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Characterizing Venom Gene Expression, Function and Species Diversity in Predatory Marine Snails of the Terebridae

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Characterizing Venom Gene Expression, Function and Species Diversity in Predatory Marine Snails of the Terebridae City University of New York (CUNY) CUNY Academic Works All Dissertations, Theses, and Capstone Projects Dissertations, Theses, and Capstone Projects 9-2018 Characterizing Venom Gene Expression, Function and Species Diversity in Predatory Marine Snails of the Terebridae Juliette Gorson The Graduate Center, City University of New York How does access to this work benefit ou?y Let us know! More information about this work at: https://academicworks.cuny.edu/gc_etds/2887 Discover additional works at: https://academicworks.cuny.edu This work is made publicly available by the City University of New York (CUNY). Contact: [email protected] CHARACTERIZING VENOM GENE EXPRESSION, FUNCTION AND SPECIES DIVERSITY IN PREDATORY MARINE SNAILS OF THE TEREBRIDAE by JULIETTE GORSON A dissertation submitted to the Graduate Faculty in Biology in partial fulfillment of the requirements for the degree of Doctor of Philosophy, The City University of New York 2018 © 2018 JULIETTE GORSON All Rights Reserved ii Characterizing venom gene expression, function and species diversity in predatory marine snails of the Terebridae by Juliette Gorson This manuscript has been read and accepted for the Graduate Faculty in Biology in satisfaction of the dissertation requirement for the degree of Doctor of Philosophy. ___________________ ______________________________________________ Date Mandë Holford, Hunter College Chair of Examining Committee ___________________ ______________________________________________ Date Cathy Savage-Dunn Executive Officer Supervising Committee Weigang Qiu, Hunter College Ntino Krampis, Hunter College Mark Siddall, American Museum of Natural History Nicolas Puillandre, Muséum National d'Histoire Naturelle Lisle Gibbs, Ohio State University THE CITY UNIVERSITY OF NEW YORK iii ABSTRACT Characterizing venom gene expression, function and species diversity in predatory marine snails of the Terebridae by Juliette Gorson Advisor: Mandë Holford The Terebridae is a group of predatory marine snails that use their venom to feed on marine annelids. Similar to other venomous organisms, the Terebridae have evolved over millions of years, diverging from their closest relative in the Paleocene era. This thesis investigates what is driving terebrid evolution and species diversification by applying a multidimensional approach to examine terebrid phylogeny, diet, and venom gene expression. The Terebridae are an ideal group for a case study in venom evolution and species diversification, as the ~ 400 described terebrid species are globally distributed, are highly representative of a broad range of foregut anatomies and produce venom peptides not found in any other venomous animal lineage to date. To provide robust hypotheses for terebrid evolution it is imperative to reconstruct a reliable phylogeny. In this thesis, an interdisciplinary approach using molecular and morphological characters was applied to reconstruct a valid working phylogeny of the Terebridae (Chapter 2). The phylogeny constructed was then used as a road map to inform questions about terebrid evolution and speciation. We identified planktotrophy as the ancestral larval state in terebrids, while lecithotrophy has evolved on at least 18 occasions and is moving towards a (small) size optimum. We also found that there is no difference in across clade diversification rates, but there is a slow increase in diversification rates over time. We determined that foregut anatomy, or the evolution of a venom apparatus, is not iv influencing diversification rates in the Terebridae. While the venom of other venomous snails, such as cone snails, have been extensively characterized, the venom of terebrids is relatively unknown and this thesis has provided the groundwork to elucidate Terebridae venom evolution and variation using next generation transcriptomic sequencing (Chapter 3). Specifically, it was discovered that the venom of the Terebridae is highly divergent from other mollusks and contains venom peptides that are unique in their structure and function. Like their venom, the diet of the Terebridae is poorly studied and this thesis presents the first molecular analyses of terebrid diet in relation to venom variation using gut metabarcoding (Chapter 4). We identified 18 species of worms in the gut of 17 terebrids, providing a foundation for exploring diet as a driver for terebrid species diversification. Finally, novel terebrid venom peptides (teretoxins) were examined by a series of functional assays to determine bioactivity (Chapter 5). This work provides the first functional bioactivity of two new teretoxins in relation to pain and diet, suggesting that these peptides may act as antinociceptive and orexigenic agents. The integrated methods applied allowed for the investigation of terebrid venom gene evolution and variation at a macro- and microevolutionary level. Terebrids are an understudied group in venom research and this multidimensional approach thoroughly advanced the knowledge of terebrid venom evolution, clarified questions about what drives venom variation in the Terebridae, and provided comparative analyses for the convergence of venom throughout the animal kingdom. v ACKNOWLEDGEMENTS I can’t believe that five years have already passed and I am publishing my dissertation as well as multiple papers about my research. When I first started at the Graduate Center, the end seemed so far away, something that I would achieve, but couldn’t even imagine. I am here today because of the dedication and passion I have for science as well as for the support that has surrounded me throughout this journey. My journey started at Hofstra University where I was getting my Master’s in marine biology. It was while at Hofstra University that I learned about cone snails. Though no one at the university studied these amazing creatures, my persistence landed me a grant to Hawaii where I was able to collect these snails and bring them back to the lab for my Master’s thesis research. It was also around this time that I landed an awesome internship at the NY aquarium and couldn’t believe that I would be creating educational programs for students to learn about marine life- it was a dream-come true. My boss at the aquarium, Chanda, put me in touch with Dr. Mandë Holford, who quickly accepted my invitation to bring the whole lab to the aquarium for a tour. It was at this time that Mandë and I first bonded and shortly thereafter, she would invite me on a collection trip to Papua New Guinea. Oh Mandë! What a ride we have been through together on this journey to explore the venom genes of the Terebridae. Mandë and I have experienced a lot together- journals rejecting our paper, arguing with the journals, the journals accepting our paper and Mandë becoming an editor at the journal. We presented our research to the Prince of Monaco, we created an exhibit at the American Museum of Natural History, and I cried with her after being hit in the head with a brick in Madang, Papua New Guinea. Mandë, I can’t imagine being mentored by anyone other than you, a social butterfly that has taught me the importance of science communication, writing, and outreach. vi I would also like to thank my wonderful committee members: Ntino, Weigang, Mark, Nico, and Lisle. Without all of your input throughout these past five years, I wouldn’t be here, defending, today. Nico, you have been especially amazing, hosting me on multiple occasions at the museum in Paris and working with me so closely on the Phylogeny project. I will always remember our trip to the AMERICAN diner in PARIS- where we stuffed our faces. I am grateful for everyone that has come through the lab and has helped me with research, given me advice, or just talked to me (for 1 min, 10 min, or 1 hour). Prachi, the post-doc of the lab, you have been an amazing friend to me since the first time we ate lunch together at Hunter North and I couldn’t stop asking you questions about your 2,000 person wedding. You have been such a huge part of my life for the past five years and I am not sure I would have made it to the end without you. Not only have you provided me with comfort over the years, you have invited me into your family. I have feasted on Mukesh’s wonderful cooking and I have gotten to watch Vrishti grow up into a mini-me! You have such an amazing daughter because you are such an amazing person. Aida, you have always been my partner in crime in the lab. We have experienced a lot together, from riding around in an Emirate’s Bentley to running around the museum creating activities 24 hours before an event! You have always provided me with someone to talk to (sorry for talking to you too much) and you have helped me understand the importance of being a woman in science. Tainya, what a kid! You have brought so much fun to the lab, with your (your mom’s) crazy stories and your upbeat personality. Let’s get chicken wings in Flushing soon. Patrick, thanks for dealing with my antics and providing me with some crazy stories. A special thank you to Emily, an amazing undergraduate who joined our lab right after being in my second ever intro chemistry class. I have gotten to see Emily grow as a person, from a girl that would cry at the smallest amount of stress to a young woman who was awarded an NSF grant and will be attending vii UCSB for a PhD program in the Fall. I am so proud of you! Also, a special thank you to Justin for being a crazy nut-ball and constantly keeping me entertained- honestly, the lab wouldn’t run without you. Although I am a scientist, I have been supported by so many others that have nothing to do with science. My family and friends have been incredible throughout my entire ride. Jan Peterson and Melissa Marquino have been there through it all. Melissa has jumped on the snail train and continues to buy me all things snail (and all things small).
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