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An Integrated View of Metazoan Evolution A AN INTEGRATED VIEW OF METAZOAN EVOLUTION A Dissertation Presented to The Graduate Faculty of The University of Akron In Partial Fulfillment Of the Requirements for the Degree Doctor of Philosophy Ashley Wain August, 2015 AN INTEGRATED VIEW OF METAZOAN EVOLUTION Ashley Wain Dissertation Approved: Accepted: ______________________________ ______________________________ Advisor Department Chair Dr. Francisco Moore Dr. Stephen Weeks ______________________________ ______________________________ Committee Member Dean of the College Dr. Richard Londraville Dr. Chand Midha ______________________________ ______________________________ Committee Member Interim Dean of the Graduate School Dr. Stephen Weeks Dr. Chand Midha ______________________________ ______________________________ Committee Member Date Dr. Joel Duff ______________________________ Committee Member Dr. Tom Leeper ______________________________ Committee Member Dr. Lisa Park ii ABSTRACT Complexity of organisms is ultimately dependent upon the number of cells present within an organism. Single-celled organisms are arguably the least complex of all living things with complexity increasing as cells are gained. The first major step in this process was achieving coloniality. The choanoflagellate species, Salpingoeca rosetta, used primarily in this study has a colonial life stage. Following that, organisms transitioned to true multicellularity with cell specialization being one of the requirements for that distinction. This transition, from colonial to multicellular animal life, is the topic of investigation in this dissertation. Multicellular animals evolved ~700 million years ago in the late Proterozoic, 1.4 billion years after the evolution of the eukaryotic cell. Investigations into the transition typically cite at least one of three major causes of the end to stasis in the animal lineage: Nursall’s “Oxygen Control Hypothesis”, the evolution of macrophagous predation, and changes in the chemical environment. Without direct fossilized evidence recorded and because the metazoan ancestor cannot be studied directly, a close relative, Salpingoeca rosetta was used in neontological tests of the roles of dissolved oxygen, predation, and the presence of serotonin, an ancient iii signaling molecule, in multicellular development. This is the first study to include long term experimental evolution of choanoflagellates to investigate the impacts of environment on the transition to multicellularity in animals. The combined evidence from the following studies indicates that the transition may have been brought about by a combination of the factors with a strong dependence on the common ancestor of unicellular and multicellular animals being pre-adapted for multicellular life. Genes for cell adhesion and intercellular communication are two of those pre-adaptations possessed by a close relative of the common ancestor, the choanoflagellates. Both were included in the following investigations and responded to experimental manipulation of environments to test the impacts of abiotic and ecological changes thought to have led to the evolution of multicellular animal. ACKNOWLEDGEMENTS I would like to thank Dr. Paco Moore for introducing me to choanoflagellates as a prospective master’s student and furthermore to the fascinating fields of micro- and macroevolution. I would also like to thank my committee members: Dr. Rich Londraville, Dr. Tom Leeper, Dr. Steve Weeks, Dr. Joel Duff, and Dr. Lisa Park for your time and input on this dissertation. Finally, I’d like to acknowledge my family, labmates, and friends who have supported me and who have been there for me, especially Dr. Lara Roketenetz, Dr. Hope Ball, Ashley Ramer, Ethan Knapp, and Scott Thomas who have been there to listen as well as to assist on projects. v TABLE OF CONTENTS Page LIST OF TABLES ........................................................................................................... viii LIST OF FIGURES .............................................................................................................x CHAPTER I. INTRODUCTION ...........................................................................................................1 II. LONG TERM EXPERIMENTAL EVOLUTION OF SALPINGOECA ROSETTA IN ENVIRONMENTS SIMULATING THAT OF THE LATE PROTEROZOIC: MORPHOLOGICAL RESPONSE: AN INTEGRATIVE STUDY ...............................16 Introduction ............................................................................................................16 Materials and Methods ...........................................................................................20 Results ....................................................................................................................25 Discussion ..............................................................................................................29 III. PREDATOR MEDIATED ADAPTIVE ASSIMILATION OF A PLASTIC MORPHOLOGICAL RESPONSE TO PREDATION IN THE CHOANOFLAGELLATE SALPINGOECA ROSETTA ..................................................37 Introduction ............................................................................................................37 Materials and Methods ...........................................................................................41 Results ....................................................................................................................47 Discussion ..............................................................................................................52 vi IV. MORPHOLOGICAL RESPONSE OF SALPINGOECA ROSETTA TO THE PRESENCE OF 5-HYDROXYTRYPTAMINE (SEROTONIN) ...................................57 Introduction ............................................................................................................57 Materials and Methods ...........................................................................................60 Results ....................................................................................................................62 Discussion ..............................................................................................................73 V. CONCLUSION ............................................................................................................82 REFERENCES ..................................................................................................................88 APPENDICES ...................................................................................................................99 Appendix A ..........................................................................................................100 Appendix B ..........................................................................................................115 Appendix C ..........................................................................................................129 Appendix D ..........................................................................................................143 Appendix E ..........................................................................................................144 Appendix F...........................................................................................................145 Appendix G ..........................................................................................................158 vii LIST OF TABLES Table Page 2.1 Average Colony Size of Source and Evolved Salpingoeca rosetta .......................26 2.2 Two-Way Nested ANOVA for the Effects of Dissolved Oxygen and Predation on Colony size ................................................................................27 2.3 Average Cell Density (Cells/50nL) of Source and Evolved Salpingoeca rosetta ................................................................................................28 3.1 Contingency of Expected Phenotypic States .........................................................44 3.2 Morphological Response to Treatment by Lineages .............................................50 3.3 Two-Way ANOVA for Cell Density .....................................................................52 4.1 Average Colony Frequencies of All Treatment Groups ........................................64 4.2 Two-Way ANOVA for S. rosetta Colony Frequency Due to Evolutionary Environment and Algoriphagus machipongonensis ..............................................64 4.3 Average Cell Density of Col- Lineages of Salpingoeca rosetta ............................65 4.4 Two-Way ANOVA for S. rosetta (Col-) Cell Density (Cells/μL) .........................66 4.5 Average Colony Frequency (%) of Col- Lineages of Salpingoeca rosetta. ..........66 4.6 Two-Way ANOVA for S. rosetta (Col-) Colony Frequency Due to Evolutionary and Ecological Environments ..........................................................67 4.7 Average Colony Size (Cells/Colony) of Col- Lineages of Salpingoeca rosetta ................................................................................................68 4.8 Two-Way ANOVA for S. rosetta (Col-) Colony Size Due to Evolutionary and Ecological Environments. ......................................................................................69 viii 4.9 Average Cell Density of Col+ Lineages of Salpingoeca rosetta ...........................70 4.10 Two-Way ANOVA for S. rosetta (Col+) Cell Density (Cells/μL) Due to Evolutionary and Ecological Environments ..........................................................70 4.11 Average
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