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Consejo Superior de Investigaciones Científicas Real Jardín Botánico de Madrid Universidad Autónoma de Madrid Facultad de Ciencias UNIVERSIDAD AUTONOMA Filogeografía, evolución de nicho y especiación en un linaje mediterráneo–macaronésico: Lavatera maritima–Lavatera acerifolia (Malvaceae) Irene Villa Machío Memoria de Tesis Doctoral Madrid, 2017 Consejo Superior de Investigaciones Científicas Real Jardín Botánico de Madrid Universidad Autónoma de Madrid Facultad de Ciencias UNIVERSIDAD AUTONOMA Filogeografía, evolución de nicho y especiación en un linaje mediterráneo–macaronésico: Lavatera maritima–Lavatera acerifolia (Malvaceae) Memoria para optar al grado de Doctor en Biología que presenta Irene Villa Machío Directores Tutor académico Dr. Francisco Javier Fuertes Aguilar Dr. Roberto Gamarra Gamarra Dr. Gonzalo Nieto Feliner Madrid, 2017 Imagen de la portada: Lavatera maritima. J. V. Sandoval-Sierra Diseño de Portada: L. Martín-Torrijos A mi familia, malagueña y madrileña AGRADECIMIENTOS Porque una tesis no la hace una persona sola, ¿cómo simplificar en pocas palabras toda la ayuda que he recibido? Me gustaría agradecer a mis directores de tesis. A Javier por darme la oportunidad de iniciarme en esta ardua carrera investigadora, y a Gonzalo por toda su dedicación, interés y esfuerzo demostrado para que esta tesis salga adelante. A mi tutor académico, Roberto Gamarra, por la atención recibida y su eficacia en resolver las dudas burocráticas. A los diferentes grupos de investigación que me han acogido en sus laboratorios. A Pilar Catalán y todo su grupo: Luis Ángel, Rubén, Ernesto y a Diana, gracias por esas tardes de aprendizaje. Gracias también a Viruel y a Esther por sus sabios consejos. Gracias por hacerme disfrutar de una estancia “tan provechosa” tanto profesional como personalmente. Y si pienso en Huesca, no puedo dejar de agradecer todo el cariño que recibí de mis padres adoptivos, gracias Simón y Tere! Quiero agradecer a Joan Vallès y Teresa Garnatje por compartir conmigo sus conocimientos sobre “tamaño genómico”. También a Marcela Rosato, por su dedicación a las “lavateras” en el estudio citogenético, y a Juli Caujapé por facilitarnos la estancia en esa maravillosa isla. A las personas que me han acompañado en los viajes de trabajo de campo: Gonzalo, Jano, Juankis y Fátima, así como a todos los que me habéis ayudado con la aportación de muestras: Javier Fuertes, Pedro Escobar, Juan Carlos Moreno, Saul Manzano, Alex Baumel, F. Médail, Stephan Scholz, Ricarda Riina, Inés Álvarez.... Al personal del RJB del Herbario, de la Biblioteca, de Administración, de Seguridad, de Limpieza, gracias por facilitar el trabajo día a día, ya sea proporcionando pliegos, facilitando el trámite de pedidos, ordenes de servicio...., por abrirme la puerta del botánico cada día (y por supuesto dejarme salir a altas horas de la noche), o por un simple saludo acompañado de una sonrisa. Al personal técnico más veterano: Guillermo Sanjuanbenito, Fátima Durán, Alberto Herrero, Emilio Cano, Yolanda Ruiz, y a la nueva generación: Marta, Lucía, Olga y Jose, por esas interminables horas de trabajo codo a codo, por esos días de risa (y por los de bajón también). Gracias! A Yolanda Ruiz por facilitarme el uso del servicio de Microscopía electrónica. A todos mis compañeros y amigos de las diferentes etapas vividas durante la tesis: Mario Mairal, Andrea S. Meseguer, Marieta, Alicia, Melisa, José Luis, Isa, Mario, Pedro, Ana, Yurena, Arantxa, Jano, Juan Carlos, Vladi, Laura, Kina, Javi, Javi Fajardo, Iván, Vicky, Bea Rumeu, Angélica, Isabel Sanmartín, Riki, Tamara... por generar tan buen ambiente de trabajo, además de aportar buenas ideas y consejos siempre constructivos. A los estudiantes que nos han visitado durante estancias más o menos largas: Vicky, Jose, Marisa, Carla, Donis, Pamela, Farideh, Yeter, porque han contribuido positivamente en mi proceso de formación, y por los buenos ratos vividos. Y a los pequeños que han ido creciendo durante este tiempo: Simón, Rubén y Noa, Jairo, Emma, Raúl y Alejandra. De manera muy especial, a los amigos que habéis estado muy cerca, siempre apoyando con vuestras ideas, conocimientos, logística, ingeniando planes y dándome mensajes de apoyo. A la familia de Delicias, al hogar de Esperanza! GRACIAS! A los amigos que ya estaban cuando empecé este camino doctoral, y que pese a la distancia y el aislamiento que conlleva la tesis, siguen ahí esperando noticias mías. Agradecer a mi tocaya Irene, la precursora de esta carrera. A mi familia, gracias por apoyarme en todo momento, gracias por estar siempre dándome las fuerzas necesarias para enfrentar esta etapa. A mi princess (para cuando empiece a leer), por hacerme disfrutar como una enana de las cosas pequeñas. Gracias a todos los que os habéis involucrado, porque una tesis no se hace sola.... ÍNDICE INTRODUCCIÓN 13 Biogeografía de la región Mediterránea 15 Biogeografía de Islas 18 Región Macaronésica - Islas Canarias 20 Dos especies hermanas del género Lavatera 23 Proceso de divergencia y especiación 26 APROXIMACIONES METODOLÓGICAS APLICADAS 27 Estudio filogeográfico 27 Marcadores moleculares: secuencias de ADN (secuenciación de Sanger) 28 Marcadores moleculares: Single nucleotide polymorphism (SNPs) 29 La nueva era de la secuenciación: NGS y filogeografía 30 Genotyping-by-sequencing (GBS) 32 Modelos de distribución de especies (SDM) 33 Solapamiento de nicho bioclimático 35 OBJETIVO PRINCIPAL 36 REFERENCIAS 38 CAPÍTULO 1 Out of North Africa twice. Phylogeography and species distribution model of the western Mediterranean Lavatera maritima (Malvaceae) ABSTRACT 47 INTRODUCTION 48 MATERIALS AND METHODS 51 Sampling strategy, DNA extraction and plastid DNA sequencing 51 Phylogeographic and genetic diversity analyses 51 Divergence times of cpDNA lineages 52 Phylogenetic analyses 53 Species distribution modelling (SDM) 55 RESULTS 56 cpDNA variation and haplotype geographic distribution 56 Genetic diversity and differentiation 58 Divergence times of cpDNA lineages 59 Modelling past and present climate suitability 59 DISCUSSION 62 Biogeographic role of North Africa during Pleistocene 62 Evolutionary history of L. maritima 63 Causes for the present phylogeographic pattern 66 ACKNOWLEDGEMENTS 68 REFERENCES 69 SUPPORTING INFORMATION 76 CAPÍTULO 2 Genotyping SNPs of hexaploid genomes: GBS data and niche modeling unveils the colonization history of the Canarian endemic shrub Lavatera acerifolia (Malvaceae) ABSTRACT 85 INTRODUCTION 86 MATERIAL AND METHODS 89 Plant material and sampling 89 Genotyping-by-sequencing 89 Bioinformatics analyses 90 Genetic structure analysis and relatedness 91 Island genetic diversity estimates 93 Species distribution model (SDM) 94 Development of bioclimatic variables 94 Model calibration 95 RESULTS 96 GBS output 96 Population genetic structure and relatedness 97 Genetic diversity 98 Species distribution modelling 100 DISCUSSION 102 Population structure in L. acerifolia 102 Island migration model and phylogeography of L. acerifolia 104 Selecting pipelines for polyploid species 106 ACKNOWLEDGEMENTS 110 REFERENCES 110 SUPPORTING INFORMATION 116 CAPÍTULO 3 Niche segregation between Mediterranean and Macaronesian lineages: the Lavatera maritima–Lavatera acerifolia divergence INTRODUCTION 125 MATERIAL AND METHODS 128 Study system and sampling 128 DNA extraction and GBS data 128 Genetic structure analyses 129 Environmental data 130 Cross-similarity between species distributed modelling (SDM) 130 Niche characteristics: overlap and equivalence test 131 Environmental variables influencing the niche of species 133 RESULTS 133 Genotyping by sequencing 133 Genetic structure of Lavatera maritima-L. acerifolia 134 Climate suitability modelling 135 Environmental niche differentiation between species 137 Environmental niche differentiation within species 141 DISCUSSION 141 A connection between Canary and Mediterranean lineages 141 Niche differentiation between sister species 143 Implications for the speciation scenario of Lavatera acerifolia 144 REFERENCES 146 SUPPORTING INFORMATION 150 DISCUSIÓN 153 1. Historia evolutiva de Lavatera maritima y L. acerifolia 155 2. Proceso de divergencia y especiación entre Lavatera maritima y L. acerifolia 158 3. Aportaciones metodológicas exploradas durante la tesis doctoral 159 4. Análisis bioinformáticos en genomas poliploides 160 REFERENCIAS 162 CONCLUSIONES 163 Apéndice 1 167 Apéndice 2 175 Apéndice 3 179 Apéndice 4 183 Other article published during the PhD work INTRODUCCIÓN Introducción 15 Durante siglos, biólogos y naturalistas han observado que el número de especies, tanto en ambientes marinos como terrestres, no se encuentra distribuido de forma aleatoria, ni a escala global ni a escala local, es decir, que existe una tendencia de los grupos de seres vivos a concentrarse en ciertas áreas geográficas o regiones. La ocupación de un área geográfica particular por un taxón es una consecuencia tanto de factores históricos como ecológicos (Lomolino et al., 2006). La distribución geográfica de los organismos es objeto de estudio de la biogeografía, que al ser parte de la biología evolutiva trata de averiguar cómo han evolucionado los organismos en el espacio a través del tiempo hasta llegar a su distribución actual. Dentro de la biogeografía, tradicionalmente ha habido dos grandes corrientes, la histórica que intenta explicar cómo los eventos geológicos y climáticos pasados han dado forma a la distribución de los organismos (Crisci, Katinas & Posadas, 2003), y otra ecológica que se ha centrado más en los factores medioambientales
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    UNIVERSIDADE NOVA DE LISBOA Faculdade de Ciências e Tecnologia Departamento de Ciências e Engenharia do Ambiente Contributo para a Caracterização e Gestão da Vegetação da Serra da Arrábida Sara Rocha Guerreiro Dissertação apresentada na Faculdade de Ciências e Tecnologia da Universidade Nova de Lisboa para a obtenção do grau de Mestre em Engenharia do Ambiente, perfil Ordenamento do Território e Impactes Ambientais Orientador: Profª. Doutora Maria Teresa Calvão Rodrigues Co-Orientador: Doutora Evelina Brigite Pires da Moura Rodrigues Lisboa 2008 Agradecimentos Dedico um especial agradecimento às minhas orientadoras, Prof.ª Doutora Maria Teresa Calvão Rodrigues e Doutora Evelina Brigite Pires da Moura Rodrigues, por todo o apoio, incentivo e amizade demonstradas ao longo de todo este trabalho. Ao Parque Natural da Arrábida, nomeadamente à Eng.ª Isabel Santos, pelo fornecimento da informação necessária à realização deste trabalho. Ao Prof. José Carlos Ferreira e Prof.João Farinha pela utilização dos recursos informáticos e electrónicos do Grupo de Ordenamento de Território. À Eng. Carmen Quaresma e à Dra. Maria José Sousa pela simpatia e amizade demonstradas em todo o trabalho. Aos meus Colegas e Amigos Carla Almeida, Claudia Ramos, Conceição Brito, Marilia Rasões, Luís Filipe Vieira, João Figueiredo, Tania Godinho, André Alves, Sandra Oliveira e João Macedo, pelo constante fornecimento de energia positiva dada durante todo o trabalho, muitas vezes fundamental para o seguimento do trabalho. A todas as outras pessoas que de alguma forma contribuíram para a minha formação pessoal e também científica. Aos meus Pais e meu irmão pela compreensão, apoio e amizade. Este trabalho é vosso. i Sumário A Serra da Arrábida desde sempre despertou as atenções do Homem devido à sua excepcional beleza.