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Molecular Phylogeny of the Freshwater Mussel Family Dreissenidae

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Molecular Phylogeny of the Freshwater Mussel Family Dreissenidae MOLECULAR PHYLOGENY OF THE FRESHWATER MUSSEL FAMILY DREISSENIDAE A Thesis By SUSAN ROSE GEDA Submitted to the Graduate School At Appalachian State University In partial fulfillment of the requirements for the degree of MASTER OF SCIENCE May 2017 Department of Biology i MOLECULAR PHYLOGENY OF THE FRESHWATER MUSSEL FAMILY DREISSENIDAE A Thesis By SUSAN ROSE GEDA APPROVED BY: ___________________________________ Michael M. Gangloff, Ph.D. Chairperson, Thesis Committee ___________________________________ Matt C. Estep, Ph.D. Member, Thesis Committee ___________________________________ Lynn Siefferman, Ph.D. Member, Thesis Committee ___________________________________ Zack E. Murrell, Ph.D. Chairperson, Department of Biology ___________________________________ Max Poole, Ph.D. Dean, Cratis D. Williams School of Graduate Studies ii Copyright by Susan Rose Geda 2017 All Rights Reserved iii Abstract MOLECULAR PHYLOGENY OF THE FRESHWATER BIVALVE FAMILY DREISSENIDAE Susan R. Geda B.S., Appalachian State University M.S., Appalachian State University Chairperson: Dr. Michael Gangloff The bivalve family Dreissenidae contains some of the most economically and ecologically important fresh and brackish-water mollusk species, including a number of problematic invaders. There has been much uncertainty surrounding phylogenetic resolution for members of Dreissenidae. The lineage is believed to have originated 83.6 million years ago in the Tethys and Paratethys seas. Three extant dreissenid genera are currently recognized, Dreissena, Mytilopsis, and Congeria. However, in 2012, an un-described mussel was discovered in the Xingu River, a tributary of the Amazon River in central Brazil. Sympatrically-occurring Congeria species have also been recently described from the region. The objective of this study was to determine the evolutionary history of the unknown South American dreissenids (USADs) and determine their proper taxonomic placement. I examined phylogenetic relationships among 10 described species within Dreissenidae and 6 related outgroups using nuclear and mitochondrial genes, a molecular clock analysis and a comparative analysis of life history characteristics to determine the evolutionary history of these enigmatic bivalves. Recent analyses suggest that these bivalves iv may comprise a distinct genus within Dreissenidae containing three species. My analyses support this hypothesis and revealed that the common ancestors of today’s USADs first diverged as a distinct lineage ~27.1 MYA. Due to phylogenetic analyses, genetic distance, and life history characteristics I believe USADs are sister taxa to Congeria and may have dispersed to South America on large scale ocean currents during the early Miocene. v Acknowledgements First and foremost, I would like to thank my advisor, Dr. Michael Gangloff. This project would not have been possible without your leadership and advice. You offered me so many research opportunities that created an extremely fulfilling graduate career for me. You pushed me enough so that I realized my potential and I would not be here without your support! I would also like to thank the members of my committee, Dr. Matt Estep and Dr. Sarah Marshburn, for their guidance, ideas, and edits to this thesis. This project would still be in progress without your insight. To all of the members of the ACRL lab, thank you for keeping me sane and making me laugh when I needed it the most. Daniel Mason, thank you for being my friend in the trenches and for being a sounding board for me to bounce my, sometimes terrible, ideas off of. Your perspective helped shape what this project is today. Michael Perkins and Raquel Fagundo, thank you both for being amazing resources for me during my analyses, for always answering the phone and talking me through the next steps, and making me laugh when I was almost ready to cry. I would also like to thank all of my collaborators. Specifically, Mark Sabaj- Perez, I would not have been able to travel to Brazil without your generous invitation. Thiago Mahlmann and Rafaela Ota at the Instituto Nacional de Pequisas da vi Amazonia and Leandro Sousa and Andre Ferriera from the Universidade Federal do Pará, thank you all for your help and hospitality regarding museum collections and field work. Nathan Lujan, thank you for sending me preliminary specimens and for involvement in previous publications. I would also like to thank Lynn Siefferman for support and many amazing dinners at the Gangloff-Siefferman household. Finally, I would like to thank my parents, Mark and Linda Geda, for their indefatigable support. They instilled in me my passion for nature, as well as my work ethic and my pride in that work. Thank you for the mindset that whatever I do is good enough, as long as I give it my all. vii Table of Contents Abstract…………………………………………………………………………………..….iv Acknowledgements…………………………………………………………………………vi List of Tables…………………………………………………………………………………x List of Figures……………………………………………………………………………….xi Foreword…………………………………………………………………………………….xii 1. Introduction………………………………….…………………………………………….1 1.1 Evolutionary History of Dreissenidae…………………………………………1 1.2 Dreissenid Biology……………………………………………………………...3 1.3 Study Sites…………………………………………………………………...….4 2. Methods…………………………………………………………………………………...6 2.1 Tissue Collection and DNA Extraction………………………………………..6 2.2 PCR Amplification………………………………………………………………7 2.3 Sequence Analyses…………………………………………………………….8 2.4 Phylogenetic Analyses…………………………………………………………9 2.5 Divergence Estimates………………………………………………………...10 3. Results………………………………………………………………………………...…11 3.1 Phylogenetic Analyses………………………………………………..………11 3.2 Genetic Diversity of USADs………………………………………………….13 3.3 Divergence Estimates………………………………………………………...15 viii 4. Discussion……………………………………………………………………………….15 4.1 Phylogenetic Analyses………………………………………………………..15 4.2 Genetic Diversity of USADs……………………………...…………………..17 4.3 Incongruent topologies………………….…………………………………….18 4.4 Divergence Estimates…………………………………………………...……23 4.5 Phylogeography and dispersal………………………………………………24 4.6 Comparative Analysis and Invasive Potential……………………………...28 References…………………………………………………………………………………30 Tables and Figures………………………………………………………………………..38 Appendix 1…………………………………………………………………………..……..72 Vita…………………………………………………………………………………………..75 ix List of Tables Table 1. Xingu Specimen Data…………………………………………………………..38 Table 2. Primers Used in Phylogenetic Analysis……………………………………....41 Table 3. Genbank Taxa Data…………………………………………………………….42 Table 4. Log Likelihood Estimates……………………………………………………....45 Table 5. Genotypes and Representative Sequences………………………………….46 Table 6. COI P-distances…………………………………………………………………47 Table 7. 28S P-distances………………………...……………………………………….48 Table 8. 16S P-distances……………………………...………………………………….49 Table 9. 18S P-distances……………………………...………………………………….50 Table 10. Hypotheses Proposed by Phylogenetic Analyses………………………….51 x List of Figures Figure 1. Map of Sampling Localities…………………………………………………....53 Figure 2. Picture of Congeria hoeblichi………………………………………………….54 Figure 3. Maximum Likelihood Analysis of COI Dataset………………………………55 Figure 4. Bayesian Analysis of COI Dataset……………………………………………56 Figure 5. Maximum Likelihood Analysis of 28S Dataset……………………...……….57 Figure 6. Bayesian Analysis of 28S Dataset……………………………………...…….58 Figure 7. Maximum Likelihood Analysis of 16S Dataset………………………...…….59 Figure 8. Bayesian Analysis of 16S Dataset…………………………………...……….60 Figure 9. Maximum Likelihood Analysis of 18S Dataset………………………...…….61 Figure 10. Bayesian Analysis of 18S Dataset…………………………………………..62 Figure 11. Maximum Likelihood Analysis of Mitochondrial Dataset………………….63 Figure 12. Bayesian Analysis of Mitochondrial Dataset…………………………….....64 Figure 13. Maximum Likelihood Analysis of Nuclear Dataset………………………...65 Figure 14. Bayesian Analysis of Nuclear Dataset……………………………………...66 Figure 15. Maximum Likelihood Analysis of Concatenated Dataset…………………67 Figure 16. Bayesian Analysis of Concatenated Dataset………………………………68 Figure 17. Comparative Analysis of Concatenated Dataset…………………………..69 Figure 18. TCS Haplotype Network of COI Dataset…………………………………...70 Figure 19. Maximum Clade Credibility Chronogram Created in BEAST…………….71 xi Foreword This research will be submitted to the peer-reviewed journal, Molecular Phylogenetics and Evolution. It has been formatted to fit the requirements for that journal. xii 1. Introduction 1.1 Evolutionary History of Dreissenidae The freshwater bivalve family Dreissenidae originated in Neogene fresh and brackish-water lake systems ~83.6 million years ago (MYA) during the Triassic period, concurrent with the time that Pangea began to separate into the continents of North and South America, Europe, and Africa (Bilandžija et al., 2013). Dreissenidae is the only extant family of the superfamily Dreissenoidea and contains three extant and two fossil genera: Prodreissensia and Dreisenomya (Nuttall 1990; Steipen et al., 2013). Mytilopsis (Conrad, 1857) and Congeria (Partsch, 1835) are sister genera and their common ancestor diverged from Dreissena (Van Beneden, 1835) ~37.4 MYA in the late Eocene (Bilandžija et al., 2013). The Eurasian Tectonic Plate was very close to its modern position. The Neotethys Sea was still in existence, creating shallow seas where Mediterranean, Italian, and North African coasts exist today. Congeria diverged from Mytilopsis ~22.8 MYA in the early Miocene when the Adriatic and Mediterranean seas were beginning to form and coastlines were similar to those during the present day (Bilandžija et al., 2013). Dreissena split from
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