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Phylogenetics, Systematics and Biogeography of Deep-Sea Pennatulacea (Anthozoa: Octocorallia) Evidence from Molecules and Morphology

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Phylogenetics, Systematics and Biogeography of Deep-Sea Pennatulacea (Anthozoa: Octocorallia) Evidence from Molecules and Morphology University of Southampton Research Repository ePrints Soton Copyright © and Moral Rights for this thesis are retained by the author and/or other copyright owners. A copy can be downloaded for personal non-commercial research or study, without prior permission or charge. This thesis cannot be reproduced or quoted extensively from without first obtaining permission in writing from the copyright holder/s. The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the copyright holders. When referring to this work, full bibliographic details including the author, title, awarding institution and date of the thesis must be given e.g. AUTHOR (year of submission) "Full thesis title", University of Southampton, name of the University School or Department, PhD Thesis, pagination http://eprints.soton.ac.uk UNIVERSITY OF SOUTHAMPTON FACULTY OF ENGINEERING, SCIENCE AND MATHEMATICS School of Ocean and Earth Science Phylogenetics, Systematics and Biogeography of Deep-Sea Pennatulacea (Anthozoa: Octocorallia) Evidence from molecules and morphology Submitted by Emily Dolan Thesis of the degree of Doctor of Philosophy September 2008 Graduate School of the National Oceanography Centre, Southampton This PhD dissertation by Emily Dolan has been produced under the supervision of the following persons Supervisors Prof. Paul Tyler and Dr Alex Rogers Chair of Advisory Panel Dr Martin Sheader Member of Advisory Panel Dr David Billett I hereby declare that no part of this thesis has been submitted for a degree to the University of Southampton, or any other University, at any time previously. The material included is the work of the author, except where expressly stated. 30 September 2008, Emily Dolan University of Southampton Abstract Faculty of Engineering, Science and Mathematics School of Ocean & Earth Sciences Doctor of Philosophy PHYLOGENETICS, SYSTEMATICS AND BIOGEOGRAPHY OF DEEP-SEA PENNATULACEA (ANTHOZOA: OCTOCORALLIA): EVIDENCE FROM MOLECULES AND MORPHOLOGY by Emily Dolan Despite its extreme environmental conditions, the deep sea harbours a unique and species-rich fauna of mostly unknown age and phylogeny. Pennatulids (Anthozoa: Octocorallia) are a group whose taxonomy and phylogenetic relationships remain poorly known and little studied, in spite of their abundance and ecological importance in soft- bottom communities. Phylogenetic analysis of a combination of partial ND2 and msh1 sequences produced well-supported phylogenetic relationships for representative deep- sea (and shallow-water) pennatulids at familial, generic and specific taxonomic levels. Generally, molecular data were congruent with current classification and previous phylogenetic reconstructions of the O. Pennatulacea based on morphology. Discrepancies were evident concerning the finer details for some families and genera: this can be attributable to the high frequency of homoplasy in pennatulids where reversals in evolution have led to taxa that possess apomorphic character states that are analogous with plesiomorphic traits. Genetic analysis gave strong support that highly-derived taxa occur in both shallow and deep water and that many may have differentiated and dispersed from the deep sea to the shallows. The Renillidae, which is considered one of the most primitive shallow-water families, evolved recently from deep-water ancestors. Conversely, the bathyal Anthoptilidae was the most primitive of families, and although more evidence is required, pennatulids as a group may have originated in deep water. The systematics of the exclusively deep-sea genus Umbellula, which contains forty- two species, remains unclear despite the repeated attempts of revision. Incorporating new morphological and distributional data from the examination of recently collected material, together with type specimens, genetic analysis, and a critical study of the literature, fifteen Umbellula species are here considered valid, including three new to science. Eight species lack sclerites in the autozooids, U. magniflora, U. encrinus, U. antarctica, U. carpenteri and Umbellula sp.1 n. sp. (quadrangular axes), and U. huxleyi and U. pellucida (round axes); and seven possess autozooid sclerites, U. thomsoni and U. hemigymna (quadrangular axes), and U. monocephalus, U. aciculifera, U. durissima, Umbellula sp.2 n. sp. and Umbellula sp.3 n. sp. (round axes). Biogeographic data and genetic evidence supported the hypothesis that species of Umbellula differentiated in the Indo-Pacific. Many radiated southwards to the Antarctic and later north into the Atlantic, E Pacific, Indian and Arctic oceans, occupying bathyal and abyssal depths. Other, older species that evolved via a separate evolutionary pathway, may have originated in the Indo-Pacific, and dispersed to the Subantarctic (U. sp.2 n. sp.) or Indian and Atlantic oceans (U. monocephalus). Further, morphological examination of Umbellula showed it adapted to the oligotrophic conditions of the deep sea by reducing the number but increasing the size of the autozooids, and in doing so, enlarged the food-catchment area; abyssal species have done so even more extremely. Acknowledgements I would like to acknowledge Natural Environmental Research Council (Student number NER/S/A/2004/12635) for funding this research. I owe a debt of gratitude to my supervisors Paul Tyler, Alex Rogers and Dave Billett for support, encouragement, opportunities and enthusiasm throughout. I am also grateful to Chris Hauton for his help and advice on molecular protocols, and Seb Holmes, Edward McCormack, Jim Barry and Teresa Amaro for assistance in attaining samples. I would like to acknowledge Scott France for his advice and Tomas Cedhagen for his introductions, and of course the technicians, Graeme and Mat, for their help. Also, special thanks goes to Gary Williams, for giving me inspiration in the world of pennatulid taxonomy. It has been a difficult journey at times, and I couldn’t have done it without those close to me. So, thank you to my Mum and Stu; you were a tower of support and were with me every step of the way. Thanks to my brother, Simon, for all your encouragement, and for putting a roof over my head when I worked in London! Many thanks to my Dad and Linda, Melanie and Andrew, you always believed in me. My friends, Clara and Lev, Fifi, and Nelia; you all kept my spirits high through good times and bad. Een grote “dank u wel”, Marijke and Ivan, for your care and support. A very special thank you goes to my fiancé, Jeroen, whose love and devotion made the completion of this thesis possible. You kept me focused and heading in the right direction at all times, and I truly appreciated the many discussions that helped me to find solutions in my own mind. Naar de maan en terug! Emily Dolan Contents V Contents Abstract III Acknowledgements IV List of Figures VIII List of Plates IX List of Tables XI Preface XII 1 General Background 1 1.1 Systematics of Octocorallia (Cnidaria: Anthozoa) and General Morphological Structure 1 1.1.1 Phylum Cnidaria 1 1.1.2 Class Anthozoa 2 1.1.3 Subclass Octocorallia 4 1.1.3.1 Classification and General Morphology of Octocorallia 4 1.1.3.2 Taxonomy and Systematics of Octocorallia 6 1.2 Order Pennatulacea 8 1.2.1 Biology of Pennatulacea 8 1.2.1.1 Gross Structure 8 1.2.1.2 The Polyps 10 1.2.2 Taxonomy and Systematics of Pennatulacea 12 2 Phylogeny and Systematics of Deep-Sea Pennatulacea (Anthozoa: Octocorallia): A molecular analysis based on mitochondrial protein- coding Sequences 14 2.1 Introduction 14 2.2 Material and Methods 19 2.2.1 Specimens 19 2.2.2 DNA Extraction 22 2.2.3 Primers, Amplification and Sequencing 22 2.2.3.1 Succinate Dehydrogenase and COI-COII Intergenic Spacer 22 2.2.3.2 16S rDNA 23 2.2.3.3 18S rDNA 24 2.2.3.4 ND2 and msh1 25 2.2.4 Sequence Analysis of ND2 and msh1 26 2.3 Results 27 2.3.1 PCR Optimisations and Primers 27 2.3.2 Sequences 29 2.3.3 Alignments 31 2.3.4 Outgroup 32 Emily Dolan Contents VI 2.3.5 Trees 32 2.4 Discussion 38 2.4.1 Phylogeny 38 2.4.2 Systematics and Classification 41 2.4.3 Conclusions 43 3 A Systematic Account of the genus Umbellula (Pennatulacea: Umbellulidae) 45 3.1 Introduction 45 3.2 Material and Methods 49 3.2.1 Specimens 49 3.2.2 Type Specimens and Literature 52 3.2.3 Sclerite Analysis 53 3.2.3.1 Light Microscope 53 3.2.3.2 Scanning Electron Microscope 53 3.2.4 Axis Analysis 55 3.2.5 Molecular Analysis 55 3.2.6 Geographic and Bathymetric Distribution 55 3.3 Results and Discussion 56 3.3.1 Glossary of Morphological and Anatomical Terms Applied to Pennatulacea 56 3.3.2 Key to the Fifteen species of Umbellula 57 3.3.3 Taxonomic Descriptions 59 3.3.3.1 Umbellula magniflora Kölliker 1880; Umbellula encrinus Linnaeus 1758; Umbellula antarctica Kükenthal and Broch 1911 59 3.3.3.2 Umbellula carpenteri Kölliker 1880 71 3.3.3.3 Umbellula sp.1 n. sp. 76 3.3.3.4 Umbellula pellucida Kükenthal 1902 80 3.3.3.5 Umbellula huxleyi Kölliker 1880 82 3.3.3.6 Umbellula spicata Kükenthal 1902 86 3.3.3.7 Umbellula thomsoni Kölliker 1874 87 3.3.3.8 Umbellula hemigymna Pasternak 1975 93 3.3.3.9 Umbellula monocephalus Pasternak 1964 99 3.3.3.10 Umbellula aciculifera J Stuart Thomson 1915 102 3.3.3.11 Umbellula durissima Kölliker 1880 108 3.3.3.12 Umbellula sp.2 n. sp. 112 3.3.3.13 Umbellula sp.3 n. sp. 115 3.3.4 A Note on Useful Morphological Characters for Umbellula Classification 119 3.3.5 Phylogenetic Analysis to Infer Systematic Relationships within Umbellula 122 3.3.6 Comments on Global Occurrence of Umbellula Species 126 3.4 Summary 135 4 Biogeography of the
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