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Filogeografía, Delimitación De Especies Y Reconstrucción De Relaciones Filogenéticas Del Complejo Liolaemus Tenuis

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Filogeografía, Delimitación De Especies Y Reconstrucción De Relaciones Filogenéticas Del Complejo Liolaemus Tenuis Universidad de Concepción Dirección de Postgrado Facultad de Ciencias Naturales y Oceanográficas -Programa de Doctorado en Sistemática y Biodiversidad Filogeografía, delimitación de especies y reconstrucción de relaciones filogenéticas del complejo Liolaemus tenuis Tesis para optar al grado de Doctor en Sistemática y Biodiversidad MARIA ALEJANDRA PANZERA ALMADA CONCEPCIÓN-CHILE 2017 Profesor Guía: Dr. Pedro F. Victoriano Sepúlveda Dpto. de Zoología, Facultad de Ciencias Naturales y Oceanográficas Universidad de Concepción TABLA DE CONTENIDOS INDICE DE TABLAS…………………….…..…………………………………………………………………...iv INDICE DE FIGURAS…………………….…..………………………………………………………………….vi AGRADECIMIENTOS………………………………………………………………………………………...…ix RESUMEN…………………………………….……………………………………………………………………x INTRODUCCIÓN GENERAL……………………………………………………………………………………1 Patrones y procesos determinantes de la biodiversidad en el sur de América del Sur……………………...1 La filogeografía como enfoque integrativo…………………………………………………………………3 Estimación de la biodiversidad real: diversidad críptica……………………….…………………………...4 Reconstrucción de las relaciones evolutivas………………………………………………………………..6 El modelo de estudio………………………………………………………………………………………..7 El problema a estudiar..……………………………………………………………………………………12 Bibliografía……...…………………………………………………………………………………………14 CAPÍTULO 1: Geography and past climate changes have shaped the evolution of a widespread lizard from the Chilean hotspot………………………………………………………………………………………..…………...32 Abstract…………………………………………………………………………………………………....33 1. Introduction…………….…………...…………………………………………………………………..35 2. Materials and methods………………………………………………………………………………….39 3. Results…………………………………………………………………………………………………..47 4. Discussion………………………………………………………………………………………………52 5.Conclusions……………………………………………………………………………………………...58 Acknowledgements…………………………………………………………………….………………….58 References………………………………………………………………………………………….……...59 CAPÍTULO 2. Are there cryptic lizard species in the Chilean biodiversity hotspot? A case study using a widespread Liolaemus species…………………………….…….…………………………………………….….101 Abstract…………………………………………………………………………………………………..102 1. Introduction………………………………………………….………………………………………103 2. Materials and methods……………………………….……………………………………………...106 3. Results…….…………………………………………………………………………………………112 4. Discussion…….……………………………………………………………………………………..115 Acknowledgements…………………………………………………………………….………………...121 ii References………………………………………………………………………………………….…….121 CAPÍTULO 3. Phylogenomic analysis of the Chilean clade of Liolaemus lizards (Squamata: Liolaemidae) based on sequence capture data…………………………….………………………………………………….………..172 Abstract…………………………………………………………………………………………………..174 Introduction………………………………………………………………………………………………175 Materials and methods…………………………………………………………………………………...177 Results……………………………………………………………………………………………………181 Discussion………………………………………………………………………………………………..184 Conclusions………………………………………………………………………………………………189 Acknowledgements…………………………………………………………………….………………...189 References………………………………………………………………………………………….…….190 DISCUSIÓN GENERAL...…………………………………………………..………………………………….239 Filogeografía……………………………………………………………………………………………..239 Delimitación de especies…………………………………………………………………………………242 Diversificación de Liolaemus tenuis sensu lato………………………………………………243 Alcances taxonómicos………………………………………………………………………...244 Comentarios sobre la aparente coloración críptica entre L. tenuis y L. punctatissimus…….244 Sobre la incongruencia entre la filogenia mitocondrial y multilocus………………………..245 Relaciones filogenéticas en el subgénero Liolaemus………………………………………………….....246 Conclusiones……………………………………………………………………………………………..249 Bibliografía……………………………………………………………………………………………….250 iii INDICE DE TABLAS Introducción general Tabla 1. Se detalla autor, estatus de conservación de acuerdo a la IUCN, localidad tipo y región correspondiente (en el caso de las especies chilenas), para todas las especies que han sido citadas como parte del clado que incluye a L. tenuis…………………………………………………………………………………………………………31 Capítulo 1 Table 1. Measures of genetic diversity for mtDNA (a) and microsatellite loci (b) in different geographic groups.75 Table 2. AMOVA results for cyt b (a) and microsatellites (b)……..……………………..……….………………76 Table S1. Collection localities for Liolaemus tenuis, geographic coordinates, sample sizes and haplotype codes for cyt b, KIF24 and LDB5B genes……………………………………………………………………………………90 Table S2. Collection localities for Liolaemus tenuis included in the microsatellite analyses.………………….....94 Table S3. Migration models assessed with the coalescent approach implemented in Migrate-n using cyt b sequences and microsatellite loci.…………….……………………………………………………………………95 Table S4. Genetic divergence (p distance) between clusters estimated by Geneland for (a) cyt b, (b) KIF24, and (c) LDB5B DNA sequences of Liolaemus tenuis……………………………………………………………….....96 Table S5. Summary statistics exploring the demographic history for each of the Liolaemus tenuis geographic groups using the nuclear markers (a) KIF24 and (b) LDB5B…………………………………………………… .97 Table S6. Measure of pairwise Fst between clusters obtained by Geneland for (a) cyt b and (b) microsatellites...98 Table S7. Migration rate values among clusters assessed with the coalescent approach implemented in Migrate-n, using (a) cyt b sequences and (b) microsatellite loci……………………………………………………………. ..99 Table S8. Numbers of Alleles (Na), Shannon’s Index (I), Observed Heterozygosity (Ho) and Expected Heterozygosity (He) for each microsatellite loci…………………………………………………………………100 Capítulo 2 Table 1. List of the seven molecular markers and primers used for PCR and Sanger sequencing……………….136 Table 2. Markers used for species tree estimation in *BEAST and species validation in BPP are shown……....137 Table 3. Description of dorsal landmarks and semilandmarks....………………………………………………...138 Table 4. Properties of the sequence matrices of each marker used in this study for species tree estimation…….139 Table 5. Posterior probabilities for the species tree recovered by BPP v.3.3 given the tree different starting species tree……………………………………………………………………………………………………..………….140 Table 6. BPP posterior probabilities for different number of species (P[1]=Probability of one species; P[2]; Probability of 1018 two species; P[3]: Probability of three species and P[4]: Probability of four species).……..141 iv Table 7. Delimited species and their posterior probabilities, as estimated by BPP v. 3.3………………………..142 Table S1. Geographic coordinates (in degrees decimals) and locality details for the specimens used for species tree inference and ecological niche modelling........................................................................................................149 Table S2. Specimens used for the divergence time estimation. ..….………………….………………………….154 Table S3. Sequences from the Eulaemus subgenus used for the divergence time estimation taken from GenBank………………………………………………………………………………………………………….155 Table S4. Within group p-distance by marker (pairwise deletion) as estimated by MEGA v. 6……………….. 156 Table S5. Between groups mean p-distance (pairwise deletion) by marker (in alphabetical order: A12F, A9C, B1D, cytb, 1219 EXPH5, KIF24 and LDB5B) as estimated by MEGA v. 6.…………………………………....157 Table S6. Data for individuals used for the geometric morphometrics analyses…………………………………158 Table S7. Landmarks (x, y) for which a significant difference in the mean (in parenthesis) was found by the Kruskal-Wallis test……………………………………………………………………………………………….161 Capítulo 3 Table 1. Species groups recognized within the Chilean clade…………………………………………………....210 Table 2. Species included in this study…..…………………………………………………………….................212 Table 3. De novo assembly results from IDBA for Liolaemus sequence capture data....................………….......214 Table 4. Features of the UCEs and protein-coding genes………………………………………………………...216 Table 5. Bootstrap support values for the main clades inferred with three different approaches using the three data-sets. …………………..……………………………………………………………….……………………..218 Table S1. Diversity of the Chilean clade of Liolaemus (species and groups) adapted and updated from Abdala & Quinteros (2013).…..…...…....…………………………………………………………………………………...220 Table S2. Detailed type locality information, including coordinates (in decimal degrees) when available, as well as bibliographic references are given………………………………………………………..…………………....229 Table S3. Comparison of de novo assembly results from IDBA across different k-mer values…………………232 v INDICE DE FIGURAS Introducción General Figura 1. Diagrama de flujo que muestra los objetivos principales (dentro de los cuadros negros) de cada capítulo de esta tesis. …..……………………………………………………………………………………………………29 Figura 2. Distribución de Liolaemus tenuis en Chile, en base a las localidades muestreadas…………………..…30 Capítulo 1 Figure captions……………………………………………………………………………………………………..78 Figure 1. Sampling sites of Liolaemus tenuis across its Chilean range. …………………………………………..80 Figure 2. Genealogical relationships of cyt b Liolaemus tenuis haplotypes as inferred by Bayesian analysis……81 Figure 3. Parsimony-based haplotype network of mitochondrial sequences (cyt b) of Liolaemus tenuis.….….…82 Figure 4. A) Population clusters (polygons) of Liolaemus tenuis identified by Geneland, based on cyt b sequences. B) Habitat suitability map for L. tenuis during the Last Glacial Maximum (upper right) and the present (lower right)……………………………………………………………………………………………………………….83 Figura 5. Bayesian Skyline plots representing recent demographic trends of
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