to be stem turtles find the origin of turtles to be much younger than previously believed (~153mya). For Amphibians, data point towards the diphyletic origin of the group (Chapter 5). Most of the recovered relationships within Squamata are consistent with the currently molecular phylogeny, with my data recovering a basal Dibamidae+Gekkonidae, but these results are in sharp contrast to recent morphological studies (Chapter 5). Mammal relationships in this phylogeny also mirror the current mammal phylogeny, favoring the Theria hypothesis (marsupial- placental sister groups) and a basal Afrotheria group (Chapter 5). For the problematic Scandentia (Tupaia) clade, there is phylogenetic signal allying Tupaia with Glires and Primates, but the signal with primates is stronger (Chapter 5). The last two groups, Actinopterygii (ray-finned fish) and Aves (birds), had relatively poor internal taxon sampling (Chapter 5). Although my results do not provide any new information, these new markers hold promise in helping to resolve relationships for fish and birds. Lastly, a species-level study was performed on turtles in Taiwan to identify the parental species of hybrid individuals found in the wild (Chapter 4). Through molecular methods, the parental species were identified as Mauremys sinensis and Mauremys reevesii. Presence of M. reevesii alleles on the main island of Taiwan indicates that this species may have been introduced. If so, then M. reevesii is non-native and conservation efforts should not be wasted protecting this species. 2 This is dedicated to my family, parents Julio and Janet, sisters Juliann and Sherina, brother-in-law Mark, and nephews Robert and Matthew. All of this was possible only with all your guidance and support. i TABLE OF CONTENTS Acknowledgements ..........................................................................................................................iii CHAPTER 1: Evaluating phylogenetic informativeness and data-type usage for new protein-coding genes across Vertebrata........................................................................................1 CHAPTER 2: The phylogenetic placement of turtles ..............................................................38 CHAPTER 3: Phylogenetic relationships within the Testudines............................................120 CHAPTER 4: DNA evidence for the hybridization of wild turtles in Taiwan: possible genetic pollution from trade animals..............................................................................142 CHAPTER 5: Phylogenetic relationships within other vertebrate groups (Actinopterygii, Amphibia, Squamata, Aves, Mammalia)...........................................................153 ii ACKNOWLEDGEMENTS “I have seen further, it is by standing on the shoulders of giants” ~ Sir Isaac Newton (1676) This quote is often used to pay homage to scientists of the past that paved the way for one’s own work. In science, this phrase is a bit cliché and incorrect at the same time. Yes, it is true that we as scientists build on the accomplishments of scientists before us, but this only half of the story. These words overlook the other people around us, the non-scientists that provide emotional and moral support to endure the work we do. This dissertation would not have been possible without the help and support of many people, and it is this motivation that kept me going. First, I would like to acknowledge and thank my dissertation committee, co- advisors Jeff Boore and Jim McGuire, and outside member Richard Harland. If it wasn’t for Jeff, I might not have had the opportunity to pursue my Ph.D. at Berkeley. Working for Jeff at the JGI while applying for Ph.D. programs, Jeff changed the trajectory of my life with a few words, “you know I am an adjuct professor and can accept students at Berkeley.” It has been great working with Jeff, and it was always refreshing to hear stories and advice from a man who’s diverse life experiences include being a professor, Lieutenant Colonel in the US Air Force, and the CEO of his own company. Jeff was an amazing advisor in that he was always supportive (even in times of stress such as qualifying exam time) and allowed me independence to pursue the research I was interested in. One of my fondest memories of Jeff will be when we were in China together for the 2004 International Congress of Zoology meeting in Beijing, sharing a beer together on the Great Wall. Jim was gracious to co-advise me during my time at Berkeley. I could always count on Jim to help me when there was a problem with my research or to review manuscripts. I was always amazed by how excited Jim would get about talking about research. Especially when I encountered problems with my work, hearing Jim’s enthusiasm about my work would reinvigorate me and get me excited again. Just like Jeff, Jim allowed me the freedom to work on research that interested me. This really allowed me to go through the growing pains of research and truly become an independent researcher. My outside committee member, Richard Harland, provided great guidance and feedback on my research. Despite being a completely different area of research, Dr. Harland took the time to read through and understand my work. Hearing him tell me he found my dissertation “interesting and refreshing” was one of the best compliments he could have given. I would also like to thank Per Palsboll, George Roderick, Craig Moritz, and Kevin Padian for participation in my qualifying exam. It was hard, but the exam prepared for the work ahead of me in my dissertation. Other professors at Berkeley that contributed to my growth as a researcher through discussions or as teaching courses together: Marvalee Wake, David Wake, Rauri Bowie, Eileen Lacey, Jim Patton, Glenys Thomson, Lewis Feldman, Mary Power, Monty Slatkin, and Vince Resh. iii Another scientist that I owe my career to is Jim Parham. Jim started off as my GSI for herpetology, and if it hadn’t been for his
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