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Biogeography and Phylogenetics of the Planktonic Foraminifera

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Biogeography and Phylogenetics of the Planktonic Foraminifera Biogeography and Phylogenetics of the Planktonic Foraminifera Heidi Seears, BSc, MSc Thesis submitted to the University of Nottingham for the degree of Doctor of Philosophy July 2011 Abstract The planktonic foraminifera are a highly abundant and diverse group of marine pelagic protists that are ubiquitously distributed throughout the worlds’ oceans. These unicellular eukaryotes are encased in a calcareous (CaCO3) shell or ‘test’, the morphology of which is used to identify individual ‘morphospecies’. The foraminifera have an exceptional fossil record, spanning over 180 million years, and as microfossils provide a highly successful paleoproxy for dating sedimentary rocks and archiving past climate. Molecular studies, using the small subunit (SSU) ribosomal (r) RNA gene are used here to investigate the biogeographical distributions and phylogenetic relationships of the planktonic foraminifera. Biogeographical surveys of two markedly different areas of the global ocean, the tropical Arabian Sea, and the transitional/sub-polar North Atlantic Ocean, revealed significant genotypic variation within the planktonic foraminifera, with some genetic types being sequenced here for the first time. The foraminiferal genotypes displayed non-random geographical distributions, suggestive of distinct ecologies, giving insight into the possible mechanisms of diversification in these marine organisms. The ecological segregation of genetically divergent but morphologically cryptic genetic types could, however, have serious repercussions on their use as paleoproxies of past climate change. Phylogenetic analyses of the foraminifera based firstly on a partial ~1,000 bp terminal 3´ fragment of the SSU rRNA gene, and secondly on the ~3,000 bp almost complete gene supported the hypothesis of the polyphyletic origins of the planktonic foraminifera, which appear to be derived from up to 5 separate benthic ancestral lineages. The almost complete gene is sequenced here in the planktonic taxa for the first time, though amplification was problematic. In a first step to addressing a pressing need for new genetic markers to support data gained from the SSU rRNA gene, a culture system was established for the benthic foraminifera, in order to provide a reliable source of DNA for EST library construction or full genome sequencing. Finally, to overcome difficulties associated with the PCR amplification of the foraminifera, a new lysis buffer and DNA extraction procedure was developed. A highly successful buffer was created, allowing high quality DNA to be extracted from foraminiferal specimens, whilst leaving the delicate calcitic shell intact for morphological reference. Acknowledgements I would like to thank my supervisor, Chris Wade, for all of his support and guidance during this project, and Kate Darling for her comments and advise. I would also like to thank the BBSRC for funding this work and NERC for providing additional financial support for the collection of specimens. I am grateful to everyone who participated in the collection of planktonic foraminiferal specimens, in particular Kate Darling and Blair Steel (cruise CD148: Arabian Sea) and Mathew Carroll (cruise CD159: North Atlantic Ocean) and would like to acknowledge the crew and scientists of the RRS Charles Darwin (cruises CD148 & CD159). I am also grateful to Professor John Murray (Southampton) for his assistance in the identification of the British intertidal foraminiferal species collected during this study. I would like to thank Don McNab and Carole East of the University of Nottingham Academic support unit. I also thank my lab mates, Ian Fontanilla, Cendrine Hudelot and Mathew Carroll for their friendship and assistance, and also Sheila Keeble for her invaluable technical support. To all of my friends, who have offered great support over the years, I am extremely grateful. In particular I would like to thank Rachel Clark. Finally, I owe special thanks to my family, without whose support I could never have completed my studies. Table of Contents 1 INTRODUCTION...................................................................................................... 1 1.1 THE FORAMINIFERA ............................................................................................................1 1.2 BIOLOGICAL CHARACTERISTICS OF THE FORAMINIFERA........................................4 1.2.1 Cellular structure .......................................................................................................4 1.2.2 Growth and Test Ontogeny........................................................................................5 1.2.3 Feeding and Nutrition ................................................................................................6 1.2.4 Symbiosis...................................................................................................................7 1.2.5 Life cycle in the Foraminifera....................................................................................9 1.3 BIOGEOGRAPHY AND ECOLOGY OF THE PLANKTONIC FORAMINIFERA ............13 1.4 THE USE OF PLANKTONIC FORAMINIFERA AS INDICATORS OF PAST ENVIRONMENTAL CONDITIONS AND CLIMATIC CHANGE......................................15 1.5 CLASSIFICATION OF THE FORAMINIFERA ...................................................................16 1.5.1 Criteria for the classification of the Foraminifera....................................................16 1.5.2 Current classification of the Foraminifera ...............................................................19 1.6 PHYLOGENETIC RELATIONSHIPS OF THE PLANKTONIC FORAMINIFERA ...........21 1.6.1 The origins of the Foraminifera: Molecular versus fossil evidence.........................22 1.6.2 The origins of the planktonic foraminifera: The move from benthos to plankton ...25 1.6.3 Evolutionary relationships within the planktonic foraminifera................................28 1.6.4 Cryptic Genetic Diversity Revealed ........................................................................30 1.7 SUMMARY OF THE AIMS OF THIS THESIS ....................................................................32 1.8 REFERENCES........................................................................................................................35 2 MATERIALS AND METHODS ............................................................................ 45 2.1 COLLECTION AND PREPARATION OF FORAMINIFERAL SPECIMENS....................45 2.1.1 Planktonic foraminiferal samples ............................................................................45 2.1.2 Benthic foraminiferal samples .................................................................................46 2.2 DNA AMPLIFICATION BY THE POLYMERASE CHAIN REACTION (PCR)................47 2.2.1 The small subunit ribosomal RNA gene..................................................................47 2.2.2 PCR primers.............................................................................................................48 2.2.3 PCR components .....................................................................................................52 2.2.4 PCR running conditions...........................................................................................53 2.3 GEL ELECTROPHORESIS....................................................................................................55 2.4 GEL EXTRACTION...............................................................................................................56 2.5 DNA QUANTIFICATION......................................................................................................57 2.6 CLONING...............................................................................................................................57 2.6.1 Selective agar plate preparation...............................................................................58 2.6.2 Setting up the TOPO TA Cloning® reaction (Invitrogen™) ....................................59 2.6.3 Transforming One Shot® TOP10 competent cells ...................................................59 2.6.4 Plasmid isolation......................................................................................................60 2.6.5 Cycle sequencing.....................................................................................................61 2.7 DNA SEQUENCE ANALYSIS..............................................................................................63 2.7.1 Assembly of the SSU rDNA sequences...................................................................63 2.7.2 Selecting nucleotide sites for phylogenetic analysis................................................63 2.7.3 Evaluating sequences for evidence of substitution saturation..................................64 2.8 PHYLOGENETIC ANALYSIS ..............................................................................................65 2.8.1 Choosing a model of sequence evolution using the likelihood ratio test (LRT)......65 2.8.2 Phylogenetic tree reconstruction..............................................................................66 2.8.3 Relative rate tests (RRT)..........................................................................................68 2.8.4 Hypothesis testing....................................................................................................69 2.9 REFERENCES........................................................................................................................71 3 GENOTYPIC VARIABILITY IN THE PLANKTONIC
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