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Species Trees and Species Delimitation with Multilocus Data and Coalescent-Based Methods Brigham Young University BYU ScholarsArchive Theses and Dissertations 2011-02-11 Species Trees and Species Delimitation with Multilocus Data and Coalescent-based Methods: Resolving the Speciation History of the Liolaemus darwinii Group (Squamata, Tropiduridae) Arley Camargo Bentaberry Brigham Young University - Provo Follow this and additional works at: https://scholarsarchive.byu.edu/etd Part of the Biology Commons BYU ScholarsArchive Citation Camargo Bentaberry, Arley, "Species Trees and Species Delimitation with Multilocus Data and Coalescent- based Methods: Resolving the Speciation History of the Liolaemus darwinii Group (Squamata, Tropiduridae)" (2011). Theses and Dissertations. 2649. https://scholarsarchive.byu.edu/etd/2649 This Dissertation is brought to you for free and open access by BYU ScholarsArchive. It has been accepted for inclusion in Theses and Dissertations by an authorized administrator of BYU ScholarsArchive. For more information, please contact [email protected], [email protected]. Species Trees and Species Delimitation with Multilocus Data and Coalescent-based Methods: Resolving the Speciation History of the Liolaemus darwinii group (Squamata: Tropiduridae) Arley Camargo Bentaberry A dissertation submitted to the faculty of Brigham Young University in partial fulfillment of the requirements for the degree of Doctor of Philosophy Jack W. Sites, Jr., Chair Mark C. Belk Keith Crandall Jerald B. Johnson Leigh A. Johnson Department of Biology Brigham Young University April 2011 Copyright © 2011 Arley Camargo Bentaberry All Rights Reserved ABSTRACT Species Trees and Species Delimitation with Multilocus Data and Coalescent-based Methods: Resolving the Speciation History of the Liolaemus darwinii group (Squamata: Tropiduridae) Arley Camargo Bentaberry Department of Biology, BYU Doctor of Philosophy !"#$%&'#(#&)#$*'$+,#)%#+$-*.&/0(%#+$0&/$,"12*3#&#4%)$(#204%*&+"%,+$0(#$'.&/05#&402$ '*($#6*2.4%*&0(17$#)*2*3%)027$0&/$)*&+#(604%*&$+4./%#+8$!"#$(#+*2.4%*&$*'$+,#)%#+$-*.&/0(%#+$ 0&/$4"#$%&'#(#&)#$*'$,"12*3#&#4%)$(#204%*&+"%,+$05*&3$+,#)%#+$0(#$(#9.%(#/$4*$/#'%&#$4"#$ .&%4+$*'$0&021+%+$0&/$4*$'%&/$4"#$5*+4$)2*+#21$(#204#/$.&%4+$'*($#602.04%&3$024#(&04%6#$5*/#2+$ *'$+,#)%04%*&8$:$"%3"2%3"4$lizards as model organisms for ecological and evolutionary studies, emphasizing their contributions to advances in understanding linkages between phylogeography and speciation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is shown to accurately delimit species given that limited or no gene flow has occurred after divergence and despite biased estimates of demographic parameters. ABC analyses supported the distinctness of two lineages within L. darwinii under a model of speciation with gene flow. Based on the species tree and the species limits obtained in this dissertation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would like to thank my graduate committee for their support and advice, and I wish to express my gratitude to the faculty and staff of the Department of Biology for their feedback and encouragement throughout the PhD program. I greatly appreciate financial support from the Department of Biology, the College of Life Sciences, the Bean Life Science Museum, and BYU Graduate Studies for a graduate research fellowship, a graduate mentoring fellowship, and several travel grants, which made possible the completion of this dissertation. I acknowledge also external financial support from a NSF-PIRE award, the Society of Systematic Biologists, and the Society for the Study of Amphibians and Reptiles. I should thank undergraduate students for their assistance in the lab, especially Greg Walker for his dedication and commitment. Many graduate students and postdocs in the Sites Lab here in the US, the Morando and Avila Lab in Argentina, and the Victoriano Lab in Chile were great companions during field trips and during time spent in the lab, meetings, and socials. Old friends back at home and new friends here in the US made the time spent during this PhD much happier; I deeply enjoyed their friendship and affection. For being always there, in very special moments, I thank Edgar, Fernanda, Rafael, Eduardo, Raúl, and Andrés. My advisor, Jack, and his wife Joanne, were invaluable through their guidance and support during difficult times. Thank you both for caring and for helping me, and my family, to grow professionally and personally. Thanks to my family, especially my parents and brother, for their unconditional encouragement and affection. This dissertation is dedicated to my wife, Melody, and my daughter, Violeta. Their infinite patience, tolerance, and consolation were essential during this journey. I am so happy that both of you are part of my life; I will always love you. TABLE OF CONTENTS 1. General Introduction . 1 1.1. Speciation models . 1 1.2. Species trees . 3 1.3. Species delimitation . 6 1.4. Conclusions and future directions . 8 1.5. References . 11 2. Lizards as Model Organisms for Linking Phylogeographic and Speciation Studies 15 2.1. Introduction . 17 2.2. Lizards as models for evolutionary studies . 18 2.3. Emerging themes in phylogeographic research . 20 2.4. Lizard phylogeography: patterns and trends . 21 2.5. Conceptual contributions to phylogeography from lizards . 24 2.5.1. Ecotones and hybrid zones . 24 2.5.2. Species delimitation . 25 2.5.3. Novel single species studies . 27 2.5.4. Novel multi-species studies . 29 2.6. Liking phylogeography to population divergence and speciation . 31 2.6.1. Speciation modes and patterns . 31 2.6.2. What modes can phylogeographic patterns distinguish? . 32 2.6.3. What kinds of data are needed? . 35 v 2.6.4. What kinds of analyses are appropriate? . 37 2.6.5. Integrating genetic, phenotypic and environmental data into tests of alternative speciation modes . 39 2.7. Synthesis and future directions . 43 2.8. References . 47 2.9. Tables . 78 2.10. Figures . 81 2.11. Appendices . 88 3. Accuracy and Precision of Species Trees: An Empirical Evaluation of Performance in Lizards of the Liolaemus darwinii Group (Squamata: Tropiduridae) under Varying Sub- sampling Designs . 130 3.1. Introduction . 132 3.2. Methods . 136 3.3. Results . 142 3.4. Discussion . 146 3.4.1. Performance . 147 3.4.2. Systematics . 154 3.5. Conclusions . 156 3.6. References . 160 3.7. Tables . 169 3.8. Figures . 171 3.9. Appendices . 181 vi 4. Species Delimitation using ABC: Accounting for Speciation with Gene Flow in Lizards of the Liolaemus darwinii Complex (Squamata: Tropiduridae) . 201 4.1. Introduction . 203 4.2. Methods . 209 4.2.1. Simulation testing . 209 4.2.2. Empirical analyses . 211 4.3. Results . 215 4.3.1. Simulation testing . 215 4.3.2. Empirical analyses . 216 4.4. Discussion . 218 4.4.1. Species delimitation using ABC and other methods . 218 4.4.2. Species limits in the L. darwinii complex . 223 4.5. Conclusions . 225 4.6. References . 227 4.7. Tables . 236 4.8. Figures . 241 4.9. Appendices . 245 vii GENERAL INTRODUCTION SPECIATION MODELS The delimitation of species, the units of biodiversity, and the resolution of their phylogenetic relationships is fundamental for evolutionary, ecological, and conservation studies (Sites and Marshall 2003; 2004). For example, the study of the population-level processes during the early stages of divergence is necessary to assess the ultimate causal factors of speciation, and phylogenetic (species) trees are required to address higher-level patterns of diversification (Barraclough 2010). After resolution of species limits and species trees, patterns of divergence in morphological, ecological, physiological, and other organismal traits, can be used to evaluate alternative models of speciation based on the role of stochastic and deterministic evolutionary forces. Allopatric speciation models represent the scenario where disjunct geographic distributions produces isolation and therefore leads to genetic divergence due to random genetic drift within populations. With sufficient time, this process can drive differentiation in compatibility or recognition systems generating reproductive isolation during an eventual geographic contact between
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