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Bivalvia: Cardiidae) Nathanael D Florida State University Libraries Electronic Theses, Treatises and Dissertations The Graduate School 2013 Molecular Phylogenetics and Historical Biogeography of Cockles and Giant Clams (Bivalvia: Cardiidae) Nathanael D. Herrera Follow this and additional works at the FSU Digital Library. For more information, please contact [email protected] THE FLORIDA STATE UNIVERSITY COLLEGE OF ARTS AND SCIENCES MOLECULAR PHYLOGENETICS AND HISTORICAL BIOGEOGRAPHY OF COCKLES AND GIANT CLAMS (BIVALVIA: CARDIIDAE) By NATHANAEL D HERRERA A Thesis submitted to the Department of Biological Science in partial fulfillment of the requirements for the degree of Master of Science Degree Awarded: Summer Semester, 2013 Nathanael D. Herrera defended this thesis on June 18, 2013. The members of the supervisory committee were: Scott Steppan Professor Directing Thesis Don Levitan Committee Member Austin Mast Committee Member The Graduate School has verified and approved the above-named committee members, and certifies that the thesis has been approved in accordance with university requirements. ii ACKNOWLEDGMENTS I would like to thank my advisor, Dr. Scott Steppan, whose support, guidance, and invaluable expertise made it possible for me to do this research. I would also like to thank my committee members, Dr. Don Levitan and Dr. Austin Mast, whose patience and helpful criticisms were essential to this work. In addition, I am thankful to Dr. John Schenk and Mr. Kenny Wray for providing stimulating discussion, advice, and encouragement while being at FSU. I would also like to thank my fellow colleagues working on the Bivalves in Time and Space project (BiTS), Jan Johan ter Poorten, Rüdiger Bieler, John Hulsenbeck, Nick Matzke, David Jablonski, Paula Mikkelsen, Rafael Robles, and André Sartori, who not only helped make this research possible but taught me an immense amount about bivalves. iii TABLE OF CONTENTS List of Tables...................................................................................................................................v List of Figures ................................................................................................................................vi Abstract .........................................................................................................................................vii 1. MOLECULAR PHYLOGENETICS AND BIOGEOGRAPHY OF COCKLES AND GIANT CLAMS (BIVALVIA: CARDIIDAE) ......................................................................1 2. HISTORICAL BIOGEOGRAPHY OF A MARINE BIVALVE (BIVALVIA: CARDIIDAE): GLOBAL PATTERNS OF ORIGINATION AND DISPERSAL ..............25 APPENDICES...............................................................................................................................44 A.1 SAMPLING AND VOUCHER INFORMATION FOR THE CARDIIDAE USED IN THIS STUDY..........................................................................................................................................44 B.1 CARDIID SEQUENCES INCORPORATED INTO THIS STUDY FROM GENBANK. .50 REFERENCES..............................................................................................................................54 BIOGRAPHICAL SKETCH.........................................................................................................61 iv LIST OF TABLES 1.1 Primers used in this study..................................................................................................16 1.2 Results of the Bayesian inference analysis by gene, the number of generations the chains were run, the number of generations discarded as the burn-in period, and the split frequencies of each run......................................................................................................17 2.1 Fossil calibrations used in the BEAST analysis................................................................33 2.2 Clade ages estimated by BEAST for 14 focal nodes with upper and lower 95% highest posterior density. ...............................................................................................................34 A.1 Sampling and voucher information for Cardiidae representatives used in this study. ......44 B.1 Cardiid sequences incorporated into this study from Genbank.........................................50 v LIST OF FIGURES 1.1 Phylogenetic relationship of the Cardiidae based on shell morphology and microstructure. Redrawn from Schneider and Carter (2001), Schneider (2002). Crosses indicate extinct taxa...........................................................................................................17 1.2 Biogeographic regions used in this study of the Cardiidae ...............................................18 1.3 16S Maximum-likelihood phylogram. ..............................................................................19 1.4 28S Maximum-likelihood phylogram. ..............................................................................21 1.5 Histone 3 Maximum-likelihood phylogram. .....................................................................22 1.6 Maximum-likelihood phylogram of concatenated dataset for three genes (His 3, 16S, 28S). ..............................................................................................................23 1.7 Biogeographic reconstruction cladogram. ........................................................................24 2.1 Biogeographic regions used in this study of the Cardiidae ...............................................35 2.2 Paleogeographical model used in the Cardiidae analysis..................................................46 2.3 Chronogram of Cardiidae produced from the BEAST analysis........................................39 2.4 Biogeographical reconstruction of ancestral ranges in the Cardiidae ...............................41 vi ABSTRACT This study produces a nearly comprehensive large-scale molecular phylogeny for the marine bivalve family Cardiidae (cockles and giant clams) and uses this topology to examine patterns of diversification in the marine realm. This study uses maximum-likelihood and Bayesian phylogenetic analyses of two nuclear (Histone 3, 28S) and one mitochondrial (16S) gene for 110 species representing 37 of the 44 recognized genera and all eight extant subfamilies. Lineage divergence times were estimated using Bayesian estimation with uncorrelated relaxed rates among lineages (BEAST). To reconstruct ancestral geographic ranges, I used the dispersal- extinction-clodegenesis method (Lagrange) with a stratified paleogeographic model in which dispersal rates were scaled according to area connectivity across three time slices. The resulting topologies are discussed with respect to traditional subfamilial classifications, and previous anatomical and molecular findings. I confirm the monophyly of two subfamilies, Tridacninae and Clinocardiinae as previously defined, but found there to be rampant paraphyly/ polyphyly of the other six subfamilies. The Cardiidae seem to have originated in the tropical Indo-Pacific some time in the early Cretaceous and diversified within the tropical Pacific. The extant diversity seen in the Atlantic is derived from species that dispersed from the tropical Indo-Mediterranean region during the Cenozoic via the Tethys sea. vii CHAPTER ONE MOLECULAR PHYLOGENETICS AND BIOGEOGRAPHY OF COCKLES AND GIANT CLAMS (BIVALVIA: CARDIIDAE) Introduction The bivalve family Cardiidae (Cockles and Giant clams) comprises about 250 extant species arranged in ca. 80 genera and eight subfamilies with the oldest fossil representative (Tulongicardiinae) dating back to the Norian (ca. 216 mya) (Lydeard and Lindberg 2003, Ponder and Lindberg 2008). Cardiids inhabit tropical to polar seas worldwide with the bulk of extant taxa distributed throughout tropical-subtropical seas. They are mainly shallowly infaunal to epifaunal in soft sand or mud in water depths up to 500 m. Typically, cardiids are suspensions feeders, but some are highly specialized, such as Tridacna, Corculum, and Fraginae, which form an endosymbiosis with dinoflagellate protists (Maruyama et al. 1998, Schneider 1998b, Kirkendale 2009). The majority of our taxonomic understanding is based upon gross morphological features of the shell and some soft anatomy (Keen 1969, Kafanov 1980, Keen 1980, Voskuil and Onverwagt 1991a, b, Schneider 1992, Vidal 1999, 2000, Schneider 2002, Savazzi and Salgeback 2004), shell microstructure (Carter and Schneider 1997, Schneider and Carter 2001), or phylogenetic studies combining these characters (Schneider 1995, 1998a, b, Nevesskaja et al. 2001, Schneider 2002). However, studies incorporating molecular data are few and restricted to few taxa (Maruyama et al. 1998, Schneider and Foighil 1999, Nikula and Vainola 2003, DeBoer et al. 2008, Kirkendale 2009). Despite the attention the family has received, the phylogeny of the family remains poorly understood, and its classification is still largely based on gross shell morphology and soft anatomy. The classification of cardiids remains incomplete, especially regarding the subfamilial and generic ranking of many groups. Stewart (1930) divided the family Cardiidae into three subfamilies based on shell morphology (Cardiinae, Trachycardiinae, and Fraginae). Kafanov and Popov’s (1977) treatment of Cardiidae divided the family into six subfamilies (Cardiinae, Clinocardiinae, Fraginae, Hemidonacinae, Protocardiinae, and Lymnocardiinae). Keen (1980), who was skeptical of Kafanov and Popov’s (1977) classification because it rested on a single character
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