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Testing Ecological Speciation in the Caribbean Octocoral Complex Antillogorgia Bipinnata-Kallos (Cnidaria: Octocorallia): an Integrative Approach

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Testing Ecological Speciation in the Caribbean Octocoral Complex Antillogorgia Bipinnata-Kallos (Cnidaria: Octocorallia): an Integrative Approach Iván F. Calixto Botía Testing Ecological Speciation in the Caribbean Octocoral Complex Antillogorgia bipinnata-kallos (Cnidaria: Octocorallia): An Integrative Approach TESTING ECOLOGICAL SPECIATION IN THE CARIBBEAN OCTOCORAL COMPLEX Antillogorgia bipinnata-kallos (CNIDARIA: OCTOCORALLIA): AN INTEGRATIVE APPROACH IVÁN FERNANDO CALIXTO BOTÍA, M.Sc. A Doctoral dissertation submitted to the Department of Biological Sciences, Universidad de Los Andes, Colombia as a requirement to obtain the degree of Doctor of Philosophy in Biological Sciences Advisor University of Los Andes JUAN ARMANDO SÁNCHEZ, Ph.D. Advisor University of Giessen THOMAS WILKE, Ph.D. UNIVERSITY OF LOS ANDES 2018 Faculty Dean: Prof. Dr. Ferney J. Rodríguez (University of Los Andes) Advisors: Prof. Dr. Juan A. Sánchez (University of Los Andes) Prof. Dr. Thomas Wilke (Justus Liebig Universität) Evaluators: Prof. Dr. Oscar Puebla (University of Kiel) Prof. Dr. Andrew Crawford (University of Los Andes) Iván F. Calixto-Botía. (2018). Testing Ecological Speciation in the Caribbean Octocoral Complex Antillogorgia bipinnata-kallos (Cnidaria: Octocorallia): An integrative approach. This dissertation has been submitted as a requirement to obtain the degree of Doctor in Philosophy (Ph.D.) Biological Sciences at the Universidad de Los Andes, Colombia, advised by Professor Juan A. Sánchez (University of Los Andes, Colombia) and Professor Thomas Wilke (Justus Liebig Universität, Germany). Table of content Introduction ………………………………………………………………………………………………………………. 1 Chapter 1. A case of modular phenotypic plasticity in the depth gradient for the gorgonian coral Antillogorgia bipinnata (Cnidaria: Octocorallia) …………………………………………………… 9 Chapter 2. Testing Adaptive genetic divergence in parallel across the depth cline: Population genomics in the coral complex Antillogorgia bipinnata-kallos (Cnidaria: Octocorallia)…….………………………………………………………………………………………………………….17 Chapter 3. Coevolution in an ecological speciation scenario: fine-scale population genomics in the gorgonian coral complex Antillogorgia bipinnata-kallos and its symbiont…...…………………………………………....................................................................... 47 TESTING ECOLOGICAL SPECIATION IN THE CARIBBEAN OCTOCORAL COMPLEX Antillogorgia bipinnata-kallos (CNIDARIA: OCTOCORALLIA): AN INTEGRATIVE APPROACH ABSTRACT The ecological speciation is a central concept in evolution to differentiate one of the two big processes by which natural selection can produce new species. Defined as the evolution of reproductive isolation by divergent natural selection in populations adapting to different ecological environments, the ecological speciation serves as a framework to test explicit predictions on the extent of natural selection to explain the diversification patterns we observe in the living forms. The present research aimed to test a putative ecological speciation scenario for two close related species where the phenotypic divergence of colonial forms overlaps between species along the depth cline. Antillogorgia bipinnata (Verrill 1864) and A. kallos (Bielschowsky 1918), conform a group of Caribbean corals where species pairs are distributed in sympatry along broad environmental ranges. We addressed this hypothesis by an integrative approach including a reciprocal transplants experiment, finding an adaptive plasticity response between depths, high survival rates and a genetic component explaining the variance of the traits assessed. Population genomic analyses with a pooling strategy detected an association between levels of genetic differentiation and habitats in four locations, implying parallel events of genetic divergence. Additionally, observations of reproductive asynchrony provided a potential mechanism for gene flow reduction. Finally, a fine-scale population genomic analysis remarkably supports the taxonomical status of the two species. Deepening in the role of plasticity, environmental mechanisms for gene flow reduction, macro- and micro-spatial genetic structure and the functional background of divergence, this research provides substantial elements to propose an ecological speciation scenario compatible with the diversification patterns for other marine organisms where the species can arise without evident barriers for the evolution of the adaptive genetic divergence. RESUMEN La especiación ecológica es un concepto central en teoría evolutiva al diferenciar uno de los dos grandes procesos por los cuáles la selección natural puede producir nuevas especies. Definida como la evolución del aislamiento reproductivo por selección natural divergente en poblaciones adaptadas a diferentes ambientes ecológicos, la especiación ecológica sirve como marco de trabajo para evaluar predicciones explícitas sobre el alcance de la selección natural para explicar los patrones de diversificación que observamos en las formas 1 vivientes. La presente investigación buscó evaluar un escenario putativo de especiación ecológica para dos especies cercanamente relacionadas donde la divergencia fenotípica de las formas coloniales se superpone entre las especies a lo largo de la clina de profundidad. Antillogorgia bipinnata (Verrill 1864) y A. kallos (Bielschowsky 1918) pertenecientes a la familia Gorgoniidae (Octocorallia), conforman un grupo de corales del Caribe donde los pares de especies se distribuyen en simpatría frente a amplios rangos ambientales. Nosotros direccionamos esta hipótesis mediante una aproximación integrativa incluyendo un experimento de trasplantes recíprocos, encontrando una respuesta plástica adaptativa entre profundidades, altas tasas de supervivencia y un componente genético explicando la varianza de los rasgos evaluados. Análisis en genómica poblacional con una estrategia de pooles detectaron asociación entre los niveles de diferenciación genética y los hábitats para cuatro regiones, implicando eventos paralelos de divergencia genética. Adicionalmente, observaciones de asincronía reproductiva proporcionaron un mecanismo potencial para la reducción del flujo génico. Finalmente, un análisis genómico a escala fina fuertemente sustenta el estatus taxonómico de las dos especies. Profundizando en el rol de la plasticidad, los mecanismos ambientales para la reducción del flujo génico, la estructura genética a escala macro y micro y el trasfondo funcional de la divergencia, esta investigación provee elementos sustanciales para proponer un escenario de especiación ecológica compatible con patrones de diversificación para otros organismos marinos, donde las especies pueden surgir sin barreras evidentes para la evolución de la divergencia genética adaptativa. INTRODUCTION A large number of studies have now emerged searching in its more intriguing details, the most inclusive theory in the field of Biological Sciences, the Natural Selection (Nielsen, Hellmann, Hubisz, Bustamante, & Clark, 2007; Rundle & Schluter, 2004). Developed by Charles Darwin and Russell Wallace, the relative role of the natural selection in the evolutionary process came to be recognized by the scientific community until the early 30 and 40’s with the evolutionary synthesis, however, testing the power of selection in speciation on in situ systems was limited in the following decades (Rundle & Schluter, 2004; Via & West, 2008). The renewed interest in recent years to assess in natural models the selective processes generating speciation is largely the result of molecular tools. Particularly, the fast advances in genomic sequencing approaches allow the recognition of heredity footprints left by selection in the evolution of species and allow to test explicit predictions about the evolution of reproductive isolation (Lee & Mitchell-Olds, 2006; Patrik Nosil, 2012; Wright & Andolfatto, 2008). Two general kinds of natural selection can be distinguished: mutation-order speciation and ecological speciation. Mutation-order speciation refers to the evolution of reproductive isolation as a consequence of different mutations fixed in separate 2 populations adapting to similar environmental pressures (Mani & Clarke, 1990; Dolph Schluter, 2009). Ecological speciation can be defined as the process by which barriers to gene flow evolve between populations as a result of ecologically based divergent selection (D Schluter & Nagel, 1995; Dolph Schluter, 2009). In this scenario, the generation of new species is a final consequence of differentiated ecological pressures, where selection directly favors the evolution of reproductive isolation (Patrik Nosil, 2012). Therefore, it has been proposed that ecological speciation can occur in both sympatric and allopatric populations, where the reproductive isolation (pre or postzygotic) finally emerges as a byproduct of divergent populations (U Dieckmann, Metz, Doebeli, & Tautz, 2004; Rundle & Schluter, 2004). The ecological speciation extending on the contemporary patterns of diversification, mechanisms and rhythm, remains unknown. Particularly, the role of phenotypic plasticity as a force of adaptive divergence promoting speciation, given the different ecological pressures, is a key question in Evolutionary biology (Aubin-Horth & Renn, S., 2009; Moczek et al., 2011). The present thesis aims to identify the ecological speciation process and propose as a research model the coral species complex Antillogorgia (=Pseudopterogorgia) bipinnata- kallos (Octocorallia: Gorgoniidae) (Williams & Chen, 2012) which, together other groups of Caribbean gorgonian corals with broad environmental status and sympatric distribution ranges, has been considered
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