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Evolution of Photosymbiosis in Marine Bivalves (Cardiidae: Fraginae)

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Evolution of Photosymbiosis in Marine Bivalves (Cardiidae: Fraginae) EVOLUTION OF PHOTOSYMBIOSIS IN MARINE BIVALVES (CARDIIDAE: FRAGINAE) By LISA ANN KIRKENDALE 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 2005 Copyright 2005 by Lisa Ann Kirkendale This document is dedicated to my grandfather, the late John Kirkendale. ACKNOWLEDGMENTS I would like to thank the staff, faculty and graduate students in the Department of Zoology and the Florida Museum of Natural History at the University of Florida for their support and advice. My committee and especially my advisor Gustav Paulay were very helpful at all stages of my doctoral research. The study would not have been possible without funding provided from a number of sources including Lerner Gray Fund for Marine Research, Sigma Xi Grants in Aid of Research, Astronaut Trail Shell Club, Western Society of Malacologists and Conchologists of America. I would also like to mention the Paris Museum of Natural History for an opportunity to work at that institution. My family has offered immense emotional (not to mention financial) support through the years. I am grateful to Peter Middelfart for his love and understanding. iv TABLE OF CONTENTS page ACKNOWLEDGMENTS ................................................................................................. iv LIST OF TABLES........................................................................................................... viii LIST OF FIGURES ........................................................................................................... ix ABSTRACT....................................................................................................................... xi CHAPTER 1 GENERAL INTRODUCTION....................................................................................1 2 MOLECULAR PHYLOGENETICS..........................................................................10 Introduction.................................................................................................................10 Higher-Level Systematics of the Cardioidea and Cardiidae ...............................13 Fraginae Monophyly ...........................................................................................15 Parvicardium and Papillicardium: Sister to all other Fragines?.........................16 The “Trigoniocardia” and “Ctenocardia” groups...............................................19 Known Photosymbiotic Representatives: Fragum, Lunulicardia and Corculum..........................................................................................................20 Materials and Methods ...............................................................................................24 Specimen Acquisition..........................................................................................24 DNA Extraction and PCR ...................................................................................24 Alignment & Molecular Analyses.......................................................................27 Results.........................................................................................................................29 General Findings- Sequence Data .......................................................................29 General Findings- Phylogenetic Methods ...........................................................29 Higher-Level Phylogenetic Findings...................................................................30 Fraginae Monophyly ...........................................................................................31 The Genus Parvicardium sensu lato: Clades I and IV .......................................35 The “Ctenocardia” and “Trigoniocardia” groups: Clade II..............................35 Fragum, Lunulicardia and Corculum: Clade III ................................................36 Species’ Boundaries in IWP Corculum, Lunulicardia and Fragum ...................36 Discussion...................................................................................................................39 Monophyly of the Cardiid Subfamily Fraginae?.................................................39 The Early Diverging Fragine genus Parvicardium: Clades I and IV.................41 The “Ctenocardia” and “Trigoniocardia” groups: Clade II..............................43 v Relationships among the IWP genera Fragum, Corculum and Lunulicardia: Clade III ...........................................................................................................44 3 CHARACTER TRAIT EVOLUTION .......................................................................49 Introduction.................................................................................................................49 Materials and Methods ...............................................................................................56 Specimen Acquisition..........................................................................................56 Determination of Photosymbiotic Condition.......................................................56 Morphological Character Trait Analyses ............................................................58 Character Data.....................................................................................................58 Windows.......................................................................................................58 Maximum observed adult size......................................................................61 Habitat ..........................................................................................................62 Shell measurements......................................................................................64 Character Trait Evolution....................................................................................66 Results.........................................................................................................................66 Photosymbiotic Status .........................................................................................66 Character Trait States ..........................................................................................67 Windows.......................................................................................................67 Maximum observed adult size......................................................................67 Habitat ..........................................................................................................69 Shell measurements......................................................................................70 Character Trait Evolution....................................................................................74 Windows.......................................................................................................77 Maximum observed adult size......................................................................78 Habitat ..........................................................................................................81 Shell measurements......................................................................................84 Discussion...................................................................................................................89 Photosymbiotic Status .........................................................................................89 Character Trait Analyses and Evolution..............................................................89 Windows.......................................................................................................89 Maximum observed adult size......................................................................90 Habitat ..........................................................................................................91 Shell measurements......................................................................................91 4 GLOBAL DISCUSSION............................................................................................94 Molecular phylogenetics.............................................................................................94 Character trait evolution .............................................................................................97 APPENDIX A NUMBER OF INDIVIDUALS EXAMINED FOR SCORED CHARACTERS OF FRAGINAE ..............................................................................................................101 vi B PHOTOSYMBIOTIC STATUS, MORPHOMETRIC AND HABITAT DATA FOR MEASURED CHARACTERS ........................................................................103 C RAW LOGGED DATA FOR 95% CONFIDENCE INTERVAL PLOTS OF KEEL ANGLE, POSTERIOR SHELL FLATTENING AND LINEARIZED SURFACE AREA TO VOLUME RATIOS.............................................................105 LIST OF REFERENCES.................................................................................................107 BIOGRAPHICAL SKETCH ...........................................................................................118 vii LIST OF TABLES Table page 2-1 Membership in the subfamily Fraginae....................................................................16 2-2 Species and distribution of recognized Fraginae......................................................18 2-3 Sampling localities and voucher information for a subset of Fraginae....................25 2-4 Primers used for
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