Evolución del Nicho Térmico en Lagartos del Género Liolaemus e Ibéricos Thermal Niche Evolution in Liolaemus and Iberian Lizards Francisco Ferri Yáñez Universitat d’Alacant Universidad de Alicante Evolución del Nicho Térmico en Lagartos del Género Liolaemus e Ibéricos Thermal Niche Evolution in Liolaemus and Iberian Lizards Francisco Ferri Yáñez Francisco Ferri Yáñez Escola de Doctorat Tesis doctoral Escuela de Doctorado ED|UA Alicante Septiembre 2016 edua.ua.es Tesis doctoral Alicante Septiembre 2016 PHD THESIS UNIVERSIDAD DE ALICANTE, SEptEMBER 2016 INSTITUTO UNIVERSITARIO DE INVESTIGACIÓN - CIBIO UNIVERSIDAD DE ALICANTE Thermal Niche Evolution in Liolaemus and Iberian lizards Evolución del nicho térmico en lagartos del género Liolaemus e ibéricos FRANCISCO FERRI YÁÑEZ Tesis presentada para aspirar al grado de: DOCTOR POR LA UNIVERSIDAD DE ALICANTE MENCIÓN DE DOCTOR INTERNACIONAL DOCTORADO EN BIODIVERSIDAD Y CONSERVACIÓN Dirigida por: DR. MIGUEL BASTOS ARAUJO DR. PABLO MARQUET Departamento de Biogeografía y Cambio Global Departamento de Ecología Museo Nacional de Ciencias Naturales (CSIC) Pontificia Universidad Católica de Chile Bajo la tutela académica de: DR. JOSÉ RAMÓN VERDÚ FARACO Instituto Universitario de Investigación - CIBIO Universidad de Alicante Esta tesis ha sido financiada por una beca JAE-Predoc del Consejo Superior de Investigaciones Científicas (CSIC: 2010 00735) y el proyecto NICHE CGL2011-26852 del Ministerio de Economía y Competitividad. A mis abuelos, José Yáñez Verdú y María Llorens Francés A mis padres, Francisco Ferri Llorens y Amelia Yáñez Tortosa Nota acerca del idioma: En la redacción de la presente tesis doctoral se han utilizado dos idiomas: español e inglés. Los apartados Introducción, Justificación y objetivos de la tesis han sido escritos en castellano, mientras que los Capítulos 1–4 aparecen íntegramente en inglés. Se incluyen en ambos idiomas los siguientes apartados: Contenidos, Resumen de la tesis y Conclusiones. Note about the language: This PhD Thesis has been written in two languages: Spanish and English. Introduction, Rationale and Objectives, have been written in Spanish, while Chapters 1-4 are entirely in English. The following sections are included in both languages: Contents, Abstract, and Conclusions. This PhD research was financially supported by a JAE pre-doctoral grant from the Consejo Superior de Investigaciones Científicas (CSIC: 2010-00735) and research project CGL2011-26852 from the Spanish Ministry for Economy and Competitiveness. A efectos bibliográficos la obra debe citarse como sigue: Ferri-Yáñez, F. (2016). Evolución del nicho térmico en lagartos del género Liolaemus e ibéricos. Tesis Doctoral. Universidad de Alicante, Alicante (España) Ferri-Yáñez, F.(2016). Thermal Niche Evolution in Liolaemus and Iberian lizards. PhD Thesis. Universidad de Alicante, Alicante (Spain) “… species of the same genus have usually, though by no means invariably, some similarity in habits and constitution, and always in structure...” Charles Darwin - 1859 On the Origin of Species. Chapter III CONTENTS Contenidos THESIS ABSTRACT 13 Resumen de la tesis INTRODUCTION 19 Introducción Theoretical background Antecedentes y estado actual del tema Thesis Rationale, and Objectives Justificación, estructura y objetivo de la tesis References Referencias CHAPTER 1. Heat freezes niche evolution 31 El calor congela la evolución del nicho CHAPTER 2. Diversification patterns and historical biogeography of the genus Liolaemus 83 Patrones de diversificación y biogeografía histórica del género Liolaemus CHAPTER 3. Evolution of thermal traits in Liolaemus lizards 127 Evolución de los rasgos térmicos de los lagartos Liolaemus CHAPTER 4. Operative temperature as a predictor of lizard species distributions 157 La temperatura operativa como predictor de la distribución de lacértidos CONCLUSIONS 179 Conclusiones APPENDICES 187 Apéndices ACKNOWLEDGEMENTS Agradecimientos 255 11 THesis ABstract Environmental changes have shaped to a great degree the current patterns of biodiversity. In the current context of fast environmental and climatic change, there is a need to forecast how species will react to it. Species have been evolving in changing environments and continue to do so but the speed at which climate change is happening now is much faster than it normally happened before the industrial era. Due to that, it is generally assumed species will not have time to adapt so their niches will remain constant. Nevertheless there are examples of fast niche shifts and even evolutionary adaptations during short time spans so that assumption is not tested. The aims of this PhD thesis are to determine how conserved is thermal physiology in relation to temperature along the phylogeny and try to evaluate how plausible is for organisms to adapt to increasing temperatures. For that I use a highly diverse group of South American iguanid lizards as model organisms in which I measured thermal ecophysiological traits and for which I construct a time calibrated molecular phylogeny. I also use fourteen species of Iberian lacertid lizards to explore the possibility of using mathematically modeled physiological temperatures as variables for bioclimatic envelope models. In Chapter 1 I analyzed the thermal tolerances of a large number of terrestrial organisms and found that heat tolerances are strongly conserved while cold tolerances vary markedly in a pattern that is consistent across taxa for ectotherms, endotherms and plants. I argue that this asymmetry causes the thermal component of the fundamental niche to overlap between species more than previously expected. Also, as a consequence, estimated niches for cold- adapted species may underestimate their upper thermal limits and potentially exaggerated the risk from climate change. On the other hand it is unlikely that species which are close to their upper thermal limit will increase their heat tolerance. In Chapter 2 I focus on Liolaemus lizards. Here I constructed a time calibrated phylogeny and analyzed the diversification patterns of the genus in relation to climate and geological history. I set the origen of diversification of the group further back in time, questioning hypothesis of Andean vicariance as a trigger for their diversification. The general pattern of diversification suggests a gradual opening of new niches. Moreover, I find that the group shows different diversification patterns on both sides of the Andean Cordillera, and that the diversification of the Argentinian group (subgenus Eulaemus) is related to global temperature change. On the Chapter 3, I incorporated thermal physiological traits to the phylogenetic analysis and estimated how fast they have been changing in time. I show that, to keep the pace of currently increasing temperatures, traits would have to evolve four or five orders of magnitude faster than the fastest rate observed. Phylogenetic comparative analysis shows that Liolaemus thermal traits are conserved beyond what is expected by Brownian Motion alone and that thermal preferences and field temperatures show more phylogenetic inertia than thermal limits. All this makes unlikely that evolutionary adaptation of thermal 13 physiological traits may play a signifficant role in their response to climate change. In addition, I explore the possibility that comparative methods can be used to estimate missing traits in species that have not been measured. Finally, in Chapter 4 I tested the claim that bioclimatic envelope models should be fitted with direct variables. I used a dynamic climate downscaling of the Iberian Peninsula to calculate operative temperatures and use them, and air temperatures, to create bioclimatic envelope models of fourteen lacertid lizards. I show that model performance is similar when using operative or air temperatures and that temporal trends during the second half of the twentieth century do not differ significantly between variables. Our study points towards that the use of proximal variables does not always possitively affects the quality of a model. 14 ResUMen DE LA tesis Los cambios ambientales han moldeado en gran medida los patrones de diversidad biológica. En el contexto actual de rápidos cambios ambientales y climáticos se hace necesario predecir cómo reaccionarán las especies a estas presiones. Las especies han evolucionado en ambientes cambiantes y continúan haciéndolo. Sin embargo, la velocidad a la que cambia el clima en estos momentos es mucho más elevada a la de cambios climáticos anteriores a la revolución industrial. Debido a ello, se suele asumir que las especies no tendrán mucho tiempo para adaptarse, por lo que sus nichos permanecerán estables. No obstante, hay ejemplos de cambios rápidos del nicho e incluso de adaptaciones evolutivas durante breves periodos de tiempo, porque lo que esa asunción necesita ser testada. Los objetivos de esta tesis doctoral son determinar hasta qué punto está conservada la ecofisiología térmica a través de la filogenia e intentar evaluar la capacidad de adaptación de los organismos al incremento de temperatura. Para ello he utilizado un grupo altamente diverso de lagartos iguánidos de Sudamérica como modelo de estudio, en el que he medido rasgos térmicos ecofisiológicos y para los que construimos una filogenia molecular calibrada con el tiempo. Además, he utilizado catorce species de lacértidos ibéricos, para explorar la posibilidad de utilizar temperaturas fisiológicas modelizadas matemáticamente como predictores en modelos bioclimáticos. En el Capítulo 1 analicé las tolerancias