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Carcharhinus Galapagensis) at Local, Regional and Oceanic Scales ResearchOnline@JCU This file is part of the following reference: Pazmiño Jaramillo, Diana Alexandra (2017) Population genomics informs conservation and management of the Galapagos shark (Carcharhinus galapagensis) at local, regional and oceanic scales. PhD thesis, James Cook University. Access to this file is available from: http://dx.doi.org/10.4225/28/58c750da105d4 The author has certified to JCU that they have made a reasonable effort to gain permission and acknowledge the owner of any third party copyright material included in this document. If you believe that this is not the case, please contact [email protected] TITLE Population genomics informs conservation and management of the Galapagos shark (Carcharhinus galapagensis) at local, regional and oceanic scales Thesis submitted by Diana Alexandra Pazmiño Jaramillo, (BSc. Biological Sciences) in July 2017 for the degree of Doctor of Philosophy in Marine Sciences College of Science and Engineering James Cook University, Townsville, Australia Statement of contribution of others Funding of PhD • Ecuador National Secretariat of Higher Education, Science, Technology and Innovation (SENESCYT) doctoral scholarship. • EcoCiencia research grant. Funding of laboratory work • School of Science and Engineering funds • Ecuador National Secretariat of Higher Education, Science, Technology and Innovation (SENESCYT) doctoral scholarship. Supervision • Dr. Lynne van Herwerden, School of Science and Engineering, James Cook University • Prof. Colin Simpfendorferr, School of Science and Engineering, James Cook University • Dr. Gregory Maes, Laboratory of Biodiversity and Evolutionary Genomics, University of Leuven. • Dr. Pelayo Salinas de León, Department of Marine Sciences, Charles Darwin Research Station. Statistical Support • Eike Steinig • Monal Lal • Madeline Green Volunteers • Diego Ortiz, Manuel Pazmiño, Eduardo Espinosa, Fernando Córdova, Luis Roberto Nieto,William Buenaño, Cecilio Tomalá, María Córdova, and other fishermen and field assistants who generously cooperated with us during sample collection. Proofreading • Diego Ortiz • Natalia Andrade II Acknowledgements Acknowledgements First and foremost, I would like to thank my supervisory panel, which were very supportive and helpful in every possible way during these four years. A special thank to Lynne van Herwerden, an incredible primary supervisor, colleague, friend, and human being. Lynne had nothing but kind words and a positive attitude towards her students every single time. From the bottom of my heart, thanks Lynne for making me forget that I am so far away from home, for guiding and teaching me (by example) how to become a good scientist and a better person every day. I would like to express my profound gratitude to Dr. Gregory Maes, my co- supervisor and friend, for being there every time I (desperately) needed. Greg would have the patience and energy to explain the most complicated problem with the simplest words to help me understand. Thanks Greg for the long skype meetings and every advice that would help me set up my current and future goals as a scientist, and thanks for being so enthusiastic about shark science. Thanks to Professor Colin Simpfendorfer for being a very patient and efficient co-supervisor, for all his guidance and for reminding me to keep a broad perspective about my work. Thanks to Dr. Pelayo Salinas de León, my external supervisor and my base in the Galápagos Islands, for all his valuable input and suggestions throughout my PhD. I consider myself fortunate to have been part of such wonderful team, always ready to step up and provide the advice and help needed. Funding for this research was provided by the National Secretariat of Higher Education, Science, Technology and Innovation of Ecuador (SENESCYT) through a Higher Education scholarship awarded from 2013-2017. Additional funding was provided by EcoCiencia through a small research EcoFondo grant. I would like to express my deepest gratitude to all the funding bodies that made this work possible. Thanks to the Galápagos National Park for their logistic support in the field and for providing the permits to collect and export tissue samples. Thanks to James Cook University and the Molecular Ecology and Evolutionary Laboratory (MEEL) for providing me an excellent environment and the opportunity to meet incredible people. A special thank to all the collaborators from around the world, Madeline Green, Dr. Carl Meyer, Dr. Sven Kerwath, Dr. Mauricio Hoyos-Padilla, Dr. Clinton Duffy, Dr. Stephen Donnellan, Dr. Claudia Junge, Dr. Charlie Huveneers, and Dr. Bronwyn Gillanders who shared valuable tissue samples and suggestions along the way, and made it possible to achieve such comprehensive and important results. III Acknowledgements My deepest, sincere love and gratitude to Diego Ortiz, for encouraging me to pursue my dreams, and for being part of this incredible journey. We have learned and grown up together sharing successes and frustrations. Thank you for inspiring me to be passionate about science, for listening at the end of the day, and for being the person I can always rely on. A big thank to those who suffered from all the complaints, that celebrated every little step forward on this journey, and had the right words on every situation, good or bad: Natalia Andrade and Dr. Chao-Yang Kuo. You guys are the best PhD mates, and friends I could ever had, and will forever have a special place in my heart. I can’t imagine how much harder this might have been without all of you. I would like to thank also Eike Steinig and Maximilian Hirschfeld, for their constant support during the data analysis and map drawing, they would have a constant smile and bring joy to the most stressful situations. Thanks to my Townsville family: Cesar Herrera, Alejandra Hernandez, Sandra Infante, Maria Nayfa, Nicolás Younes, Estefanía Erazo, Rose Basiita, Roger Huerlimann, Heather Loxton, Blanche D’Anastas, Omar Ramirez, and to all the friends and colleagues who shared this experience with me. We cried, we laugh, we got excited about the free barbeques, we spent long nights awake checking the news from home (wherever that is for each one of us), we shared the good and the bad news, we spent long days in the laboratory, but more importantly we were there for one another. Being surrounded by loving, caring people like you kept me sane and motivated every day to keep going. Lastly, thanks to my family for their endless love and support. This thesis is dedicated to you. To my father Manuel Pazmiño who introduced me to the marine world, for supporting and sharing my passion for nature. For being the best field assistant I could have asked for, and my biggest fan in every step of my life. To my mother, Teresa Jaramillo, for being my role model and the woman to look up to every day, for being strong for all of us, for teaching me how to be good and pushing me to be better. Thank you for believing in me. Thanks to my brother, Andrés Pazmiño, no matter what we say, no matter where we are, we simply know we can count on each other, thanks for being there for me. IV Abstract Abstract Elasmobranchs (sharks and rays) have increasingly experienced human pressures over recent decades, ranging from overfishing to habitat loss. Addressing these pressures is the main challenge for elasmobranch conservation. Specific life-history traits (including slow growth, late maturation, long gestation periods, and small litters) have resulted in high susceptibility to excessive mortality, and have limited their recovery ability. A better understanding of aspects of their biology, population connectivity, habitat use, adaptation and demographic patterns is an important step towards improved management and conservation of elasmobranchs. Yet there is insufficient information to understand the status of almost 50% of elasmobranch species, according to the IUCN Red List of Threatened species. The advent of Next Generation Sequencing (NGS) technologies has seen a transition from conservation genetics to genomics (from gene to genome scales), which is informing our understanding of species and improving conservation outcomes based on these insights. This technology has provided access to thousands of genome-wide markers, collectively capable of providing reliable inferences about demographic patterns and enabling detection of local adaptation. Developing and applying genomics tools to investigate elasmobranch biology and ecology is therefore an important step towards improving their management and conservation. This thesis focuses on the Galapagos shark (Carcharhinus galapagensis), a species categorized as “Near Threatened” by the IUCN in 2003, with a circumtropical distribution and a preference for isolated oceanic islands in tropical and warm temperate waters. Importantly, information about population structure and connectivity across most of the species’ geographic range is lacking, and current knowledge of habitat use and population structure is limited to specific areas. Hence, C. galapagensis is a good elasmobranch case study to apply comprehensive genomics tools to detect stock structure, inter-population connectivity, intra- population self-replenishment and to estimate effective population sizes. Informed by these measures, population status at different geographic scales can be used to prioritize populations V Abstract in need of improved management. Galapagos sharks also co-occur with a closely related carcharhinid, Carcharhinus obscurus in parts of their respective distribution ranges.
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