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A Systematic Study of the Clam Shrimp Genus

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A Systematic Study of the Clam Shrimp Genus A SYSTEMATIC AND BIOGEOGRAPHIC STUDY OF THE CLAM SHRIMP GENUS EULIMNADIA PACKARD, 1874 (BRANCHIOPODA: SPINICAUDATA: LIMNADIIDAE) AND AN INVESTIGATION INTO THE EVOLUTION AND MAINTENANCE OF ANDRODIOECY IN EULIMNADIA DAHLI DAKIN, 1914 A dissertation submitted to Kent State University in cooperation with The University of Akron in partial fulfillment of the requirements for the degree of Doctor of Philosophy by Sadie K. Reed Stimmell August 2013 i Dissertation written by Sadie K. Reed Stimmell B.S., Northern Arizona University, 2000 M.S., Northern Michigan University, 2003 Ph.D., Kent State University, 2013 Approved by ____________________________, Chair, Doctoral Dissertation Committee Dr. Stephen C. Weeks ____________________________, Co-advisor, Doctoral Dissertation Committee Dr. Walter R. Hoeh ____________________________, Members, Doctoral Dissertation Committee Dr. Andrea Case ____________________________, Dr. Lisa E. Park ____________________________, Dr. Alison Smith Accepted by ____________________________, Chair, Department of Biological Sciences Dr. Laura G. Leff ____________________________, Dean, College of Arts and Sciences Dr. Raymond Craig ii TABLE OF CONTENTS LIST OF FIGURES………………………………………………………………..v LIST OF TABLES…………………………………………………………………vi ACKNOWLEDGMENTS…………………………………………………………vii CHAPTERS I. GENERAL INTRODUCTION……………………………………………..1 II. A SYSTEMATIC STUDY OF EULIMNADIA Abstract…………………………………………………………………….3 Introduction………………………………………………………………..4 Materials and Methods…………………………………………………….11 Results………………………………………………………………………16 Discussion…………………………………………………………………...29 Acknowledgements………………………………………………………….38 III. A BIOGEOGRAPHIC ANALYSIS OF THE EULIMNADIA WITH AN ASSESSMENT OF THE EVOLUTION OF ANDRODIOECY Abstract……………………………………………………………………..39 Introduction…………………………………………………………………40 Materials and Methods………………………………………………………42 Results……………………………………………………………………….44 Discussion……………………………………………………………………50 Acknowledgements…………………………………………………………..55 IV. AN INVESTIGATION OF THE MAINTENANCE OF ANDRODIOECY VIA METAPOPULATION DYNAMICS IN EULIMNADIA DAHLI Abstract………………………………………………………………….56 iii Introduction……………………………………………………………...57 Materials and Methods…………………………………………………..63 Results…………………………………………………………………….65 Discussion…………………………………………………………………71 Acknowledgements………………………………………………………..78 V. GENERAL DISCUSSION AND CONCLUSIONS………………………..80 REFERENCES…………………………………………………………………..86 iv LIST OF FIGURES Figure 2.1 Phylogenetic tree resulting from analysis of both cytb and EF1 Figure 2.2 Phylogenetic tree resulting from analysis of EF1 Figure 2.3 Phylogenetic tree resulting from maximum likelihood analysis of cytb Figure 2.3a Clade from phylogenetic tree resulting from maximum likelihood analysis of cytb Figure 2.4 Phylogenetic tree resulting from Bayesian inference analysis of cytb Figure 2.4a First clade from phylogenetic tree resulting from Bayesian inference analysis of cytb Figure 2.4b Second clade from phyloenetic tree resulting from Bayesian inference analysis of cytb Figure 3.1 Continental plates used for distributional areas Figure 3.2 Ancestral area reconstruction for Eulimnadia based on both EF1 and cytb Bayesian analysis Figure 3.3 Present day species distributions and biogeographic dispersal events Figure 4.1 Percent males versus genetic diversity Figure 4.2 Gene flow versus distance of outcrops v LIST OF TABLES Table 2.1 List of valid Eulimnadia species names in Brtek (1997) Table 2.2 Additional Eulimnadia species Table 2.3 List of specimens included in phylogenetic analysis Table 2.4 Primer Pairs used for DNA amplification Table 2.5 Current taxonomic status of the North American Eulimnadia species Table 4.1 Population Descriptive Statistics Table 4.2 Pairwise FST and Nm Estimates Table 4.3 Heirarchical model of population genetic structure vi ACKNOWLEDGEMENTS Many times throughout my dissertation research, I heard the quest for a PhD described as a lonely pursuit. This is very much not the case as I look back and find I am overwhelmed with the number of people who helped me along the way. I am filled with the deepest gratitude to all of the people who have supported me in this degree. First, I would like to extend my thanks to my doctoral advisor, Dr. Steve Weeks. He was a true mentor in every aspect of my academic career, from research and writing to teaching and field work. He has been a friend and was always quick to offer encouragement and praise when I needed it. He never gave up and always believed I could accomplish this dissertation, and that is truly why I have. I would like to thank my co-advisor, Dr. Walter R. Hoeh for much time learning techniques in the lab and much of his encouragement along the way. I would also like to thank my committee members, Dr. Lisa Park Bousch, Dr. Andrea Case, and Dr. Alison Smith for many helpful comments and suggestions that have strengthened this document. I have been so fortunate to receive a great amount of help and support from a number of professors at the University of Akron. Dr. Joel Duff never hesitated to offer so much of his time in the lab and was always willing to take time to explain things over and over until I understood. This research would certainly not have been completed without him. Dr. Francisco Moore was a huge help in all of my statistical questions and always had an open ear for ideas and frustrations. Thank you also to Dr. Peter Niewiarowski, Dr. Brian Bagatto, Dr. Richard Londraville and Dr. Randy Mitchell. I would also very much like to thank Dr. Mark Kershner for his help and support at Kent State University. vii My field experience in Western Australia was filled with adventure and once-in- a-lifetime experiences. It would not have been possible without the limitless generosity of Dr. Brenton Knott, who welcomed us into his lab and home. I will cherish the memories of Friday lab meetings complete with “drinkable” reds and cheese and classical music. All of the wonderful people at the School of Animal Biology at the University of Western Australia, in Perth contributed to our successful research and fantastic experience. Thank you to Kerry, Debra, Danny, Magdalena, Wally, Bonnie, and Rob. I am so grateful to have enjoyed three field seasons in Las Cruces, NM at the Jornada LTER. We were so fortunate to have the help and friendship of Dr. Naida Zucker and Dr. Richard Spellenberg, along with Dr. Michele Nishiguci’s and her lab team. So many friendships were formed with the students in the Department of biology at NMSU, including Vinod, Bryan, TuShun, and Will. Thank you for the lab space and so much fun. I can truly say that one person was with me through all the ups and downs and experiences of graduate school, Dr. Chiara Benvenuto. She was with me in every field season all over the globe and shared every adventure. Thank you for your continuous support and friendship through thick and thin. The “clam shrimp crew” was a conglomeration of wonderful people who were always helpful and friendly and supportive in every way. Thank you to Allisa Calabrese, Tom Sanderson, Beth Wallace, and Amanda Crow. I formed a number of friendships with so many fellow students at the University of Akron and I am particularly thankful to Jenn Purrenhage for all of her talks through my anxieties. viii So much happens in the many years it takes to complete a doctorate. I was fortunate to marry a loving and supportive person who has always encouraged me and done everything in his power to help be along the way. Thank you so very much, Sean Stimmell, for always believing in me and adding a healthy dose of humor to every situation. We were also blessed with two children, Finnbar and Josette, during the course of this degree and they have added to my life in so many ways and given me the perspective needed to finish. Thank you to the number of generous people who have helped with childcare during my final writing phase: Kate Stimmell, Amy Carlson, and Jenn DePiano. Thank you to my parents who have encouraged me in every step, from my very first. Tish Lacy Reed and Raymond Reed, this would not have been accomplished without you. This dissertation was by no means a lonely pursuit with the number of people who stood by me and helped in every way they could. Thank you to any one I may have left out as I was blessed to be surrounded by so many wonderful folks. I am indebted to all of you and I am sincerely grateful. ix I. GENERAL INTRODUTION The clam shrimp genus Eulimnadia is a cosmopolitan taxon comprising approximately 54 species (Brtek 1997; Martin & Belk 1989; Roessler 1990; Pereira & Garcia 2001; Durga-Prasad & Simahachalam 2004; Simahachalam 2004, 2005; Timms & McLay 2005; Babu & Nandan 2010; Rogers et al. 2010). It is the most speciose spinicaudatan genus and is of particular interest due to its exhibition of an extremely rare mating system - androdioecy (Weeks et al. 2006; Weeks 2012). Androdioecy is the co- occurrence of males and hermaphrodites in populations in the absence of true females. The evolutionary benefits of such a makeup are unclear. Males can play an important role in hermaphroditic populations to avoid inbreeding depression and to supplement male allocation in sperm-limited hermaphrodites (Wolf & Takebayashi, 2004). Yet males have difficulty invading hermaphroditic populations because of reduced mating opportunities due to the ability of hermaphrodites to self-fertilize. This requires males to more than double their mating success (i.e., successful fertilizations) relative to hermaphrodites to effectively invade the population. Theoretical
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