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UNIVERSITY of CALIFORNIA Los Angeles the Causes And UNIVERSITY OF CALIFORNIA Los Angeles The causes and consequences of venom evolution in cone snails (Family, Conidae) A dissertation submitted in partial satisfaction of the requirements for the degree Doctor of Philosophy in Biology by Mark Anthony Phuong 2018 © Copyright by Mark Anthony Phuong 2018 ABSTRACT OF THE DISSERTATION The causes and consequences of venom evolution in cone snails (Family, Conidae) by Mark Anthony Phuong Doctor of Philosophy in Biology University of California, Los Angeles, 2018 Professor Michael Edward Alfaro, Chair The ability to produce venom has evolved multiple times throughout the animal kingdom and consist of complex mixtures of toxic proteins. The causes and consequences of venom evolution frequently remain unclear, potentially due to the difficulty of obtaining comprehensive data on venom composition across multiple species. Here, I present an in-depth analysis of the factors governing venom evolution, and the impact of venom evolution on speciation rates. Chapter 1 focuses on the impact of diet on venom evolution. Using RNAseq data to characterize the venom cocktails of 12 Conidae species, I recovered a positive correlation between venom complexity and dietary breadth, suggesting that species with more generalist diets express a greater number of venom proteins. Chapter 2 investigates the impact of genetics on venom evolution. Using a novel targeted sequencing approach, I describe how positive selection, gene duplication, and expression regulation all contribute to the diversification of venom. Finally, in Chapter 3, I ii investigate the impact of venom evolution on speciation rates. Using a targeted sequencing approach, I characterize the venom repertoire of over 300 cone snail species and find no relationship between venom evolution and speciation rates. My results suggest that venom is not the rate-limiting factor in determining speciation events and that other factors, such as ecological opportunity or traits regulating dispersal are more critical in governing diversification patterns. iii The dissertation of Mark Anthony Phuong is approved. Thomas Duda David K. Jacobs Michael Edward Alfaro, Committee Chair University of California, Los Angeles 2018 iv TABLE OF CONTENTS ABSTRACT OF THE DISSERTATION ....................................................................................... ii ACKNOWLEDGMENTS ........................................................................................................... viii VITA/BIOGRAPHICAL SKETCH............................................................................................... xi Chapter 1: Dietary breadth is positively correlated with venom complexity in cone snails ......... 1 Abstract ....................................................................................................................................... 1 Background ................................................................................................................................. 2 Results ......................................................................................................................................... 6 Discussion ................................................................................................................................. 14 Methods ..................................................................................................................................... 22 Data availability ........................................................................................................................ 30 Acknowledgements ................................................................................................................... 30 List of Figures ........................................................................................................................... 31 List of Tables ............................................................................................................................. 32 Figures ....................................................................................................................................... 33 Tables ........................................................................................................................................ 35 List of supplementary material .................................................................................................. 36 Chapter 2: Targeted sequencing of venom genes from cone snail genomes improves understanding of conotoxin molecular evolution ......................................................................... 39 v Abstract ..................................................................................................................................... 39 Introduction ............................................................................................................................... 40 Results ....................................................................................................................................... 42 Discussion ................................................................................................................................. 46 Materials and Methods .............................................................................................................. 56 Acknowledgements ................................................................................................................... 67 List of Figures ........................................................................................................................... 69 Figures ....................................................................................................................................... 72 List of supplementary material .................................................................................................. 75 Chapter 3: Speciation rates are decoupled from venom gene diversity in cone snails ............... 78 Abstract ..................................................................................................................................... 78 Introduction ............................................................................................................................... 79 Methods ..................................................................................................................................... 81 Results ....................................................................................................................................... 94 Discussion ................................................................................................................................. 97 Data availability ...................................................................................................................... 106 Acknowledgements ................................................................................................................. 106 List of Figures ......................................................................................................................... 109 Figures ..................................................................................................................................... 111 List of supplementary material ................................................................................................ 112 vi References .................................................................................................................................. 117 vii ACKNOWLEDGMENTS Chapter 1 is a reproduction of the following published paper: Phuong, MA, GN Mahardika, ME Alfaro. (2016) Dietary breadth is positively correlated with venom complexity in cone snails. BMC Genomics 17:401. https://bmcgenomics.biomedcentral.com/articles/10.1186/s12864-016- 2755-6. For this work, MAP designed the study, conducted the field and laboratory work, carried out the bioinformatic analyses, and drafted the manuscript. GNM participated in field work. All authors read, reviewed, and approved the final manuscript. This paper is under a Creative Commons Attribution license, which means that it can be re-used in any way, subject to proper attribution. Chapter 2 is a reproduction of the following published paper: Phuong, MA, GN Mahardika. (2018) Targeted sequencing of venom genes from cone snail genomes improves understanding of conotoxin molecular evolution. Molecular Biology and Evolution 35: 1210–1224. https://doi.org/10.1093/molbev/msy034. This work was published by Oxford University Press.nFor this work, MAP designed the study, conducted the field and laboratory work, carried out the bioinformatic analyses, and drafted the manuscript. GNM participated in field work. All authors read, reviewed, and approved the final manuscript. Under the licensing agreement, authors may use their own material in other publications, provided that Molecular Biology and Evolution is acknowledged as the original place of publication and Oxford University Press is acknowledged as the publisher. Chapter 3 is based on the following manuscript that is in preparation for publication: Phuong, MA, MA Alfaro, GN Mahardika, RM Marwoto, RE Prabowo, T von Rintelen, PWH Vogt, JR Hendricks, N Puillandre. Speciation rates are decoupled from conotoxin gene diversity in cone snails. In prep. For this work, MAP designed the study, conducted the field and laboratory work, viii carried out the bioinformatic analyses, and drafted the manuscript. GNM, RMM, REP, TvR, and PWHV participated
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