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A Biogeographic Perspective of Speciation Among Desert Tortoises in the Genus Gopherus

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A Biogeographic Perspective of Speciation Among Desert Tortoises in the Genus Gopherus A Biogeographic Perspective of Speciation Among Desert Tortoises in the Genus Gopherus Item Type text; Electronic Dissertation Authors Edwards, Taylor Artemus Publisher The University of Arizona. Rights Copyright © is held by the author. Digital access to this material is made possible by the University Libraries, University of Arizona. Further transmission, reproduction or presentation (such as public display or performance) of protected items is prohibited except with permission of the author. Download date 04/10/2021 12:23:17 Link to Item http://hdl.handle.net/10150/556486 A BIOGEOGRAPHIC PERSPECTIVE OF SPECIATION AMONG DESERT TORTOISES IN THE GENUS GOPHERUS by Taylor Edwards ______________________________ A Dissertation Submitted to the Faculty of the SCHOOL OF NATURAL RESOURCES AND THE ENVIRONMENT In Partial Fulfillment of the Requirements For the Degree of DOCTOR OF PHILOSOPHY With a Major in Natural Resources In the Graduate College of THE UNIVERSITY OF ARIZONA 2015 THE UNIVERSITY OF ARIZONA GRADUATE COLLEGE As members of the Dissertation Committee, we certify that we have read the dissertation prepared by Taylor Edwards, titled A Biogeographic Perspective of Speciation among Desert Tortoises in the Genus Gopherus and recommend that it be accepted as fulfilling the dissertation requirement for the Degree of Doctor of Philosophy. ______________________________________ Date: 13 Feb 2015 Melanie Culver ______________________________________ Date: 13 Feb 2015 Michael S Barker ______________________________________ Date: 13 Feb 2015 Robert Ward Murphy ______________________________________ Date: 13 Feb 2015 Adrian Quijada-Mascarenas Final approval and acceptance of this dissertation is contingent upon the candidate’s submission of the final copies of the dissertation to the Graduate College. I hereby certify that I have read this dissertation prepared under my direction and recommend that it be accepted as fulfilling the dissertation requirement. ______________________________________ Date: 13 Feb 2015 Dissertation Director: Melanie Culver 2 STATEMENT BY AUTHOR This dissertation has been submitted in partial fulfillment of the requirements for an advanced degree at the University of Arizona and is deposited in the University Library to be made available to borrowers under rules of the Library. Brief quotations from this dissertation are allowable without special permission, provided that an accurate acknowledgement of the source is made. Requests for permission for extended quotation from or reproduction of this manuscript in whole or in part may be granted by the head of the major department or the Dean of the Graduate College when in his or her judgment the proposed use of the material is in the interests of scholarship. In all other instances, however, permission must be obtained from the author. SIGNED: _________Taylor Edwards__________ 3 ACKNOWLEDGEMENTS I am grateful for the support of a multitude of people, not the least of which is my wife, Cori Dolan. She and our daughter Amira made the significant sacrifice of allowing me time away to complete this work. This dissertation was truly a collaborative effort and would not have been possible without the contributions of my coauthors on the manuscripts featured in each of the appendices. I especially want to thank my graduate committee for their support and guidance, including M Nachman who greatly influenced the direction of this research. Additional guidance and support came from M Kaplan, B Fransway, R Sprissler and my friends and colleagues at the UAGC as well as my fellow graduate students in the Culver Lab. L Johnstone, S Miller and N Merchant were invaluable in their technical assistance with computing and scripting. R Sandoval graciously provided me with office space to complete this work. Sample collection and coordination would not have been possible without the assistance of many, many people and this international project involved the collaboration of the US Geological Survey, Tucson Herpetological Society, Arizona Game and Fish Department, and the Comisión de Ecologíca y Desarollo Sustentable del Estado de Sonora (CEDES) in Mexico. I obtained Mexican samples with assistance from CEDES and FR Méndez de la Cruz, Instituto de Biología, Universidad Nacional Autónoma de México (UNAM). Permits for Mexican samples were facilitated by Secretaría de Medio Ambiente y Recursos Naturales (SEMARNAT). Field collection of samples in Mexico would not have been possible without the help of C Melendez, P Rosen, M Vaughn, A Karl, P Woodman, L Smith, M Figueroa, Y Leon and numerous volunteers that participated in the project. K Berry, US Geological Survey graciously provided samples from California collected by K Anderson, T Bailey, R Evans, R Woodard, P Woodman, P Frank, B Henen and K Nagy. Many of the Arizona samples were provided by C Jones and the Arizona Game and Fish Department and were collected by D Grandmaison, S Goodman and P Woodman. A McLuckie granted use of samples of G. agassizii collected in Utah. B Brandner provided samples of G. berlandieri. I thank J Jarchow and the Sonoran Animal Hospital (Tucson, AZ) for their assistance in obtaining RNA samples from G. agassizii. RNA samples collected in Nevada were facilitated through J Germano, San Diego Zoo’s Desert Tortoise Conservation Center and R Averill-Murray, US Fish and Wildlife Service. Sample collection in Nevada was assisted by B Jurand, R Lamkin, S Madill, J Rose and A Dolan. I thank J Still, J Galina-Mehlman and S Sotak at Arizona Research Laboratories and the University of Arizona Genetics Core (UAGC) for assistance with Sanger and next- 4 generation sequencing. J Barraza, Y Jimenez, M Christinsen and E Cox assisted with laboratory work. Financial support came from several awards including the Fisher Scientific Scholar of Excellence Award, the Jarchow Conservation Award presented by the Tucson Herpetological Society and the David J. Morafka Memorial Research Award presented by the Desert Tortoise Council. Finally, I thank the communities of the Tucson Herpetological Society and the Desert Tortoise Council for their continued inspiration and support. 5 DEDICATION To my mom and dad, Sandy and Artemus Edwards who encouraged me to follow my passions; and to my daughter Amira, whom I hope will inherit the same joie de vivre that I was so fortunate to receive from my parents. 6 TABLE OF CONTENTS ABSTRACT………………………………………………………………………..……08 SUMMARY………………………………………………………………………..……09 LITERATURE CITED…………………………………………….…………………..19 APPENDIX A…………………………………………………...………………………..……24 Testing Taxon Tenacity of Tortoises: Evidence for a geographical-selection gradient at a secondary contact zone; Published Manuscript: Ecology and Evolution APPENDIX B …………………………………………………...………………………..……67 Shaping species with ephemeral boundaries; the distribution and genetic structure of desert tortoise (Gopherus morafkai) in the Sonoran Desert Region; Manuscript submitted for publication – in review APPENDIX C…………………………………………………...………………………....…102 Assessing models of speciation under different biogeographic scenarios; an empirical study using multi-locus and RNA-seq analyses; Manuscript submitted for publication – in review APPENDIX D………………………………………..………...………………………..……149 Population and Conservation Genetics; book chapter published in: Biology and Conservation of North American Tortoises. 2014. D.C. Rostal, E.D. McCoy and H.R. Mushinsky (eds). Johns Hopkins University Press, Baltimore, MD. 7 ABSTRACT One of the important contributions genetic studies have made to conservation is the ability to resolve taxonomy and define relationships among populations. However, this can be complicated when species exhibit hybridization. Hybridization can be an important part of the evolutionary process and a critical component in a species ability to adapt to a changing environment. Most hybrid zones are observed at ecotones between two distinct habitats and this may be important in defining the role of hybrid zones in the evolutionary process. I examined hybridization among the three distinct lineages of desert tortoises in the genus Gopherus. An important aspect of this study system is the presence of areas of overlap between divergent lineages of desert tortoise which allowed me to test hypotheses about which forces influence these taxonomic boundaries. Specifically, I tested hypotheses about the contribution of physical vs. ecological segregation and the relative importance of isolation and gene flow in the formation of these disparate desert tortoise lineages. I used mtDNA sequence data and 25 microsatellite loci to perform Bayesian clustering, clinal analyses and habitat suitability modeling to infer population structure and influence of landscape features at each contact zone. In both instances, I observed ecological niche partitioning and limited hybridization at ecotones. I then used mtDNA and four nDNA loci to perform a multi-locus phylogenetic analysis to estimate the species tree among desert tortoise lineages and tested for ancestral admixture with RNA-seq data using demographic inference employed in the software package ∂a∂i. My results validate taxonomic distinction among all three lineages without evidence of ancestral introgression. These data suggest that despite the presence of contemporary hybridization and incomplete reproductive isolation, divergence among these lineages is consistent with species-level differentiation. By clarifying the evolutionary processes that influence the distribution of desert tortoise lineages, this study
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