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(Title of the Thesis)* EVIDENCE FOR SPECIATION WITH GENE FLOW: AN EXAMINATION OF THE EVOLUTIONARY GENETICS OF BLUE- FOOTED AND PERUVIAN BOOBIES by Scott Anthony Taylor 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, 2011) Copyright ©Scott Anthony Taylor, 2011 Abstract Successful preservation of Earth‟s biodiversity requires an understanding of the processes that generate new species. The generation of species without gene exchange is considered predominant; however, a growing body of evidence indicates that populations can diverge while exchanging genes, and that this may be common. Previous research hypothesized that blue- footed (Sula nebouxii) and Peruvian (S. variegata) boobies diverged from their common ancestor while exchanging genes. Here, I combine ecological and genetic perspectives to thoroughly evaluate this hypothesis. Using a panel of eight molecular markers, I estimate population differentiation for each species. I find evidence of weak population differentiation for both species, an uncommon pattern in seabirds, and argue that specialization to an unpredictable food resource has shaped contemporary population differentiation. Next, I use molecular markers and morphology to evaluate the hybrid status of five morphologically aberrant individuals. I report that all are likely F1 (first generation) hybrids, and are the product of crosses between female Peruvian boobies and male blue-footed boobies. Sex biases in pairing may occur because of an underlying preference for elaborate courtship displays. I then expand the dataset to 19 loci and use cline theory and Bayesian assignment tests to characterize the hybrid zone, to examine introgression, and to evaluate the hybrid status of the aberrant individuals. The hybrid zone is most likely maintained by strong endogenous and exogenous selection against hybrids and dispersal of parentals into the hybrid zone (a tension zone), and introgression is low for nuclear loci and absent for mitochondrial loci. Finally, I test the hypothesis that this species pair diverged from their common ancestor with gene flow using recently developed analyses and multiple loci. Divergence without gene ii flow is rejected and unidirectional introgression of sex-linked loci during divergence is reported. The results of this study support the hypotheses that: 1) populations can diverge while exchanging genes; 2) the Z chromosome may play a role in avian speciation; and 3) organisms specialized to variable foraging environments should exhibit low population differentiation. This study adds to our understanding of both population differentiation and speciation in seabirds, and of the generation of new species more generally. iii Co-Authorship This thesis is structured according to the manuscript format as outlined in the guidelines provided by The School of Graduate Studies and Research. All chapters are co-authored by Dr. Vicki Friesen, whose contributions include financial support for lab and field work, and intellectual support in project design, project development, and manuscript design and editing. The first data chapter was also co-authored by Laura Maclagan, an undergraduate student who collected a subset of the data for her undergraduate thesis project, and Dr. David Anderson, who supplied samples for the project and assisted with editing the manuscript. The second data chapter was co- authored by Dr. Carlos Zavalaga, who assisted with sample collection in Peru and manuscript editing, Dr. Guillermo Luna –Jorquera, who assisted with sample collection in Chile and manuscript editing, Dr. Alejandro Simeone, who assisted with sample collection in Chile and manuscript editing, and Dr. David Anderson, who assisted with sample collection in Chile and manuscript editing. The third data chapter was co-authored by Dr. Carlos Zavalaga, who supplied samples and morphological measurements and assisted with manuscript editing. The fourth data chapter was co-authored by Dr. David Anderson, who assisted with sample collection and manuscript editing, and by Dr. Carlos Zavalaga, who assisted with sample collection and manuscript editing. The fifth data chapter was co-authored by Dr. David Anderson, who assisted with sample collection and manuscript editing. Publications arising from and included in this thesis: Taylor, S.A., Zavalaga, C.B. & Friesen, V.L. (2010) Hybridization between blue-footed (Sula nebouxii) and Peruvian (S. variegata) boobies in Northern Peru. Waterbirds, 33, 251-257. The final publication is available at http://www.bioone.org/loi/cowa. iv Taylor, S.A., Zavalaga, C.B., Luna –Jorquera, G., Simeone, A., Anderson, D.J. & Friesen, V.L. (2010) Panmixia and high genetic diversity in a Humboldt Current endemic, the Peruvian Booby (Sula variegata). Journal of Ornithology, DOI: 10.1007/s10336-010-0628-3. The final publication is available at www.springerlink.com. Taylor, S.A., Maclagan, L., Anderson, D.J. & Friesen, V.L. (2011) Could specialization to cold water upwelling systems influence genetic diversity and gene flow in marine organisms? A case study using the blue-footed booby, Sula nebouxii. Journal of Biogeography, DOI: 10.1111/j.1365-2699.2010.02445. The final publication is available at http://onlinelibrary.wiley.com. Taylor, S.A., Anderson, D.J., Zavalaga, C.B. & Friesen, V.L (in review) Tension in the eastern Pacific: examination of a marine hybrid zone in northern Peru. Molecular Ecology. Taylor, S.A. & Friesen, V.L. Evidence for divergence with gene flow and a role for the Z chromosome in the divergence of blue-footed (Sula nebouxii) and Peruvian (S. variegata) boobies. Will be submitted to Evolution. Publications arising from, but not included in this thesis: Molecular Ecology Resources Primer Development Consortium (Morris-Pocock, J.A., Taylor, S.A., Sun, Z. & Friesen V.L.) (2010) Permanent genetic resources added to Molecular Ecology Resources Database 1 October 2009–30 November 2009. Molecular Ecology Resources, 10, 404-408. Morris-Pocock, J.A., Taylor, S.A., Birt, T.P. & Friesen, V.L. (2010) Concerted evolution of duplicated mitochondrial control regions in three related seabird species. BMC Evolutionary Biology, 10, 14. v Taylor, S.A., Morris-Pocock, J.A., Sun, Z. & Friesen, V.L. (2010) Isolation and characterization of ten microsatellite loci in blue-footed (Sula nebouxii) and Peruvian boobies (S. variegata). Journal of Ornithology, 151, 252-258. Zavalaga, C.B., Halls, J.N., Mori, G.P., Taylor, S. A. & Dell‟Omo, G. (2010) At-sea movement patterns and diving behavior of Peruvian boobies Sula variegata : sexual segregation by foraging habitat in a rich marine environment? Marine Ornithological Progress Series, 404, 259-274. Zavalaga, C.B., Taylor, S.A., Dell‟Omo, G., Anderson, D.J. & Friesen, V.L. (2009) Male/female classification of the Peruvian booby. Wilson Journal of Ornithology, 121, 739-744. vi Acknowledgements This thesis is truly a product of collaboration and I acknowledge that it could never have been completed without the help of numerous people. Foremost, I would like to thank my supervisor, Vicki Friesen, for her unwavering support and encouragement, and for giving me the opportunity to complete such an interesting project. She provided assistance with every aspect of the project and was a consistent voice of calm and reason during stressful fieldwork and patience-testing lab work. She went out of her way to provide me with learning opportunities and teaching experience, and encouraged my involvement in the Society for Conservation Biology. All of these experiences have helped me develop as a researcher, a teacher, and an individual. I could not have asked for a more supportive and understanding supervisor. Thanks also to Tim Birt for his patience and encouragement. He provided excellent guidance in the lab and without his expertise this project would not have been possible. I would also like to thank Stephen Lougheed, William Bendena, and Paul Treitz for their valuable input and for the time and effort they put in serving on my committee, and Darren Irwin for agreeing to serve as my external examiner. Studying tropical seabirds is a rewarding experience but it requires a strong stomach, the ability to tolerate harsh environments, quite often the ability to speak another language, and the help of numerous people. As is obvious from the number of co-authors on my thesis chapters, and from the acknowledgements of each chapter, many people helped collect samples for this project. I am very grateful to David Anderson for his assistance planning this project, facilitating sample collection in Peru and Chile, for being an excellent travelling companion in Chile, and for his helpful advice and manuscript editing. I am incredibly grateful to Carlos Zavalaga for his assistance planning and carrying out fieldwork in Peru, and in manuscript writing and editing. vii Without his help, collecting blood samples in Peru would have logistically impossible and no hybrid samples would have been available for this study. I am also grateful to Giacomo Dell‟Omo for his unwavering good mood, an important quality when working in unfavourable conditions on desert islands. Thanks also to Alfredo Castillo, Scott Schaffer, Matthew Miller, Martina Müller, Kathryn Huyvaert, Alejandro Simeone, Guillermo Luna-Jorquera, Tammy Steeves, and Jamie Morris-Pocock for their help obtaining samples. Thanks to the wardens of the Peruvian islands, especially R.J. Balbín and A.T. Nieto, and to Loretta
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