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Evolution and Development of Cetacean Appendages Across the Cetartiodactylan Land-To-Sea Transition

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Evolution and Development of Cetacean Appendages Across the Cetartiodactylan Land-To-Sea Transition EVOLUTION AND DEVELOPMENT OF CETACEAN APPENDAGES A dissertation submitted to Kent State University in partial fulfillment of the requirements for the degree of Doctor of Philosophy by Lisa Noelle Cooper December, 2009 Dissertation written by Lisa Noelle Cooper B.S., Montana State University, 1999 M.S., San Diego State University, 2004 Ph.D., Kent State University, 2009 Approved by _____________________________________, Chair, Doctoral Dissertation Committee J.G.M. Thewissen _____________________________________, Members, Doctoral Dissertation Committee Walter E. Horton, Jr. _____________________________________, Christopher Vinyard _____________________________________, Jeff Wenstrup Accepted by _____________________________________, Director, School of Biomedical Sciences Robert V. Dorman _____________________________________, Dean, College of Arts and Sciences Timothy Moerland ii TABLE OF CONTENTS LIST OF FIGURES ........................................................................................................................... v LIST OF TABLELS ......................................................................................................................... vii ACKNOWLEDGEMENTS .............................................................................................................. viii Chapters Page I INTRODUCTION ................................................................................................................ 1 The Eocene Raoellid Indohyus ......................................................................................... 2 Cortical Bone Evolution in Cetartiodactylans .................................................................. 5 The Apical Ectodermal Ridge .......................................................................................... 6 Hyperphalangy ................................................................................................................. 8 The Soft Tissue Flipper ..................................................................................................... 9 II MORPHOLOGY AND LOCOMOTION OF THE MIDDLE EOCENE RAOELLID INDOHYUS (ARTIODACTYLA: MAMMALIA) .................................................................... 11 Introduction ................................................................................................................... 11 Materials and Methods .................................................................................................. 15 Results ............................................................................................................................ 16 Discussion ...................................................................................................................... 47 III EVOLUTION OF BONE MICROSTRUCTURE DURING THE AQUATIC INVASION OF CETARTIODACTYLA (MAMMALIA) ........................................................... 63 Introduction ................................................................................................................... 63 Materials and Methods .................................................................................................. 69 Results ............................................................................................................................ 77 Discussion ...................................................................................................................... 88 IV EVOLUTION OF THE APICAL ECTODERM IN THE DEVELOPING VERTEBRATE LIMB ....... 95 Introduction ................................................................................................................... 95 Materials and Methods ................................................................................................ 105 Results .......................................................................................................................... 106 Discussion .................................................................................................................... 114 iii TABLE OF CONTENTS (Continued) CHAPTER Page V DEVELOPMENT OF DOLPHIN FLIPPERS: MOLECULAR EVOLUTION OF HYPERPHALANGY AND INTERDIGITAL WEBBING ........................................................ 119 Abstract ........................................................................................................................ 119 Introduction ................................................................................................................. 120 Materials and Methods ................................................................................................ 123 Results .......................................................................................................................... 124 Discussion .................................................................................................................... 130 VI REVIEW OF THE EVOLUTION AND DEVELOPMENT OF CETACEAN APPENDAGES ....... 135 Developmental Processes ............................................................................................ 135 Form and Function ...................................................................................................... 138 Performance ................................................................................................................ 144 Environment ................................................................................................................ 146 Biological Role ............................................................................................................. 147 REFERENCES .............................................................................................................................. 148 APPENDIX: CATALOGUE OF INDOHYUS POSTCRANIAL ELEMENTS FROM THE A. RANGA RAO COLLECTION USED IN THIS ANALYSIS ............................................................ 181 iv LIST OF FIGURES Figure Page 1 Reconstruction of Indohyus ............................................................................................. 3 2 A block of sediment showing several disarticulated bones of Indohyus ......................... 4 3 Hyperphalangy in modern cetaceans .............................................................................. 8 4 Skeletal reconstruction of Indohyus .............................................................................. 13 5 Ribs and vertebrae of Indohyus ..................................................................................... 17 6 Vertebrae of Indohyus ................................................................................................... 22 7 Forelimb elements of Indohyus ..................................................................................... 26 8 The manus and pes of Indohyus .................................................................................... 31 9 Pelvic limb elements of Indohyus .................................................................................. 36 10 Tarsal elements of Indohyus .......................................................................................... 42 11 Phalangeal cross-sections in Indohyus, pakicetids, and Ambulocetus natans............... 56 12 Bone cross-sectional geometries in Indohyus compared to terrestrial artiodactyls with an equivalent body size (Tragulus and Hyemoschus) ....................... 59 13 Mathematial model that calculates amount of bone as a function of the distance to the center of the bone ................................................................................ 75 14 Radiographs through long bone midshafts of cetartiodactylans .................................. 78 15 Radiographs through long bone midshafts of fossil cetaceans from the archaeocete Family Remingtonocetidae ....................................................................... 79 16 Double logarithmic plots of P (a measure of bone thickness) ....................................... 81 17 Phylogenetic tree showing an ancestral character state reconstruction by squaredchange parsimony in fossil and extant cetartiodactylans ............................ 84 v LIST OF FIGURES (Continued) Figure Page 18 A graphical summary of P-values calculated in this analysis ......................................... 86 19 Schematics of apical ectodermal (AE) morphologies .................................................... 98 20 Morphology of an approximately 110 day old (Carnegie Stage 23) pantropical spotted dolphin (Stenella attenuata, LACM 94285) ................................. 103 21 Schematic of the transition from an apical ectodermal ridge (AE-1) to a finfold in the killifish (Aphyosemion scheeli, modified from Wood, 1982) ............................. 107 22 Apical ectodermal morphologies associated protein signals in the forelimbs of dolphins ................................................................................................................... 111 23 Forelimb development in embryos of the dolphin Stenella attenuate ....................... 121 24 Fibroblast growth factor (Fgf) protein signals in the developing forelimb of Stenella embryos and a fetus. ................................................................................. 125 25 Wingless type 9a (Wnt-9a) protein signals in the developing forelimb of Stenella embryos ......................................................................................................... 126 26 Gremlin and bone morphogenic protein (Bmp) signals in the developing forelimb of Stenella embryos
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