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THE SYSTEMATICS OF PORTUNOIDEA RAFINESQUE, 1815, AND THE EVOLUTION OF SYMBIOTIC SWIMMING CRABS By NATHANIEL MICHAEL EVANS 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 2016 © 2016 Nathaniel Michael Evans To my wife, Alice Catches ACKNOWLEDGMENTS I would like to thank all those who made this work possible, especially my advisor Gustav Paulay and everyone in the Division of Invertebrate Zoology at the Florida Museum of Natural History. I thank my committee for their guidance as this research progressed. I thank Rafael Lemaitre, Chris Meyer, Karen Reed, Rob Lasley, and Matt Leray for helping me successfully navigate the Smithsionian. I thank C. Gloor and C. Pitmann. This research was partially supported by the FLMNH McGinty Fund, the National Science Foundation (grant number 1406368), the Crustacean Society, and the Smithsonian Peter Buck Fellowship program. Finally, I thank my friends, family and wife for their continued support and encouragement over the years. 4 TABLE OF CONTENTS page ACKNOWLEDGMENTS .................................................................................................. 4 LIST OF TABLES ............................................................................................................ 6 LIST OF FIGURES .......................................................................................................... 7 ABSTRACT ................................................................................................................... 10 CHAPTER 1 INTRODUCTION .................................................................................................... 12 2 MOLECULAR PHYLOGENETICS OF SWIMMING CRABS (PORTUNOIDEA) SUPPORTS A REVISED CLASSIFICATION AND REVEALS A COMPLEX, DERIVED ORIGIN OF SYMBIOSIS........................................................................ 15 Introduction ............................................................................................................. 15 Materials and Methods............................................................................................ 19 Results and Discussion........................................................................................... 24 Systematic Account ................................................................................................ 42 3 A REVIEW AND MOLECULAR ANALYSIS OF THE SYMBIOTIC GENUS LISSOCARCINUS (PORTUNIDAE: THALAMITINAE) ............................................ 97 Introduction ............................................................................................................. 97 Materials and Methods............................................................................................ 98 Results and Discussion......................................................................................... 100 Systematic Account .............................................................................................. 103 Key to species of Lissocarcinus. ........................................................................... 123 4 MORPHOLOGICAL DISPARITY IN CARAPACE SHAPE AND THE EMERGENCE OF SYMBIOTIC SWIMMING CRABS (PORTUNIDAE) ................ 142 Introduction ........................................................................................................... 142 Materials and Methods.......................................................................................... 143 Results and Discussion......................................................................................... 145 5 SUMMARY AND FUTURE DIRECTIONS ............................................................ 178 Summary .............................................................................................................. 178 Future Directions .................................................................................................. 179 LIST OF REFERENCES ............................................................................................. 182 BIOGRAPHICAL SKETCH .......................................................................................... 195 5 LIST OF TABLES Table page 2-1 Taxon sampling and operational taxonomic unit (OTU) composition of sequence data used for phylogenetic analyses. ................................................. 56 2-2 Primer pairs, annealing temperatures and resulting fragment sizes for PCR reactions. ............................................................................................................ 78 2-3 Composition of eight molecular datasets constructed for phylogenetic analyses. ............................................................................................................ 79 2-4 Best scoring partition schemes for three concatenated molecular datasets. ...... 80 2-5 Best scoring partition schemes for four single marker molecular datasets. ........ 81 3-1 Taxon sampling and operational taxonomic unit (OTU) composition of sequence data used for phylogenetic analyses. ............................................... 126 3-2 Best scoring partition schemes for the concatenated molecular dataset. ......... 128 3-3 Kimura 2-parameter (K2P) genetic distances for 658 bps of mtDNA CO1 sequence data from 10 distinct Lissocarcinus lineages. ................................... 129 3-4 Genetic diversity indices for Lissocarcinus orbicularis based on 568 bps of CO1. ................................................................................................................. 130 3-5 Population pairwise FST values. ...................................................................... 130 3-6 Summary of distinguishing features in Lissocarcinus laevis s.l. species .......... 131 4-1 Taxon sampling for molecular and geometric morphometric (GMM) analyses. 148 4-2 Best scoring partition schemes for the concatenated molecular dataset .......... 155 4-3 Vouchered specimens used for geometric morphometric analyses (GMM) ..... 156 6 LIST OF FIGURES Figure page 2-1 Representatives of various Portunoidea clades included in this study. .............. 82 2-2 Representative non-symbiotic species from Thalamitinae. ................................. 83 2-3 Representative symbiotic species from Thalamitinae. ........................................ 84 2-4 Summary of major recent changes to the classification of Portunoidea and a new proposed scheme. ...................................................................................... 85 2-5 ML phylograms of Portunoidea based on analyses of single marker datasets of mitochondrial 16S rRNA and CO1.. ................................................................ 86 2-6 ML phylograms of Portunoidea based on analyses of single marker datasets of nuclear 28S rRNA and H3. ............................................................................. 87 2-7 ML phylogram of Portunoidea based on analyses of 174 OTUs and a 3313 bp alignment of partial 16S rRNA, CO1, 28S rRNA, and H3 sequence data. ..... 88 2-8 ML phylograms of Portunoidea based on analyses of 163 and 138 OTUs and a 3313 bp alignment of 16S rRNA, CO1, 28S rRNA, and H3 sequence data. .... 89 2-9 Subsections of ML and BI topologies for Portunoidea based on analyses of 174 and 138 OTUs and a 3313 bp alignment of 16S rRNA, CO1, 28S rRNA, and H3 sequence data.. ..................................................................................... 92 2-10 ML phylogram of Brusinia profunda and 308 mostly brachyuran taxa based on analyses of a 447 bp alignment of 16S rRNA sequence data........................ 93 2-11 A selection of morphological features discussed in the Systematic Account. ..... 96 3-1 ML phylogram of 10 Lissocarcinus and 16 outgroup taxa based on analyses of 2484 bps of partial 16S rRNA, CO1, 12S rRNA, and H3 sequence data. ..... 132 3-2 NJ topology (K2P model) of 657 bps of CO1 sequence data from 85 Lissocarcinus specimens. Bootstrap support values are based on 500 replicates; values greater than 50% are displayed. .......................................... 133 3-3 Lissocarcinus orbicularis and L. holothuricola CO1 (568 bps) haplotype diversity and distribution. .................................................................................. 134 3-4 Holotype and original illustration of Caphyra elegans (Boone, 1934). .............. 135 3-5 Morphology and live color of Lissocarcinus arkati Kemp, 1923, and original illustrations of type material for L. arkati and L. echinodisci Derijard, 1968. ..... 136 7 3-6 Holotype and additional material of Lissocarcinus holothuricola (Streets, 1877). ............................................................................................................... 137 3-7 Illustration, morphology and live color of Lissocarcinus laevis Miers, 1886, s.s. and L. aff. laevis sp. nov. C. ....................................................................... 138 3-8 Morphology and live color of Lissocarcinus aff. laevis sp. nov. A and L. aff. laevis sp. nov. B. .............................................................................................. 139 3-9 Syntype and additional material and illustrations of Lissocarcinus orbicularis Dana, 1852. ...................................................................................................... 140 3-10 Holotype illustration and additional material of Lissocarcinus polybioides Adams & White, 1849, species complex. ........................................................
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