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The Genetic Landscape of Caribbean Acropora Corals

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The Genetic Landscape of Caribbean Acropora Corals The Genetic Landscape of Caribbean Acropora Corals by Elizabeth M. Hemond B.A. in Environmental Biology, Columbia University M.S. in Marine Biology, University of North Carolina Wilmington A dissertation submitted to The Faculty of the College of Science of Northeastern University in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the field of Biology November 18, 2014 Dissertation directed by Steven V. Vollmer Associate Professor of Biology & Marine and Environmental Sciences Dedication This dissertation is dedicated to my husband, Raşit Bilgin. ii Acknowledgements First, I would like to thank my advisor, Steve Vollmer, for giving me the opportunity to join his lab, the chance to work on a topic of my choice, and the support to publish and finish my PhD. I also want to thank the members of my committee, Drs. Matt Bracken, Erin Cram, Les Kaufman and Geoff Trussell for their generosity with their time and their constructive feedback. I would like to thank and acknowledge Betsy Gladfelter, whose pioneering work on Acropora growth inspired much of the work presented in this dissertation. Betsy generously and openly shared her extensive knowledge, providing invaluable suggestions and critiques on this work. Thank you to the Northeastern Biology Department, the Marine Science Center and the Three Seas Program for providing teaching and research opportunities and support during my studies. In particular, I thank Frauke Argyros for her encouraging energy and advice. And thank you to the Northeastern Office of the Provost for additional financial support through the University Excellence Fellowship. This dissertation would not have been possible without the scientific support and camaraderie of the other members of the Vollmer Lab and the graduate students at the Marine Science Center. To my guardian “angle”, Silvia Libro, go endless thanks for her friendship, advice and help in all aspects of my PhD. Many thanks go to Kylla Benes, Sean Kent, David Combosch, Stefan Kaluziak, Chris Marks, Catherine Matassa, Carmel Norman, Meredith Doellman and Celia Schunter, all of whom contributed immensely to my research and experience during this time. I feel very lucky for the chance to work alongside you. iii This research was made possible due to the field and logistical support provided by the Smithsonian Tropical Research Institute in Bocas del Toro and Panama City, Panama. I am also grateful to the government of Panama for their support of basic coral reef research to understand and conserve these priceless ecosystems. The Florida component of this dissertation work was made possible by samples provided through the generosity of Mark Chiappone and Steven Miller with the support of NOAA's NURC at UNCW, and NOAA's Florida Keys National Marine Sanctuary. Finally, I want to acknowledge the support of my family, who always encouraged me to pursue my passion in biology. Most of all, I dedicate this work to my husband, Raşit Bilgin, who had faith in my ability to succeed and encouraged me throughout this long-term commitment, even from half-way across the world. iv Abstract of Dissertation This dissertation explores multiple genetic aspects of Caribbean Acropora biology with a focus on transcriptomic regulation of growth and symbiosis, in addition to population genetics. These topics are unified in the application of genetics to understanding the evolution and biology of important endangered scleractinian coral species that have historically been the foundation of many Caribbean reef ecosystems. The two true Caribbean Acropora coral species, Acropora cervicornis and A. palmata, provide an important and useful system to study coral growth because they exhibit within-colony differentiation of polyps, they have rapid growth rates, and they are sister species with distinctive growth morphologies. With an emphasis on A. cervicornis in Florida, Caribbean Acroporas are also the focus of ongoing restoration efforts to replenish their populations. This dissertation investigates: (1) gene expression patterns involved in growth, calcification and division of labor within the coral colony, (2 & 3) differences in gene expression between day and night for both the coral host and their endosymbiotic Symbiodinium, and (4) population genetic structure and viability of A. cervicornis in a highly disturbed reef system, the Florida Keys. The first three studies employ next-generation RNA sequencing (RNA-seq) analyses to evaluate gene expression profiles in Caribbean Acropora corals and their Symbiodinium. These three studies also explore the differences in gene expression due to division of labor within the colony, using samples from coral colony branch bases and tips. The comparison of functionally different regions of the colony for the two species revealed that adult coral Acropora colonies have a high degree of genetic division of labor (> 2200 differentially expressed transcripts) within the colony and up-regulate numerous genes involved in developmental signaling among v other processes in the growing region of the colony. Both Acroporas appear to use similar genes for growth, but differences in growth form between species may be related to developmental signaling pathways, bicarbonate transport and extracellular matrix proteins. The comparison of coral gene expression in A. cervicornis samples between day and night revealed a potential influence of symbiont photosynthesis on coral circadian gene expression, as well as the potential control of Symbiodinium populations by nitrogen regulation and the glutamine metabolic pathway. Taking advantage of the same samples and RNA-seq data to evaluate Symbiodinium gene expression between day and night and within the coral colony revealed a diel aspect of transcription-driven photoacclimation in Symbiodinium, but low magnitude gene expression changes suggest that some photosynthesis proteins may be post-transcriptionally regulated. Additionally, expression of some Symbiodinium genes differed between regions of the colony, suggesting that coral-driven regulation of symbiont populations may affect symbiont transcription. The final study utilized a mitochondrial DNA marker to characterize the genetic diversity of A. cervicornis in the Florida Keys and to understand relationships among Florida Keys and Caribbean populations. The results indicate high genetic diversity and connectivity within Florida with limited genetic exchange between Florida and other reefs in the Caribbean. This information can be used to support conservation policies for this species. vi Table of Contents Page Dedication .................................................................................................................ii Acknowledgements ..................................................................................................iii Abstract of Dissertation ...........................................................................................v Table of Contents .....................................................................................................vii List of Figures ...........................................................................................................xi List of Tables ............................................................................................................xiii Chapter 1. General Introduction Overview ...............................................................................................................1 Coral physiology and biochemistry ......................................................................6 Cnidarian development and colony coordination .................................................11 Symbiosis with Symbiodinium spp. ......................................................................13 Effects of climate change and increasing CO2 on corals ......................................15 Caribbean Acropora corals ...................................................................................17 Molecular techniques ............................................................................................20 Dissertation objectives ..........................................................................................22 Chapter 2. The Genetics of Colony Form and Function in Caribbean Acropora Corals Abstract .................................................................................................................24 Background ...........................................................................................................26 Methods.................................................................................................................30 vii Page Results and discussion .........................................................................................34 Conclusion ............................................................................................................63 Availability of supporting data .............................................................................63 List of abbreviations .............................................................................................64 Acknowledgements ...............................................................................................64 Tables ....................................................................................................................65 Figures...................................................................................................................70 Chapter 3. Diurnal and
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