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A Complex History of Isolation and Gene Flow

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PHYLOGEOGRAPHY OF BROWN AND RED-FOOTED BOOBIES: A COMPLEX HISTORY OF ISOLATION AND GENE FLOW by James Andrew Morris-Pocock A thesis submitted to the Department of Biology In conformity with the requirements for the degree of Doctor of Philosophy Queen’s University Kingston, Ontario, Canada (April, 2012) Copyright © James Andrew Morris-Pocock, 2012 Abstract Speciation is an important process that is responsible for the generation of biodiversity on Earth. The importance of gene flow during speciation is hotly debated; however, it can be investigated by studying the process of intraspecific population differentiation. Here, I investigate the mechanisms that influence population differentiation and gene flow in brown (Sula leucogaster) and red-footed boobies (S. sula). These species are congeneric, broadly sympatric, and ecologically similar; however, they differ in their marine habitat preference (inshore vs. pelagic). I hypothesized that: (i) gene flow is restricted by major physical barriers in both species, and (ii) gene flow in the absence of physical barriers is more prevalent in red-footed boobies due to their pelagic marine habitat preference. First, I characterized the structure and function of the booby mitochondrial genome. Using extensive DNA sequencing and phylogenetic methods, I found that boobies have tandemly duplicated mitochondrial control regions that evolve in concert. I suggest that concerted evolution of duplicated control region may be common in seabirds. To quantify matrilineal population genetic structure and gene flow, I sequenced one control region in 513 brown and red-footed boobies. Both species exhibited strong population genetic structure that was attributable to continental barriers to gene flow such as the Isthmus of Panama. In the absence of physical barriers, gene flow was more prevalent in red-footed boobies. I also used microsatellite and nuclear intron loci to perform multilocus phylogeographic analyses of brown and red-footed boobies. Individuals of both species could be grouped into four genetic populations that corresponded to oceanographic regions. In red-footed boobies, gene flow following secondary contact of previously isolated lineages was common, perhaps due to a pelagic habitat preference. In brown boobies, major genetic populations apparently diverged in ii the absence of gene flow. Despite this, Isla San Benedicto in the Eastern Pacific is a site of secondary contact between brown booby lineages that diverged approximately one million years ago, and hybrids are apparently fertile. These findings suggest that gene flow following secondary contact may be an important, but overlooked, component of speciation. iii Co-Authorship This thesis has been prepared in Manuscript Form as defined by the Queen’s University School of Graduate Studies. Dr. Vicki Friesen co-authored all manuscripts, was critical in research design, project development, and manuscript preparation, and financially supported much of this research. The second chapter was co-authored by Dr. Scott Taylor and Dr. Tim Birt, who both assisted with conceptual design of the study, laboratory work, and manuscript editing. Chapters three, four, and five were co-authored with Dr. David Anderson, who was instrumental in financing and organizing much of the field work involved in this thesis. Dr. Anderson also contributed conceptualy during the revision of each manuscript. The third chapter is co-authored by Dr. Tammy Steeves who collected many of the samples used for the paper, helped conceive the research, and critically revised the manuscript. The third chapter is also co-authored by Felipe Estela, who helped with sample collection, and laboratory work, and critically revised the manuscript. Publications arising from and included in this thesis: Morris-Pocock JA, Taylor SA, Birt TP, Friesen VL (2010) Concerted evolution of duplicated mitochondrial control regions in three related seabird species. BMC Evolutionary Biology, 10, 14. Morris-Pocock JA, Steeves TE, Estela FA, Anderson DJ, Friesen VL (2010) Comparative phylogeography of brown (Sula leucogaster) and red-footed boobies (S. sula): The influence of physical barriers and habitat preference on gene flow in pelagic seabirds. Molecular Phylogenetics and Evolution, 54, 883-896. iv Morris-Pocock JA, Anderson DJ, Friesen VL (2011) Mechanisms of global diversification in the brown booby (Sula leucogaster) revealed by uniting statistical phylogeographic and multilocus phylogenetic methods. Molecular Ecology, 13, 2835-2850. Morris-Pocock JA, Anderson DJ, Friesen VL (in review) Dynamic barriers to gene flow influence population differentiation in a pelagic seabird. Publications arising from, but not included in this thesis: Molecular Ecology Resources Primer Development Consortium (Morris-Pocock JA, Taylor SA, Sun Z, Friesen VL) (2010) Permanent genetic resources added to Molecular Ecology Resources Database 1 October 2009 – 30 November 2009. Molecular Ecology Resources, 10, 404-408. Taylor SA, Morris-Pocock JA, Sun Z, Friesen VL (2010) Isolation and characterization of ten microsatellite loci in blue-footed (Sula nebouxii) and Peruvian boobies (S. variegata). Journal of Ornithology, 151, 252-258. Patterson SA, Morris-Pocock JA, Friesen VL (2011) A multilocus phylogeny of the Sulidae (Aves: Pelecaniformes). Molecular Phylogenetics and Evolution, 58, 181-191. Morris-Pocock JA, Hennicke JC, Friesen VL (in review) Effects of long-term isolation on genetic variation and within-island population genetic structure in Christmas Island seabirds. Conservation Genetics. v Acknowledgements This thesis would not have been possible without the assistance, support, and friendship of many people. Foremost among them is Vicki Friesen, my supervisor and mentor. Throughout this PhD, Vicki has been an incredible academic and personal inspiration. She has been instrumental in all parts of this project and has provided me with endless opportunity. I would also like to thank Tim Birt and Zhengxin Sun, who were helpful during all stages of this project and taught me most of what I know about molecular genetic lab work. The manuscripts in this thesis were shaped by the valuable input of my co-authors, and I am indebted to David Anderson, Tim Birt, Felipe Estela, Tammy Steeves, Scott Taylor, and of course, to Vicki. I would also like to thank Brian Cumming, Paul Martin, and Sherry Taylor for their assistance in this project as committee members, and Irby Lovette for serving as an examiner at my defence. This research would never have been possible if it weren’t for the help of seabird biologists from around the world. First, I would like to thank David Anderson for coordinating much of the field effort to collect samples. I participated in two incredible field seasons, and I thank Giacomo Dell’Omo, Janos Hennicke, and Carlos Zavalaga for coordinating logistics and introducing me to seabird field biology. I am also indebted to the many people who helped collect the samples used in this project, including Jill Awkerman, Patricia Baião, Barry Baker, Michael Betts, Lena Braun, Alfredo Castillo, Maryam Chaib, Chris Depkin, Elena Gómez-Díaz, Jacob González-Solís, Lindsay Hayes, Herve Lormee, Martina Müller, Wendy Murray, Donna O’Daniel, Patty Parker, Robert Pitman, Maria Schiffler, Scott Shaffer, Tammy Steeves, Scott Taylor, Bernie Tershy, and Jeisson Zamudio. This field work was partially funded by an National Sciences and Engineering Research Council (NSERC) Discovery Grant to Vicki Friesen and a United States National Science Foundation Grant (#DEB9629539) to David Anderson. Logistical vi support in the field was provided by the Charles Darwin Research Station, Christmas Island National Park, Conservación Internacional-Colombia and Fundación Yubarta, the Galápagos National Park Service, Gorgona National Park, the Puerto Rico Department of Natural Resources, the Royal Society for the Protection of Birds, TAME airline, the United States Coast Guard, and the United States Fish and Wildlife Service. I am grateful to NSERC for supporting me throughout my PhD via CGS-D and Michael Smith Foreign Study Supplement scholarships. I am also grateful to Queen’s University for supporting me through an EG Bauman Fellowship, Queen’s University Graduate Awards, a Queen’s University Travel Grant for Doctoral Field Research, and for providing funding to travel to scientific meetings. Thanks also to the Waterbird Society and Pacific Seabird Group for funding travel to meetings. I would like to acknowledge all of my friends and colleagues in the Biology Department at Queen’s University. I consider myself fortunate to have worked in this academically and socially stimulating department. In particular, I would like to thank Scott Taylor, who has been an incredible friend, scientific collaborator, and lab mate. I can’t think of a better person with whom to share a study system. I would also like to thank the other members of the Friesen Lab for their friendship, scientific discourse, and good spirits. Thanks to Gaby, Petra, Sarah, Anna, Andree, Laura, Sam, Kim, Will, Scott B., Rebecca, Melissa, and Erin. I would like to thank Karen McCoy and everyone at the Institut de Recherche pour le Développement in Montpellier for their hospitality and scientific inspiration during my stay in France. My parents, Gail and Chris, have supported me in every endeavour in life. I’m sure that I’ll never be able to thank them fully, but at this point I would like to thank them for bringing me up with an appreciation of nature and the outdoors.
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  • Special Paper 470 3300 Penrose Place, P.O

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    What Is a Volcano? edited by Edgardo Cañón-Tapia Centro de Investigación Científica y de Educacíon Superior de Ensenada Department of Geology Carretera Ensenada-Tijuana No. 3918 Fraccionamiento Zona Playitas Ensenada Baja California Mexico C.P. 22860 Alexandru Szakács Sapientia University Department of Environmental Sciences Cluj-Napoca, Romania and Romanian Academy Institute of Geodynamics Bucharest, Romania Special Paper 470 3300 Penrose Place, P.O. Box 9140 Boulder, Colorado 80301-9140, USA 2010 Downloaded from http://pubs.geoscienceworld.org/books/book/chapter-pdf/960985/front_matter.pdf by guest on 27 September 2021 Copyright © 2010, The Geological Society of America (GSA), Inc. All rights reserved. GSA grants permission to individual scientists to make unlimited photocopies of one or more items from this volume for noncommercial purposes advancing science or education, including classroom use. For permission to make photocopies of any item in this volume for other noncommercial, nonprofit purposes, contact The Geological Society of America. Written permission is required from GSA for all other forms of capture or reproduction of any item in the volume including, but not limited to, all types of electronic or digital scanning or other digital or manual transformation of articles or any portion thereof, such as abstracts, into computer-readable and/or transmittable form for personal or corporate use, either noncommercial or commercial, for-profit or otherwise. Send permission requests to GSA Copyright Permissions, 3300 Penrose Place, P.O. Box 9140, Boulder, Colorado 80301-9140, USA. GSA provides this and other forums for the presentation of diverse opinions and positions by scientists worldwide, regardless of their race, citizenship, gender, religion, or political viewpoint.