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Limits of Life History in Taxonomic Classification of Lampreys with Implications for Conservation A thesis presented to the faculty of the Voinovich School of Leadership & Public Affairs In partial fulfillment of the requirements for the degree Master of Science Aaron B. Cranford August 2013 © 2013 Aaron B. Cranford. All Rights Reserved. 2 This thesis titled Limits of Life History in Taxonomic Classification of Lampreys with Implications for Conservation by AARON B. CRANFORD has been approved for the Program of Environmental Studies and the Voinovich School of Leadership & Public Affairs by Matthew M. White Associate Professor of Biological Sciences Mark Weinberg Director, Voinovich School of Leadership & Public Affairs 3 ABSTRACT CRANFORD, AARON B., M.S., August 2013, Environmental Studies Limits of Life History in Taxonomic Classification of Lampreys with Implications for Conservation Director of thesis: Matthew M. White In the genus Ichthyomyzon there are closely related species that are morphologically and ecologically similar in their larval stage known as paired species (Docker et al., 2012). The nonparasitic Mountain Brook Lamprey (I. greeleyi) and the parasitic Ohio Lamprey (I. bdellium) is a species pair found in the Eastern United States. The Mountain Brook Lamprey is endangered in Ohio (OhioDNR, 2013). These two species are genetically very similar. This raises questions about the appropriateness of using trophic behavior alone for lamprey classification, and a better understanding of this relationship may better inform any conservation efforts. The current study examined the relationship between the nonparasitic I. greeleyi and parasitic I. bdellium using the ND3 and Noncoding I genes in the lamprey mitochondrial genome. My results support multiple origins with recent expansion of I. greeleyi and I. bdellium. These results are consistent with other studies of paired lamprey species. However, alternative hypotheses such as ongoing gene flow with ecotypes of the same species, single origin, and mitochondrial introgression cannot be ruled out. Additional data are needed to clarify these hypotheses for paired lamprey species. The results will inform decisions on whether the two feeding modes can be managed as a single species. 4 DEDICATION I dedicate this to my friends and family. Thank you for all of your support and guidance through the years. None of this would have been possible without you. I also dedicate this to my advisor, committee members, and other collaborative colleges. You input and support has been invaluable. 5 ACKNOWLEDGMENTS I would like to acknowledge the following: Ohio EPA, Ohio State University Museum of Biodiversity, Ohio University, United States National Museum (USNM), North Carolina Museum of Natural History (NCMNH), and Margaret F. Docker for the samples they contributed; my advisor Dr. White for his patience, guidance, support, unwavering optimism, and willingness to work with me; my committee members, Dr. Kuchta and Dr. Ballard for their patience and understanding; Dr. Kruse for helping with my locality map; Vijay Nadella and his technicians for the quick turnaround on sequences; OFMWA for allowing me to present my poster at their conference; Jeff Thuma for printing my poster; The Voinovich School of Leadership and Public Affairs for accepting me into their program and giving me the opportunity to continue to peruse my education; and all the other MSES and EEB graduate students for stimulating conversations that kept me fascinated with science. 6 TABLE OF CONTENTS Page Abstract ................................................................................................................................ 3 Dedication ............................................................................................................................ 4 Acknowledgments ............................................................................................................... 5 List of Tables ....................................................................................................................... 7 List of Figures ...................................................................................................................... 8 Introduction ......................................................................................................................... 9 Materials and Methods ...................................................................................................... 14 Animals and Localities .................................................................................................. 14 DNA Sequencing ........................................................................................................... 14 Data Analysis ................................................................................................................. 15 Results ............................................................................................................................... 17 ND3 ............................................................................................................................... 17 NCI ................................................................................................................................ 18 ND3/NCI Combined ...................................................................................................... 18 Discussion .......................................................................................................................... 19 Genetics Results ............................................................................................................ 19 Relationship to Other Species Pairs .............................................................................. 20 Conservation Implications ............................................................................................. 21 Future Directions for Research ...................................................................................... 22 References ......................................................................................................................... 38 7 LIST OF TABLES Page Table I: Dataset and GenBank Accession Numbers ....................................................... 23 8 LIST OF FIGURES Page Figure 1. Mountain Brook lamprey Oral Disc ................................................................ 26 Figure 2. Mountain Brook lamprey Profile .................................................................... 26 Figure 3. Ohio lamprey Oral Disc .................................................................................. 27 Figure 4. Localities Map ................................................................................................. 28 Figure 5. Mountain Brook lamprey distribution map ..................................................... 29 Figure 6. Ohio lamprey distribution map ....................................................................... 30 Figure 7: ND3 Maximum Likelihood Tree .................................................................... 31 Figure 8: ND3 Minimum Spanning Network ................................................................. 32 Figure 9: ND3 Frequency Distribution Chart ................................................................. 33 Figure 10: NCI Maximum Likelihood Tree ................................................................... 34 Figure 11: NCI Minimum Spanning Network ................................................................ 35 Figure 12: ND3/NCI Combined Maximum Likelihood Tree ......................................... 36 9 INTRODUCTION The traditional convention for lamprey classification is based on life history characteristics, (Potter and Bailey, 1972; William et al., 1988; Kucheryavyi et al., 2007) morphometrics, and meristics (Potter, 1980; William et al., 1988; Lanteigne, 1988; Bird et al., 1994). The life history characteristic refers to lamprey’s feeding mode (parasitic and nonparasitic) and the timing of sexual maturation relative to metamorphosis. Morphometric and meristic characteristics include dentition patterns, body size, myomere counts, fin patterns, and pigmentation. Some studies have used body proportions (percentages of a particular body part relative to the total length) for species classification(Richards et al., 1982; Meeuwig et al., 2006; Renaud, 2011). Yet, considerable evidence suggests diagnostic characteristics are not the best tool for assessing the status of and relationships among lamprey species. This is because many lamprey species occur as species pairs, and there is support for considering some pairs a single species. Many species in the family Petromyzontidae exist as closely related species pairs(Lang et al., 2009). Paired lamprey species are characterized by larvae that are morphologically and ecologically similar, but after metamorphosis they are morphologically distinct (Docker et al., 2012). These pairs are also characterized as being either a parasitic form or a nonparasitic form(Salewski, 2003; Docker et al., 2012). Within a species pair, life history traits differ between the parasitic and nonparasitic forms. The primary difference in life history between two species that make up a pair is the feeding mode after metamorphosis. After metamorphosis, a parasitic species will 10 make its way to a larger water body (river, pond, lake, or ocean) and feed on the blood of other fish. A nonparasitic species does not feed and will stay in its resident stream to spawn (Potter,
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