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Carex (Cyperaceae) La Disyunción Bipolar En Biogeografía: Casos De Estudio En El Género Carex (Cyperaceae)

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Carex (Cyperaceae) La Disyunción Bipolar En Biogeografía: Casos De Estudio En El Género Carex (Cyperaceae) Dpto. Biología Molecular e Ingeniería Bioquímica The bipolar disjunction in biogeography: case studies in the genus Carex (Cyperaceae) La disyunción bipolar en biogeografía: casos de estudio en el género Carex (Cyperaceae) TESIS DOCTORAL Tamara Villaverde Hidalgo Sevilla, 2015 Dpto. Biología Molecular e Ingeniería Bioquímica The bipolar disjunction in biogeography: case studies in the genus Carex (Cyperaceae) La disyunción bipolar en biogeografía: casos de estudio en el género Carex (Cyperaceae) Memoria presentada por la licenciada en Biología Tamara Villaverde Hidalgo para optar al título de Doctora en Estudios Medioambientales (Doctorado Internacional) por la Universidad Pablo de Olavide de Sevilla. Sevilla, Julio 2015 Directores Dr. Modesto Luceño Garcés Dr. Santiago Martín Bravo Dr. Marcial Escudero Lirio Agradecimientos Para poder llegar hasta el volumen que tienes ahora en las manos, ha sido necesaria la ayuda de muchas personas. Éste ha sido un camino muy duro, aunque también muy enriquecedor, que no hubiera sido posible terminar sin las manos prestadas por los siguientes compañeros de viaje: Mis directores de tesis. Modesto, muchas gracias por dejarme cumplir un sueño y darme la oportunidad de crecer profesionalmente. Hacer una tesis sin beca es una de las situaciones más indeseables para un doctorando. Gracias por creer que merecía la pena invertir en mí y por darme la posibilidad de estar en las aulas, ha sido una de las experiencias más gratificantes de mi vida. Siempre te estaré agradecida. Marcial y Santi, además de prestaros a ser mi brújula y mi mapa, habéis puesto el ímpetu y las ganas para llegar hasta aquí. Gracias por subiros al barco, cuidarme tanto y darme vuestro afecto. Ha sido un verdadero placer aprender a vuestro lado. Gracias de todo corazón. Mis compañeros de laboratorio. Enrique, Inés, Jose, Marcial, Modesto, Mónica, Paco, Pedro y Santi, sois mi familia en la UPO. Gracias por haber actuado como una válvula de escape al estrés de la tesis, a veces, volviéndome a poner los pies en la tierra, y otras, haciéndome reír hasta perder la respiración. He tenido mucha suerte llegando a un grupo como el vuestro, donde siempre he contado con vuestra ayuda y cariño. ¡Gracias! Sir Henry, me siento muy afortunada por haberte conocido y por haber encontrado en ti un hombro (el de un gigante) en el que apoyarme durante este camino. Gracias por ser una persona tan maravillosa conmigo. ¡MagVilla’s! También quiero darle las gracias a esos compañeros que han pasado por el laboratorio y con los que he pasado uno buenos momentos: Carlos, Carmen, Cristina, Flo, Gloria, Laura, Manu, Nacho, Paloma, Samuel, Víctor… y a todos los estudiantes del área de botánica que han estado conmigo estos años. Compañeros de otros laboratorios. Quiero darle las gracias a todo el equipo de Andrew Hipp (The Morton Arboretum): Andrew, Bethany, Elisabeth, Marlene, grupo de voluntarios, Elisabeth Li (biblioteca) y demás compañeros, que han hecho que mi estancia en Chicago haya sido fabulosa. ¡Gracias por vuestra ayuda y por enseñarme tantas cosas! Quiero darle también las gracias a las personas que han recolectado para estos trabajos (Leo Bruederle, Pedro Jiménez Mejías, Mihai Pusças, Wayne Sawtel, Pablo Vargas,), y a todos los conservadores de los herbarios que nos han dado acceso a sus colecciones. También quiero darle las gracias a Paco Rodríguez Sánchez (Estación Biológica de Doñana – CSIC) por su ayuda y comentarios a los análisis de nicho ecológico así como a José Luis Blanco Pastor por su ayuda con el programa Maxent. Gracias a todos los investigadores del Canadian Museum of Nature, Jeff Saarelay Lynn Gillespie, por ayudarme con los trabajos de morfometría y a Michel Gosselin por facilitarme mucha bibliografía ornitológica. También a mis compañeros de laboratorio: Anna, Jocelyn, Katia, Neda, Paul, Roger, Wayne... Mis amigos. Tengo un grupo de cinco amigas de toda la vida a las que quiero agradecer que siempre hayan estado, y estén, ahí. Carmen, Campano, María, Martínez y Porti, gracias por ser mis Malvadas hermanas postizas. Llegar hasta aquí ha sido gracias a tardes llenas de risas y sabios consejos. Tengo otro grupo de amigos que, aunque hayan llegado un poco más tarde, son los culpables de ponerme un sonrisote y una cerveza en la mano estos años de tesis: Cobos, Coco, Vero, Edu, Eli, Elisa, Esteban, Estrella, Jeovani, Maite, Raquel, Rosa, Paco, compis de la carrera, compis del máster en la UPO, compis de Toastmaster Sevilla, … Mi familia. Tengo la familia más molona del mundo mundial. Sois mi refugio, mi ejemplo de esfuerzo y mi inspiración diaria. Gracias por ser incondicionales y buscar los medios, las palabras y los abrazos necesarios para animarme a perseguir mis metas en la vida. A mis padres. A mis hermanos. ÍNDICE Abstract / Resumen …………………………………………………………… 1 Chapter 1. Introduction ……………………………………………………. 1 Biogeography ……………………………………………………………. Bipolar plant disjunctions ……………………………………………… 22 Hypothesis tested in bipolar disjunctions ……………………………… 23 Molecular markers for biogeographical studies and the need of divergence analyses ………………………………………………………………… 28 Carex (Cyperaceae), the genus with the greatest number of bipolar species ……………………………………………………………………. 30 Objetives by chapters …………………………………………………… 36 References ……………………………………………………………… 38 Appendix S1 ……………………………………………………………. 47 Chapter 2. Taxonomy of the Carex capitata complex………………………… 59 Abstract ………………………...……………………………………… 62 Introduction ………………………………………………………………63 Materials and methods …………………………………………..…… 64 Results …………………………………………………………….…… 68 Discussion ……………………………………………………………...... 75 References ……………………………………………………………….. 93 Appendix S1 ……………………………………………………………... 97 Additional Information ……………………………………………...…... 123 Chapter 3. Direct long-distance dispersal best explains the bipolar distribution of Carex arctogena (Carex sect. Capituligerae, Cyperaceae) ……………………. 155 Abstract ……………………………………………………………...... 154 Introduction ……………………………………………………….....…. 154 Materials and methods ………………………………………………159 Results ………………………………………………………………….... 160 Discussion …………………………………………………………...........162 Acknowledgements ……………………………………………………. 166 References …………………………………………………………….... 166 Appendix S1 ………………………………………………………….….. 169 Chapter 4. Long-distance dispersal during the middle–late Pleistocene explains the bipolar disjunction of Carex maritima (Cyperaceae)……………………... 187 Abstract ………………………………………………………………... 189 Introduction ……………………………………………………………. 189 Materials and methods ………………………………………………… 190 Results …………………………………………………………………. 192 Discussion …………………………………………………………….. 195 Acknowledgements ……………………………………………………. 198 References ……………………………………………………………... 198 Appendix S1 …………………………………………………………... 201 Appendix S2 …………………………………………………………....... 217 Chapter 5. Two independent dispersals to the Southern Hemisphere to become the most widespread Carex bipolar species: biogeography of C. canescens Cyperaceae) …………………………………………………………………………………… 229 Abstract …………………………………………………………………... 232 Introduction ………………………………………………………………. 234 Materials and methods ………………………………………………… 236 Results …………………………………………………………………. 240 Discussion ……………………………………………………………...... 243 Acknowledgements ……………………………………………………. 247 References ……………………………………………………………... 248 Appendix S1 ……………………………………………………………... 261 Appendix S2 ……………………………………………………………... 275 Capítulo 6. Discussion and conclusions ……………………………………….. 283 Carex arctogena is a bipolar species …………………………………….. 285 Geological and climatic changes since the Miocene that allowed Northern and Southern…………………………………………………………………... 292 Direct long-distance dispersal vs. mountain-hopping …………………. 296 North to South long-distance dispersal ………………………………... 297 Means of dispersal ……………………………………………………….. 300 Successful establishment after dispersal in Carex bipolar species………. 305 Conclusions ………………………………………………………………. 308 References ………………………………………………………………... 310 Abstract At a global level, one of the most fascinating plant distribution patterns is the bipolar disjunction. Bipolar species are defined here as species occurring at very high latitudes (>55ºN and >52ºS) in both hemispheres, regardless of their distribution in intermediate areas. Under these criteria, around 30 vascular plant species have such distribution, being Carex (Cyperaceae) the genus with the largest number of bipolar species (six). We performed a biogeographic study on three of them (C. arctogena, C. maritima and C. canescens), based on morphological, molecular and bioclimatic data to shed light on the origin of their bipolar distribution. The four traditional hypotheses accounting for this pattern were tested: vicariance, direct long-distance dispersal, mountain hopping and convergence / parallel evolution. Methods used to accomplish this objective include molecular phylogenetic and phylogeographic analyses, divergence time estimation analyses, uni- and multivariate morphometric analyses, and species niche modelling. The low levels of genetic differentiation found between populations of both Hemisphere and relatively recent times of diversification allow rejecting all but the long-distance dispersal hypothesis (including direct long distance dispersal and mountain hopping) for the studied Carex bipolar species. The studied species probably migrated from the Northern Hemisphere to the Southern Hemisphere. In the case of C. canescens, two independent dispersal events were needed to achieve its current distribution. Resumen A nivel global, uno de los patrones de distribución más fascinantes
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