SPECIATION AND DIVERSIFICATION IN THE INDO-WEST PACIFIC: INFERENCES FROM THE MOLECULAR SYSTEMATICS OF REEF-ASSOCIATED CRUSTACEANS By MARIA CELIA DEFRANCE MALAY A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY UNIVERSITY OF FLORIDA 2010 1 © 2010 Maria Celia Defrance Malay 2 To my extraordinary grandparents, Marie Leprêtre Defrance, Léonce Defrance, Paula Carolina Santos Malay, and Armando de Jesus Malay 3 ACKNOWLEDGMENTS Acknowledgments for Chapter 2: We are deeply grateful to Joseph Poupin for his advice, encouragement, specimens, and for kind permission to use the images and information posted on his excellent website on Calcinus. Yoyo Rahayu kindly lent us a paratype specimen, and Regis Cléva facilitated access to the MNHN collections. We thank Patsy McLaughlin and Joseph Poupin for help with some of the identifications. We wish to acknowledge the many people who contributed specimens to this study: D. Eernise, M. Frey, J. Hooper, L. Kirkendale, J. O’Donnell, B. Olaivar, C. Pittman, J. Poupin, L. Rocha, W. Sterrer, and P. Wirtz. Photo credits: J. Poupin (C. californiensis, explorator, imperialis, inconspicuus, mclaughlinae, orchidae, pascuensis, aff. sirius), L. Albenga (albengai, aff. albengai), J. Hoover (hakahau), W. Sterrer (verrilli), C. d’Udekem d’Acoz (tubularis), P. Wirtz (talismani), J. Okuno (anani), and D.L. Felder (obscurus). All other photos are by G. Paulay and M. Malay. We are also grateful to Mike Hellberg and 3 anonymous reviewers for their helpful comments on the manuscript. Acknowledgements for Chapters 3 and 4: I am grateful to Bill Newman, Arnold Ross (1936-2006), Roger Portell, Yair Achituv, Andrew Hosie, Fabio Pitombo, and Benny Chan for patiently answering my questions on barnacle taxonomy, morphology, and evolution. For contributing samples, I thank Patricia Cabezas-Padilla, Camilla Floros, François Michonneau, Seabird McKeon, Lisa Kirkendale, John Starmer, Gustav Paulay, Helmut Zibrowius, Yair Achituv, and Andrew Hosie. For contributing sequences and for logistical support in sequencing, I thank Marcos Pérez-Losada, Maegan Finley, Chris Meyer, and Maggie Fagan. I also wish to acknowledge help from Rebecca Kimball, Ed Braun, Mike Miyamoto, and Fan Qiu for advice on topological tests, and 4 Pam Soltis for advice on how to deal with missing data. For logistical and/or administrative support in field work, I am very grateful to Annete Juinio-Meñez, Perry Aliño, Edgardo Gomez, Wilfredo Licuanan, the University of the Philippines Marine Science Institute, Keryea Soong, Minghui Chen, Michel Claereboudt, Esther Emmanuelli, Vincent Hollevout, the École Pratique des Hautes Études (EPHE), the Centre des Recherches Insulaires et Observatoire de l’Environnement (CRIOBE) in Mo’orea, the Gump Station in Mo’orea, Mireille Guillaume, Henrich Bruggemann, the Université de la Réunion, Philippe Bouchet, Victor Bonito, Miri Tabaiwalu and everyone in the village of Votua, Gerald McCormack, and Teina and Jackie Rongo. Jada-Simone White generously allowed me to use her larval culturing setup at the Gump Station in Mo’orea. I thank my two student volunteers, Karina Concha and Austin Perlmutter, for all their hard working help in dissecting barnacles and setting up PCRs. I am grateful to the governments of the Republic of the Philippines, the Gouvernement de la Polynésie Française, the Republic of the Fiji Islands, the Government of the Cook Islands, Taiwan/the Republic of China, the Sultanate of Oman, Terres Australes et Antartiques Françaises (TAAF), and the Republic of France, for granting permission to sample in their territories. I am exceedingly grateful for financial support I have received through the years from the University of Florida Alumni Fellowship, the Department of Zoology (now Biology), the Brian Riewald Memorial Fund Research Grant, the Leila and William Brayfield Scholarship in Invertebrate Paleontology, the Lerner-Gray Grant at the American Museum of Natural History, the FACE program (Ocean Bridges: A Florida- France Training & Research Cooperative in Coral Reef Conservation and Biodiversity), 5 the Kuroshio Research Fellowship at the National Sun Yat-Sen University of Taiwan, the American Microscopical Society, the Crustacean Society, and the Carcinological Society of Japan. The Florida Museum of Natural History and the Department of Biology at the University of Florida have been excellent academic homes throughout my PhD. I am most grateful to the team at the Invertebrate Zoology lab at FLMNH, especially Mandy Bemis, Sarah McPherson, Jenna Moore, Chelsey Campbell, Kim Kemppanion, and John Slapcinsky, for all the curatorial support. I also acknowledge Chris Meyer, Lisa Kirkendale, Jessica Light, François Michonneau, and Nat Evans for advice on phylogenetic programs and analyses; and Matt Gitzendanner and the University of Florida Phyloinformatics Cluster for High Performance Computing in the Life Sciences for computational support. My committee members David Reed, Pam Soltis, Rebecca Kimball, and Mike Miyamoto were there to help me throughout the long process of the PhD, and I wish to thank them for their support. I most gratefully acknowledge my awesome PhD supervisor, Gustav Paulay, for all the intellectual, financial, logistical, emotional support through the years, and for getting me started on these projects in the first place. None of these studies would have been possible without him. Lastly, I thank my family; my Mama and Papa, my sister Pat and brother Ali, my cousins near and far, aunts and uncles, and my dear departed grandparents; all of whom I love so much and who love me equally back. My fiancé Jimmy Huang gave me all-out love and emotional and moral support through these years, and kept me honest and grounded on reality. Jimmy’s family, especially Ping, have been wonderfully 6 supportive too. Lastly I thank all my friends, old and new (there are too many to mention!) for their love. 7 TABLE OF CONTENTS page ACKNOWLEDGMENTS ...................................................................................................... 4 LIST OF TABLES .............................................................................................................. 11 LIST OF FIGURES ............................................................................................................ 12 ABSTRACT........................................................................................................................ 15 CHAPTER 1 INTRODUCTION ........................................................................................................ 17 Introduction to Indo-West Pacific Marine Biogeography ........................................... 17 Overall Goals .............................................................................................................. 22 2 PERIPATRIC SPECIATION DRIVES DIVERSIFICATION AND DISTRIBUTIONAL PATTERN OF REEF HERMIT CRABS (DECAPODA: DIOGENIDAE: Calcinus) ............................................................................................ 24 Introduction ................................................................................................................. 24 Materials and Methods ............................................................................................... 26 Specimens ............................................................................................................ 26 Molecular Methods ............................................................................................... 28 Sequence Analysis............................................................................................... 29 Molecular Clock Analysis ..................................................................................... 31 Analysis of Speciation and Biogeography ........................................................... 32 Results ........................................................................................................................ 34 Sequence Attributes ............................................................................................. 34 Phylogeny Reconstruction and Species Boundaries .......................................... 34 Molecular Clock Results ...................................................................................... 36 Distribution of Calcinus Species .......................................................................... 36 Diversity Patterns in Calcinus .............................................................................. 37 Speciation ............................................................................................................. 37 Discussion ................................................................................................................... 38 Species Boundaries ............................................................................................. 38 Evolution of Color Patterns .................................................................................. 41 Geography of Speciation ..................................................................................... 42 Inter-Regional Comparisons ................................................................................ 46 Ecology ................................................................................................................. 47 Diversity Patterns ................................................................................................