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Amaryllidaceae) ECOLOGÍA EVOLUTIVA DEL POLIMORFISMO ESTILAR EN Narcissus papyraceus KER- GAWL. (AMARYLLIDACEAE). EVOLUTIONARY ECOLOGY OF STYLAR POLYMORPHISM IN Narcissus papyraceus KER-GAWL. (AMARYLLIDACEAE). Tesis Doctoral Violeta Simón Porcar Mayo de 2013 Directores: Dr. Juan Arroyo y Dr. F. Xavier Picó ÍNDICE Resumen General…………….……………………………………………………………………………… 15 General Abstract………..…………………..……………………………………….………………………. 16 Capítulo 1. Introducción General Chapter 1. General Introduction La ecología evolutiva en el campo de la biología floral………………...…........ 19 La heterostilia………………………………………………………………………………..………... 20 La promoción de la fecundación cruzada………………………………..……………... 23 El dimorfismo estilar…………………………………………………............................………. 26 El polimorfismo estilar en Narcissus ……………………………………..…………..…… 27 El género Narcissus L……………………………………………………………..………..……... 30 El caso de Narcissus papyraceus Ker-Gawler………………………………………..… 31 Características de Narcissus papyraceus como modelo de estudio……….. 34 Objetivos de la Tesis Doctoral……………………………………..…………………………. 37 Estructura de la Tesis Doctoral……………………………………………………………..… 38 Referencias…………………………………………………………………………………..……….... 40 Capítulo 2. La autoincompatibilidad homomórfica y ovárica en Narcissus papyraceus (Amaryllidaceae) se debe a una respuesta precigótica Chapter 2. Homomorphic ovarian self-incompatibility in Narcissus papyraceus (Amaryllidaceae) is due to a pre-zygotic response Resumen…...………………………………………………….……………………..……………………55 Abstract…....…………………………..………………………………………..……….….…….………56 Introduction…….….…………………………………………………..………………………..………57 Material and Methods………….………………………………..…………………………….… 60 Results…..…...…………………………………………………………..……………………………… 65 Discussion……....…………………………………………………………………..………………… 75 References…..…..………………………………………………………..………………………….… 79 Capítulo 3. Nuevos marcadores microsatélites para Narcissus papyraceus (Amaryllidaceae) y amplificación en otras especies congéneres Chapter 3. New microsatellite loci for Narcissus papyraceus (Amaryllidaceae) and cross-amplification in other congeneric species. Resumen ….………………………………………………………………...…….………………..…… 97 Abstract...……………………..……………………………………………..…..…….………………… 97 Introduction….………………………………………………………..…..………………...………… 98 Methods and Results ….……………………………………………..…………………….…… 101 Conclusions …..……………………………………………………….…..………….……………… 105 References …..………………………………………………………….....……………….……...… 106 Capítulo 4. Genética de poblaciones y variación en la proporción de morfos florales en toda el área de distribución de la especie dimórfica estilar Narcissus papyraceus (Amaryllidaceae) Chapter 4. Range-wide population genetics and variation in floral morph ratio in style-dimorphic Narcissus papyraceus (Amaryllidaceae) Resumen ….……………………………………………………………..………………………….… 113 Abstract..……………………………………………………………………...………..……………… 114 Introduction….……………………………………………………………...……………….………. 116 Material and Methods ….……………………………………...……...……………………..… 119 Results …...…………………………………………………………………..………………….…..… 128 Discussion …..……………………………………………………………..…….…………………… 139 References …..……………………………………………………………..…………………….….. 144 Capítulo 5. Los insectos de probóscide larga promueven la transferencia de polen entre los morfos estilares de Narcissus papyraceus (Amaryllidaceae) Chapter 5. Long-tongued insects promote disassortative pollen transfer between style-length morphs of Narcissus papyraceus (Amaryllidaceae) Resumen ….……………………………………………………………………….……..…………… 167 Abstract..…………………………………………………………………………………..…………… 168 Introduction ….………………………………………………………………………..…….……… 170 Material and Methods..….…………………………………………………………..………..… 174 Results …...………………………………………………………………………………..…………… 183 Discussion …..……………………………………………………………………….…..…………… 192 References.…..…………………………………………………………………………..…………… 197 Capítulo 6. Los cruzamientos entre morfos prevalecen en la especie dimórfica estilar sin reciprocidad sexual Narcissus papyraceus (Amaryllidaceae) Chapter 6. Disassortative mating prevails in non-reciprocal style-dimorphic Narcissus papyraceus (Amaryllidaceae) Resumen ….…………………………………………………………………….……………..……… 209 Abstract..………………………………………………………………………………………..……… 210 Introduction ….………………………………………………………………………….…..……… 212 Material and Methods ….………………………………………………………………….…… 217 Results …...………………………………………………………………………………………..…… 226 Discussion …..…………………………………………………………………………………..….… 234 References …..…………………………………………………………………………………..…… 240 Capítulo 7. Discusión General Chapter 7. General Discussion Factores implicados en el patrón de variación de la proporción de morfos en las poblaciones de Narcissus papyraceus…………..……………...… 253 El escenario poblacional para la expresión y desempeño de los morfos estilares…………………………………………………………………………. 253 Los patrones de cruzamiento de los morfos estilares…..………...… 255 La pérdida del morfo S…………………………………………….………..…….... 260 La aplicación del modelo evolutivo de la heterostilia de Lloyd y Webb al género Narcissus……………..……..…..………….………………..……….…….……. 263 Estado ancestral y selección del polimorfismo estilar…………........ 269 El dimorfismo estilar más allá de Narcissus….…………………..………. 271 Consideración final.…………………………………………...…………………..….…….……. 272 Referencias.…………………………………..………………………………………………………. 273 Conclusiones Generales…………….……………………………………………….……………..…… 285 General Conclusions……………..……………..……………………………………….………………... 289 Agradecimientos…………………..…………………………….……………………………………..…… 296 “A first-hand study is always instructive, and often... full of surprises.” R.A. Fisher 1965 RESUMEN GENERAL Narcissus papyraceus es un geófito del oeste del Mediterráneo que posee dimorfismo estilar, un polimorfismo similar a la heterostilia pero que carece tanto de reciprocidad sexual perfecta entre morfos como de sistema de incompatibilidad heteromórfico. Sin embargo, como en la heterostilia, la estabilidad evolutiva del dimorfismo estilar depende de las tasas de cruzamiento entre morfos. Las poblaciones de N. papyraceus son dimórficas (con morfos longistilo y brevistilo) en el centro y sur de su distribución, pero monomórficas (con morfo longistilo) en su límite norte. Con el fin de encontrar las causas de este patrón espacial, en esta Tesis Doctoral se estudian en detalle (i) el sistema de incompatibilidad de la especie y (ii) los patrones de polinización y de cruzamientos efectivos de los morfos florales, y se infieren (iii) los procesos demográficos poblacionales. Se muestra que, dado su sistema de autoincompatibilidad totalmente homomórfico, los patrones de polinización son altamente determinantes del éxito reproductor de los morfos florales. La mayor reciprocidad sexual dentro del morfo longistilo que dentro del morfo brevistilo favorece mayores tasas de cruzamientos entre los individuos del morfo longistilo. Además, el morfo brevistilo sufre una merma de su éxito reproductor femenino cuando actúan los polinizadores de probóscide corta. Las desventajas del morfo brevistilo se ven acentuadas por posibles eventos demográficos históricos en las poblaciones y por la selección dependiente de la frecuencia, lo cual puede haber abocado a este morfo a la extinción en las poblaciones del norte de la distribución de la especie. 15 GENERAL ABSTRACT Narcissus papyraceus is a western Mediterranean geophyte having stylar dimorphism, a polymorphism similar to heterostyly but lacking both perfect sexual reciprocity between morphs and heteromorphic incompatibility system. However, as in heterostyly, evolutionary maintenance of stylar dimorphism depends on disassortative mating rates. Populations of N. papyraceus are dimorphic (with long- and short-styled morphs) in the center and south of its range, but monomorphic (with the long-styled morph) in its northern boundary. In order to find the causes of this geographical pattern, in this PhD thesis they are studied in detail (i) the incompatibility system of the species and (ii) the patterns of pollination and effective mating of floral morphs, and they are inferred (iii) the population demographic processes. It is find out that, given their fully homomorphic self-incompatibility system, pollination patterns are highly determinant of reproductive success of floral morphs. Higher sexual reciprocity within L-morph than within S-morph favors higher rates of assortative mating in the L-morph. In addition, the S-morph suffers depletion of female reproductive success under the action of short-tongued pollinators. The disadvantages of the S-morph are accentuated by possible historical demographic events in populations and the frequency-dependent selection, which may have doomed this morph to extinction in northern populations of the species’ distribution. 16 CAPÍTULO 1 INTRODUCCIÓN GENERAL GENERAL INTRODUCTION La ecología evolutiva en el campo de la biología floral La ecología evolutiva integra la biología evolutiva con la ecología, considerando los aspectos históricos y contemporáneos que influyen en los patrones de variación y el valor adaptativo de estos últimos (Fox et al. 2001, Mayhew 2006). Esta rama de la ciencia se fundamenta en el pilar central de la teoría darwinista de la evolución (Darwin 1859): los organismos se adaptan generación tras generación a su ambiente por medio de la selección natural. Así, tanto las interacciones intraespecíficas como las interespecíficas, y las de los organismos con las condiciones geográficas, climáticas o fisiográficas de su hábitat, pueden ser fuerzas selectivas directas o indirectas que determinen evolución fenotípica en los organismos implicados (Moore et al. 1997, Hairston et al. 2005, Svensson et
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