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A Dissertation Submitted to the Faculty of the Richard Gilder Graduate MORPHOLOGICAL AND MOLECULAR EVOLUTION OF SEA ANEMONES AS REVEALED BY AN EMERGING MODEL ORGANISM: AIPTASIA (CNIDARIA: ACTINIARIA: AIPTASIIDAE) A Dissertation submitted to the Faculty of The Richard Gilder Graduate School at the American Museum of Natural History in partial fulfillment of the requirements for the degree of Doctor of Philosophy By Alejandro Grajales, M.Sc. Richard Gilder Graduate School at the American Museum of Natural History New York, NY January 31, 2014 © Copyright 2014 by Alejandro Grajales M.Sc. All Rights Reserved ii MORPHOLOGICAL AND MOLECULAR EVOLUTION OF SEA ANEMONES AS REVEALED BY AN EMERGING MODEL ORGANISM: AIPTASIA (CNIDARIA:ACTINIARIA:AIPTASIIDAE) Alejandro Grajales M.Sc. Chair: Estefanía Rodriguez, Ph.D. ABSTRACT Sea anemones (Cnidaria: Actiniaria) of the family Aiptasiidae Carlgren, 1924 are conspicuous members of shallow-water environments and several species within the family are widely used as model systems for studies of cnidarian-dinoflagellate symbiosis and coral bleaching. Although previously published phylogenetic studies of sea anemones recovered the family Aiptasiidae as monophyletic, they only included partial sampling of its diversity. This study explores the diversity within this group of organisms in an integrative way, from the family to population levels. In this study, I explored the morphological and molecular diversity of the group using newly collected material covering the distribution of most of the described genera and species. The family Aiptasiidae was found to be a monophyletic lineage. Similarly, most of the genera within the family represent monophyletic lineages, with the exception of the genus Aiptasia, now divided into Aiptasia and Exaiptasia. Bellactis Dube, 1983 and Ragactis Andres, 1883 are now genera included within Aiptasiidae, in agreement with previous morphological studies and the morphological homogeneity observed here by the members of this family. In addition, I discovered new diagnostic morphological characters supporting the relationships among the major clades within the family. The iii molecular phylogenetic results provided evidence to diagnose two species within Exaiptasia: E. pallida—a single widespread species—and a new cryptic species, E. brasilensis sp. nov.—restricted geographically to the southwestern Caribbean Sea and the southwestern Atlantic Ocean. Finally, although the algal diversity within the group showed no evidence of coevolution at the family level, an interesting pattern of adaptation and cladogenesis of the endosymbiotic algae (Symbiodinium spp.) was found within host species. iv ACKNOWLEDGEMENTS I am very grateful to colleagues who assisted with fieldwork, particularly to C. Arvanitidis (Hellenic Centre for Marine Research, MRC, Greece), A. Baird (James Cook University, Townsville, Australia), J. Campbell (Smithsonian Marine Station at Fort Pierce, USA) R. Collins (Smithsonian Tropical Research Institute, STRI, Panama), V. Cumbo (James Cook University, Townsville, Australia), J. Frommlet (Centro de Estudios do Ambiente e do Mar, CESAM, Portugal), R. González (Universidad Nacional Autónoma de Mexico, UNAM) L. Gusmão (Universidade de São Paulo, Brazil), K. Hiscock (Marine Biological Association Plymouth, U.K.), P.J. López González (Universidad de Sevilla, Spain), P. Manent (Instituto Canario de Ciencias Marinas, Spain), O. Nir (Haifa University, Israel), J. Reimer (Ryukyus University, Okinawa, Japan) M. Takabayashi (U. Hawaii, Hilo) and P. Wirtz. Comments from M. Brugler (AMNH) M. Daly (Ohio State University) and D. Thornhill (Defenders of Wildlife, Washington) improved this manuscript. An RGGS Graduate Fellowship and student research funds and the Lerner-Gray Fund for Marine Research (AMNH) provided support for this work, as did a Doctoral Dissertation Improvement Grant (NSF DEB 1110754) to AG and ER, and the Bermuda Institute of Ocean Sciences (BIOS, Bermuda). v TABLE OF CONTENTS COPYRIGHT PAGE ............................................................................................................... ii ABSTRACT ......................................................................................................................... iii ACKNOWLEDGEMENTS .........................................................................................................v FIGURES AND TABLES ....................................................................................................... vii CHAPTER I. BACKGROUND ..............................................................................................1 CHAPTER II. MORPHOLOGICAL REVISION OF THE GENUS AIPTASIA AND THE FAMILY AIPTASIIDAE (CNIDARIA, ANTHOZOA, ACTINIARIA, METRIDIOIDEA) .........13 CHAPTER III. MOLECULAR SYSTEMATICS OF THE FAMILY AIPTASIIDAE (CNIDARIA, ACTINIARIA, METRIDIOIDEA)....................................................................121 CHAPTER IV. PATTERNS OF SYMBIODINIUM SPP. SPECIFICITY WITHIN THE FAMILY AIPTASIIDAE, A MONOPHYLETIC LINEAGE OF SYMBIOTIC OF SEA ANEMONE .................................................................................................155 CHAPTER V. CONCLUSIONS ..........................................................................................178 APPENDICES .....................................................................................................................184 vi FIGURES AND TABLES Figures 2.1 Map showing localities where studied species were collected. ............................18 2.2 External anatomy of Aiptasia couchii ....................................................................28 2.3 Internal anatomy of Aiptasia couchii. ....................................................................30 2.4 Cnidae of Aiptasia couchii .....................................................................................32 2.5 External anatomy of Aiptasia mutabilis .................................................................39 2.6 Internal anatomy of Aiptasia mutabilis ..................................................................41 2.7 Cnidae of Aiptasia mutabilis ..................................................................................43 2.8 External anatomy of Exaiptasia pallida comb. nov...............................................50 2.9 Internal anatomy of Exaiptasia pallida comb. nov ................................................52 2.10 Cnidae of Exaiptasia pallida comb. nov................................................................54 2.11 External anatomy of Aiptasiogeton hyalinus. ........................................................64 2.12 Internal anatomy of Aiptasiogeton hyalinus. .........................................................66 2.13 Cnidae of Aiptasiogeton hyalinus. .........................................................................68 2.14 External anatomy of Bartholomea annulata ..........................................................78 2.15 Internal anatomy of Bartholomea annulata ...........................................................88 2.16 Cnidae of Bartholomea annulata. ..........................................................................82 2.17 External anatomy of Bellactis ikalyseae ................................................................88 2.18 Internal anatomy of Bellactis ikalyseae .................................................................90 2.19 Cnidae of Bellactis ikalyseae. ................................................................................92 2.20 External anatomy of Ragactis lucida .................................................................... 98 vii 2.21 Internal anatomy of Ragactis lucida ................................................................... 100 2.22 Cnidae of Ragactis lucida. ...................................................................................102 3.1 Representative species of the genera within the family Aiptasiidae ....................128 3.2 Phylogenetic position of the family Aiptasiidae ..................................................137 3.3 Detailed phylogenetic relationships within the family Aiptasiidae .....................140 3.4 Parsimony character state reconstructions of morphological traits of the species within the family Aiptasiidae. ............................................................................149 4.1 Maximum likelihood (ML) tree showing the phylogenetic position of Symbiodinium spp. within members of the family Aiptasiidae ...........................158 4.2. Detailed view of Symbiodinium spp. per host genera and species .......................165 Tables 2.1 Size ranges of the cnidae of Aiptasia couchii. .......................................................34 2.2 Size ranges of the cnidae of Aiptasia mutabilis. ....................................................45 2.3 Size ranges of the cnidae of Exaiptasia pallida comb. nov ...................................56 2.4. Size ranges of the cnidae of Aiptasiogeton hyalinus .............................................70 2.5 Size ranges of the cnidae of Bartholomea annulata. ............................................84 2.6 Size ranges of the cnidae of Bellactis ilkalyseae. ..................................................94 2.7 Size ranges of the cnidae of Ragactis lucida. ......................................................104 3.1 Taxa included in this study, with voucher and location. Old species concepts, plus changes proposed in this manuscript and in Grajales et al 2013 ..................131 3.2 Morphological characters and character states of species within the family
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