Population Genetics and Phylogeography of Hawaiian Coral Reef Echinoderms

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Population Genetics and Phylogeography of Hawaiian Coral Reef Echinoderms ISLANDS, ARCHIPELAGOS, AND BEYOND: POPULATION GENETICS AND PHYLOGEOGRAPHY OF HAWAIIAN CORAL REEF ECHINODERMS A DISSERTATION SUBMITTED TO THE GRADUATE DIVISION OF THE UNIVERSITY OF HAWAI‘I AT MĀNOA IN PARTIAL FULFILLMENT OF THE REQUIREMENT FOR THE DEGREE OF DOCTOR OF PHILOSOPHY IN ZOOLOGY AUGUST 2012 By Derek J. Skillings Dissertation Committee: Robert Toonen, Chairperson Brian Bowen Charles Birkeland Andrew Taylor Ronald Bontekoe i DEDICATION This dissertation is dedicated to my wife, Melissa Kay Skillings. ii ACKNOWLEDGEMENTS First, I would like to thank my committee members who provided essential guidance and encouragement throughout my graduate career. Foremost, I would like to thank my advisor and committee chair Rob Toonen. He has generously offered me a near endless supply of advice and guidance, as he does for anyone who knocks on his door. He also gave me the flexibility and encouragement needed to make getting two simultaneous graduate degrees possible. My graduate career has been very unconventional, and Rob has supported me every step of the way. I would like to thank Brian Bowen for giving me the structure I needed to succeed. Given my tendency to get lost in an always increasing number of projects, I would have never finished in a reasonable amount of time without his firm hand at setting deadlines and his enthusiastic encouragement to meet those deadlines. Rob and Brian gave me the perfect balance of freedom and focus that I needed to succeed. I would like to thank Chuck Birkeland for helping me to put my work in the larger perspective of coral reef ecosystems. Chuck also encouraged my philosophical and historical investigations into biology through insightful conversation; every time I saw he seemed to have a valuable and important text that he wanted to give me for my collection, many from his personal library. I would like to thank Andy Taylor for his critical eye, for being able to see through the details to get at the heart of the problem. Andy first taught me statistics, a field that I didn’t appreciate at first, but have since come to focus on greatly because of his influence. Even though we have come to take different approaches to statistics, he has always challenged me in a way that has made my thinking clearer and has made me a better academic. Finally, I would to thank Ron Bontekoe for his dual service as a committee member for my PhD and as my advisor for my philosophy MA. His insightful questions and critical feedback have pushed my writing leaps and bounds ahead of where I thought it could be. iii Thank you to the facility, staff, and postdoctoral researchers at the Hawai‘i Institute of Marine Biology and the University of Hawai‘i at Mānoa Zoology department. I would like to thank: Matt Iacchei, Michelle Gaither, Jon Puritz, Joseph DiBattista, Mike Stat, Zoltan Szabo, Greg Concepcion, Kim Andrews, Marc Crepeau, Steve Karl and the rest of the extended ToBo lab for helpful discussions and support. I would especially like to thank Chris Bird, who spent many hours teaching me the skills I needed to be a successful molecular biologist. This work was made possible by the financial support of several agencies including: National Science Foundation, Papahānaumokuākea Marine National Monument, Northwestern Hawaiian Islands Coral Reef Reserve, University of Hawai‘i Art and Sciences Council, and the Jessie D. Kay Fellowship. iv ABSTRACT Genetic connectivity determines the evolutionary independence of populations and plays a primary role governing intraspecies evolution. Patterns of genetic connectivity can also be used to make inferences about macroevolutionary processes. For my dissertation I used mtDNA sequences in phylogeographic and population level analyses to examine connectivity within and between Pacific Archipelagos, utilizing four species of tropical echinoderms. First, I review and prescribe non-lethal sampling techniques for use in genetic studies of many species of marine invertebrates. Second, I showed that two species of sea cucumber, Holothuria atra and Holothuria whitmaei, with a similar life history, species range, and habitat usuage cannot be used as proxies for each other in order to predict phylogeographic patterns, degree of connectivity, and population genetic structure within the Hawaiian Archipelago. Third, I examined the genetic population structure of H. atra across the central tropical Pacific to show that despite its large range, H. atra has hierarchical, fine-scale population structure driven primarily by between- archipelago barriers, but with significant differences between sites within an archipelago. Finally, I compared population genetic patterns in two congeneric brittle stars, Ophiocoma pica and Ophiocoma erinaceous, across Hawai‘i and Central and Eastern Polynesia. I found contrasting phylogeographic patterns in these two similar species, as was the case with H. atra and H. whitmaei. Given the real-world constraints of limited time and money in marine ecosystem management it would be ideal if model species could stand in as proxies for a host of similar species. This dissertation shows that this ideal scenario is unlikely to be the case; similar life histories and close phylogenetic relationships do not appear to predict population connectivity. Generalizations based on a few representative taxa are unlikely to offer much in terms of delineating boundaries for spatial management areas. Though a more inclusive multi-species v approach is bound to cost more in terms of time and resources, it should ultimately payout as more informed, if complex, management. vi TABLE OF CONTENTS Dedication ………………………………………………………………………………… ii Acknowledgements ………………………………………………………………………... iii Abstract …………………………………………………………………………………... v List of Tables ……………………………………………………………………………... ix List of Figures ……………………………………………………………………………... x Chapter 1: Introduction …………………………………………………………………... 1 References ………………………………………………………………………... 5 Table ……………………………………………………………………………. 9 Chapter 2: It’s Just a Flesh Wound: Non-lethal Sampling for Conservation Genetics Studies……………………………………………………………………...…………... 12 Abstract …………………………………………………………………………... 13 Introduction ………………………………………………………………………... 13 Methods ...………………..………………………………………………………... 15 Discussion ………………………………………………………………………... 20 Conclusions ……………………………………………………………………….. 23 Acknowledgements ……………………………………………………………….. 23 References ………………………………………………………………………... 25 Figure ..…………………………………………………………………………...... 27 Chapter 3: Contrasting Phylogeography of Two Coral Reef Sea Cucumbers, Holothuria atra and Holothuria whitmaei ………………….…………………………………….. 28 Introduction ……………………………………………………………………... 29 Methods ……………………………………………………………………...……. 35 Results ……………………………………………………………………...……… 38 Discussion …………………………………………………………………...…… 42 Conclusions ……………………………………………………………………….. 46 References …………………………………………………………………...…… 47 Tables ……………………………………………………………………...……… 60 Figures …………...……………………………………………………...………… 65 Chapter 4: Gateways to Hawai‘i – Genetic population structure of the tropical sea cucumber Holothuria atra ……………………………………………….…………… 68 vii Abstract ………………………………………………………...………………… 69 Introduction ………………………………………………………………...……… 69 Methods ……………...……………………………………………………..……. 73 Results ……………………………………………………………………………... 78 Discussion ………………………………………………………………………… 82 Conclusions ……………………………………………………………………….. 88 Acknowledgments ………………………………………………………………… 89 References ………………………………………………………………………... 91 Figures ………………………………………………………...………………… 104 Tables ………………………………………………………………………...…… 106 Appendices ………………………………………………………………………... 110 Chapter 5: Contrasting Phylogeography Patterns in Two Pacific Brittle Stars, Ophiocoma erinaceous and Ophiocoma pica …………..………………………………………...… 113 Introduction ………………………………………………………………...……… 114 Methods ……………...……………………………………………………..……. 119 Data Analysis ……………………………………………………………………... 121 Results ……………………………………………………………………………... 123 Discussion ………………………………………………………………………… 127 Conclusions ……………………………………………………………………….. 131 References ………………………………………………………………………... 132 Tables ………………………………………………………………………...…… 146 Figures ………………………………………………………...………………… 150 Chapter 6: Summary and Synthesis ………………..…………………...………………… 152 Summary ………………………………………………………………...………… 153 Synthesis ………...…...……………………………………………………..……. 155 viii LIST OF TABLES Chapter 3: Contrasting Phylogeography of Two Coral Reef Sea Cucumbers, Holothuria atra and Holothuria whitmaei Table 3.1 Molecular diversity indices and sample sizes ………..........…………… 61 Table 3.2 Pairwise F statistic comparisons ………………………………...…...… 62 Table 3.3 Pairwise Dest_chao comparisons …………………………………………. 63 Table 3.4 AMOVAs by region ……………………………………………………. 64 Table 3.5 Pairwise population migration rate estimates …………………………... 65 Chapter 4: Gateways to Hawai‘i – Genetic population structure of the tropical sea cucumber Holothuria atra Table 4.1 Molecular diversity indices and sample sizes ………………………… 107 Table 4.2 Pairwise Dest_chao and FST comparisons ……………………….……….. 108 Table 4.3 AMOVAs for different population groupings ……………………….… 109 Table 4.4 Pairwise population migration rate estimates ………………..………… 110 Chapter 5: Contrasting Phylogeography Patterns in Two Pacific Brittle Stars, Ophiocoma erinaceous and Ophiocoma pica Table 5.1 Molecular diversity indices and sample sizes ………………………… 147 Table 5.2 AMOVAs by region …………………….…………………….……….. 148 Table 5.3 Pairwise Dest_chao and FST comparisons ……...……………………….… 149 Table 5.4 Pairwise population migration rate estimates ………………..………… 150 ix LIST OF
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