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Adaptive Divergence and Speciation Across Depth in a Caribbean

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Adaptive Divergence and Speciation Across Depth in a Caribbean Louisiana State University LSU Digital Commons LSU Doctoral Dissertations Graduate School 2014 Adaptive Divergence and Speciation across Depth in a Caribbean Candelabrum Coral Carlos Andrés Prada Montoya Louisiana State University and Agricultural and Mechanical College, [email protected] Follow this and additional works at: https://digitalcommons.lsu.edu/gradschool_dissertations Recommended Citation Prada Montoya, Carlos Andrés, "Adaptive Divergence and Speciation across Depth in a Caribbean Candelabrum Coral" (2014). LSU Doctoral Dissertations. 1736. https://digitalcommons.lsu.edu/gradschool_dissertations/1736 This Dissertation is brought to you for free and open access by the Graduate School at LSU Digital Commons. It has been accepted for inclusion in LSU Doctoral Dissertations by an authorized graduate school editor of LSU Digital Commons. For more information, please [email protected]. ADAPTIVE DIVERGENCE AND SPECIATION ACROSS DEPTH IN A CARIBBEAN CANDELABRUM CORAL A Dissertation Submitted to the Graduate Faculty of the Louisiana State University and Agricultural and Mechanical College in partial fulfillment of the requirements for the degree of Doctor of Philosophy in The Department of Biological Sciences by Carlos Prada B.S., Universidad Jorge Tadeo Lozano, 2002 M.S., University of Puerto Rico, 2008 AuGust 2014 To my mother, Cielo Montoya ii Acknowledgments I would like to thank my adviser, Mike HellberG. Mike has been a perfect match for me. Mike allowed me the freedom to develop my own ideas, was instrumental in pointing out dead ends, and canalized my work to Generate publishable material of the hiGhest possible quality. Mike was always there to talk with me about my research and provided advice on my career plans. Mike has encouraGed me to write and has been Generously patience to correct all my writinGs, often within 24 hours. His close readings provided thoughtful comments that one by one have over the years sharpened my mind; making me a better communicator and a more independent researcher. Mike encouraGed me to develop my own system and supported my ideas on the importance of lonG pre-reproductive selection in long-lived orGanisms, the role of natural selection in the formation of species, and the role of plasticity in evolution. I would also like to thank Andrew Whitehead, whose admirable scholarship has impreGnated my career and increased the quality of my research. Talks with Andrew in and out of class were instrumental to my understanding of the dynamic nature of Genomes, the compleXity in GeneratinG phenotypes -incredibly understudied in biology- and the pervasive role of natural selection in evolution. I would like to thank MorGan Kelly, who provided detailed comments on Chapter 4 and was generous to agree to be part of my Graduate committee after Bryan Carstens moved to Ohio State. I thank Robb Brumfield, who provided advice for my research and career as a whole. Robb deepened my knowledGe about the neutral theory and the coalescent, especially as they apply to systematics. HavinG a committee member from the Museum also opened the possibility to learn about vertebrate evolution, especially of Neotropical birds. The HellberG lab members also provided unlimited support to my research durinG my stay in Baton RouGe. I want to hiGhliGht Melissa Debiasse, my lab sister, whom I shared most of my academic eXperiences. Melissa reviewed various aspects of my dissertation, spent unlimited hours talkinG with me, debunked my ideas and increased my oral communication skills. Melissa’s inteGrity is admirable and I had not remembered a sinGle misunderstandinG with her even durinG moments of eXtreme pressure. I also thank Ron, Alice, Karine, Mark, Cata and MaXine from whom I learned at different times durinG my Ph. D. I would like to thank Bill Eberhard and Mary Jane West-Eberhard for spendinG many hours talkinG to me about my ideas, provide advice, and most of all for sharinG their admirable and enviable inteGrative view of evolution. I feel fortunate to have my understandinG of the role of plasticity in evolution –often underappreciated and misunderstood in bioloGy- shaped first hand by Mary Jane. I am Glad to have such prestiGious bioloGists as my Guides durinG my Ph. D. I thank Louisiana State University, the Department of Biological Sciences and the Graduate School, which provided me with numerous opportunities, including the Huel D. Perkins and the Graduate Year fellowships, which financed my studies and provided freedom to devote my time entirely to research. I would also like to thank the academic community at the Systematics, EcoloGy, and Evolution division at LSU and the folks at the Museum. The wide iii variation in species, techniques and approaches has enriched my carrier and constructed bridges for future collaborations. I specially thank Sandra Galeano and Metha Klock, who provided unforgettable talks during coffee breaks. Funds for this project came from the National Science Foundation (OCE-0550270 to Baums and Hellberg and DEB-1311579 to Prada and HellberG), the Society for Systematic BioloGists, a Rosemary Grant Award from the Society for the Study of Evolution, a Lerner Gray Award from the American Museum of Natural Science, the Department of Marine Sciences of the university of Puerto Rico, MayaGuez throuGh Richard Appeldorn and the NOAA project NA06NOS4780190. I would also like to thank Howard Lasker, who Generously allowed me to join his team in The Bahamas. I also thank Mark Vermeij and the Caribbean Research and ManaGement of Biodiversity (CARMABI) and Rachael Collin and The Smithsonian Tropical Research Institute for their valuable support durinG field collections. Contributions from Shelby Mcllroy, Mary Alice Coffroth, Daniel Valient and Diana Beltrán helped to develop Chapter 3. Comments from Joe NieGel improved Chapter 2. I thank Paul Yoshioka, who initially inspired me to study octocorals and also provided unrestricted access to his long-term demoGraphic data of shallow-water octocorals. I thank Matt Brown and The Socolofsky Microscopy Center at Louisiana State University that provided assistance for morpholoGical measurements. Last but not least, I would like to thank my family. My mother, Cielo Montoya, is largely responsible for me beinG here, providinG the initial financial support and encouraGement to pursue graduate studies. She dedicated herself to my education durinG my elementary years and set the foundation of my reasoninG and critical thinking, which were fundamental to developing my dissertation. I thank Diana Beltran, who has stood with me all this time, has been part of most of my field eXpeditions, has supported most of my ideas and without whom I had simply not had been able to finished this dissertation. All my Gratitude for her love and patience all this time. iv Table of Contents AcknowledGments……………………………………………………………………………………. iii Abstract……………………………………………………………………………………………………..vi Chapter 1. Introduction……………………………………………………………………………….1 Chapter 2. Long Pre-reproductive Selection and Divergence by Depth in a Caribbean Candelabrum Coral……………………………………………………………………..6 Chapter 3. Cryptic Diversity Hides Host and Habitat Specialization in a Gorgonian-algal Symbiosis……………………………………………………………………... 22 Chapter 4. Strong Natural Selection on Juveniles Maintains a Narrow Adult Hybrid Zone in a Broadcast Spawner………………………………………………………. 33 Chapter 5. Conclusions…….………………………………………………………………………..46 References……………………………………………………………………………………………..…48 Appendix A. Supplementary Information for Chapter 2……………………….……..67 Appendix B. Supplementary Information for Chapter 3………………………………74 Appendix C. Supplementary Information for Chapter 4………………………………75 Appendix D. Agreement to Reproduce Chapter 2………………………………………77 Appendix E. AGreement to Reproduce Chapter 3………………………………………78 Vita………………………………………………………………………………………………………….79 v Abstract Since Darwin, biologists wonder how orGanisms cope with environmental variation, why there are so many species, and how species form. In my dissertation, I explore how species of long-lived, clonal reef orGanisms originate across depth gradients. In Chapter 2, I evaluate the strength of depth to isolate populations by comparinG the Genes and morpholoGies of pairs of depth-seGreGated populations of the candelabrum coral Eunicea flexuosa across the Caribbean. Eunicea flexuosa is a long-lived clonal cnidarian that associates with an alga of the genus Symbiodinium. Genetic analysis revealed two depth- segregated lineages, each genetically well-miXed across the Caribbean. Survivorship data, combined with estimates of selection coefficients based on transplant eXperiments, suGGest that selection is strong enough to segregate these two lineages. Limited recruitment to reproductive age, even under weak annual selection advantage, is sufficient to generate habitat seGreGation because of the cumulative selection accrued during prolonged pre- reproductive growth. I then studied in detail the genetic diversity of Symbiodinium in each Shallow and Deep E. flexuosa lineage (Chapter 3). I sampled colonies of the two ecotypes across depths at three Caribbean locations. I find that each host lineage is associated with a unique Symbiodinium variant. This relationship between host and alga is maintained when host colonies are reciprocally transplanted. Even when the clades of both partners are present at intermediate depths, the specificity between host and alGal lineaGes remained. I then test whether the Shallow/Deep adaptive divergence occurs in natural populations, by eXamininG
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