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“Phylogeography and Evolution of Butterflyfish “PHYLOGEOGRAPHY AND EVOLUTION OF BUTTERFLYFISH IN THE SUBGENUS CORALLOCHAETODON: CHAETODON LUNULATUS, CHAETODON TRIFASCIATUS, CHAETODON AUSTRIACUS, CHAETODON MELAPTERUS” A THESIS SUBMITTED TO THE GRADUATE DIVISION OF THE UNIVERSITY OF HAWAI`I IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE IN ZOOLOGY (MARINE BIOLOGY) MAY 2014 By Ellen Waldrop Thesis Committee: Brian Bowen, Chairperson Robert Toonen Robert Thomson ACKNOWLEDGMENTS Funding Sources National Science Foundation Grants OCE-0453167 and OCE-0929031 to B.W. Bowen Elizabeth Alison Kay Endowed Award Graduate Student Organization Travel Grant Papahanaumokuakea Marine National Monument NOAA National Marine Sanctuaries Program MOA No. 2005-008/66882 to R.J. Toonen National Geographic Society Grant 9024-11 to J.D. DiBattista KAUST Red Sea Research Center funding to M.L. Berumen University of Hawaii at Manoa Institutional Logistic Support Toonen-Bowen Laboratory University of Hawaii Diving Safety Program University of Hawaii sequencing lab Hawaii Institute of Marine Biology Hawaii Department of Land and Natural Resources King Abdullah University of Science and Technology University of Hawaii Annual Testers Symposium 9TH Indo-Pacific Fish Conference Conservation International Coral Reef Research Foundation Phoenix Island Protected Area Dept. of the Environment, Australian Government Government of Kiribati Administration of the British Indian Ocean Territories Fagatele Bay National Marine Sanctuary (NOAA) Dept. of Marine and Wildlife Resources, American Samoa Government of Fiji and the Chiefs and people of Wagamimi, Tavewa, and ii Yasawas villages Government of French Polynesia U.S. Fish and Wildlife Service (Johnston Atoll) For assistance with field work and collections, I thank Alexander Alfonso, Senifa Annadale, Kim Anderson, Paul H. Barber, Brian Bowen, W.K. Chan, J. Howard Choat, Richard Coleman, Pat and Laura Colin, Greg Concepcion, Joshua Copus, Matthew Craig, Toby S. Daly-Engel, Nancy Daschbach, Joseph DiBattista, Joshua A. Drew, John L. Earle, Jeff Eble, Kevin Flanagan, Michelle R. Gaither, Brian D. Greene, J.P Hobbs, Matthew Iacchei, Stephen A. Karl, Randall K. Kosaki, Carl G. Meyer, Darren Okimoto, Yannis P. Papastamatiou, David Pence, Mark Priest, Jon Puritz, Richard Pyle, John Randall, Joshua Reece, D. Ross Robertson, Luiz Rocha, Nick Russo, Jennifer Schultz, Charles Sheppard, Derek Skillings, Derek Smith, Zoltan Szabo, Sue Taei, Kim Tenggardjaja, Tukabu Teroroko, Robert Thorn, Allen Tom, Bill Walsh, Christie Wilcox, Ivor Williams, Jill Zamzow, and the crew of the R.V. Hi’ialakai. For logistic support, advise, and valuable consultation, I thank Robert Toonen, Robert Thomson, John Randall, Stephen Karl, Jo-Ann Leong, David Pence, Luiz Rocha, Joseph DiBattista, Jason Jones, Narineh Nazarian, Les Watling, Michelle Gaither, Iria Fernandez-Silva, Zac Forsmen. Finally, I would like to thank my husband Anthony and my family for all of their love and continued support. iii ABSTRACT The subgenus Corallochaetodon consists of four partially overlapping specialized corallivores: Chaetodon lunulatus (Pacific Ocean), Chaetodon trifasciatus (Indian Ocean), Chaetodon melapterus (northern Indian Ocean), Chaetodon austriacus (Red Sea). Phylogenetic and population genetic analysis of mtDNA cytochrome b sequences reveal divergent patterns of genetic diversity and population structure. Phylogenetic reconstruction shows that C. lunulatus diverged from sister species C. trifasciatus approximately 3 million years ago, while C. melapterus and C. austriacus comprise a cluster of closely related haplotypes derived from C. trifasciatus over the last half million years. Microsatellite loci analysis revealed varying levels of population structure in C. lunulatus and C. trifasciatus. This evolutionary divergence may have been initiated along biogeographic boundaries such as the barrier between Indian and Pacific Oceans, and between the Indian Ocean and Red Sea. Species integrity in regions of overlap may be reinforced by ecological factors such as mate choice, habitat preferences, and the documented differences in coral prey between species. iv TABLE OF CONTENTS ACKNOWLEDGMENTS...................................................................................................ii ABSTRACT.......................................................................................................................iv LIST OF TABLES.............................................................................................................vii LIST OF FIGURES..........................................................................................................viii CHAPTER 1 GENERAL INTRODUCTION.....................................................................9 CHAPTER 2 PHYLOGEOGRAPHIC PATTERNS IN THE BUTTERFLYFISH SUBGENUS CORALLOCHAETODON............................................................................15 INTRODUCTION.................................................................................................15 MATERIALS AND METHODS...........................................................................17 Sample Collection......................................................................................18 Mitochondrial DNA Sequencing................................................................18 RESULTS..............................................................................................................21 Genetic diversity within species.................................................................21 Genetic divergence between species..........................................................23 DISCUSSION........................................................................................................25 Population Structure..................................................................................25 Range Size and Marine Biogeography......................................................28 Implications of Specialization....................................................................32 CONCLUSION......................................................................................................34 CHAPTER 3 INTRA-SPECIES DIFFERENTIATION IN THE BUTTERFLYFISH SUBGENUS CORALLOCHAETODON (Chaetodon lunulatus and C. trifasciatus)......35 INTRODUCTION.................................................................................................35 MATERIALS AND METHODS..........................................................................36 RESULTS..............................................................................................................39 Chaetodon lunulatus..................................................................................39 Chaetodon trifasciatus...............................................................................42 DISCUSSION........................................................................................................43 Chaetodon lunulatus..................................................................................43 v Chaetodon trifasciatus...............................................................................45 CONCLUSION......................................................................................................46 CHAPTER 4 FINAL SUMMARY....................................................................................48 APPENDIX........................................................................................................................49 LITERATURE CITED......................................................................................................50 vi LIST OF TABLES Table 2.1. Sample size and molecular diversity indices for C. lunulatus, C. trifasciatus, C. melapterus, and C. austriacus based on mtDNA cytochrome b (cyt b) data........21 Table 2.2. Matrix of population pairwise ΦST values and associated P values based on mtDNA cyt b sequence data from C. lunulatus.....................................................22 Table 2.3. Matrix of population pairwise ΦST values and associated P values based on mtDNA cyt b sequence data from C. lunulatus Hawaiian sampling locations......22 Table 2.4. Matrix of population pairwise ΦST values and associated P values based on mtDNA cyt b sequence data: C. trifasciatus, C. melapterus, C. austriacus..........23 Table 2.5. Estimation of divergence time between species...............................................32 Table 3.1. Characteristics of microsatellites used in this study, developed for C. lunulatus by Lawton et al. 2010.............................................................................................37 Table 3.2. Matrix of population pairwise FST values and associated P values based on microsatellite genotypes for C. lunulatus..............................................................40 Table 3.3. Microsatellite statistics averaged over all loci for each location and species...41 Table 3.4. Matrix of population pairwise FST values and associated P values based on microsatellite genotypes for C. trifasciatus...........................................................44 Table A.1. Matrix of population pairwise ΦST values, FST values, and associated P values for C. lunulatus at Hawaiian sampling locations...................................................49 vii LIST OF FIGURES Figure 1.1. The subgenus Corallochaetodon, including four sister species......................10 Figure 1.2 Distribution map of the Corallochaetodon subgenus.......................................13
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