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Population Genetic Structure and Taxonomic Evaluation Of POPULATION GENETIC STRUCTURE AND TAXONOMIC EVALUATION OF TWO CLOSELY RELATED FRESHWATER MUSSEL SPECIES, THE EASTERN FLOATER, PYGANODON CATARACTA, AND THE NEWFOUNDLAND FLOATER, P. FRAGILIS, IN ATLANTIC CANADA by LJILJANA MARIJA STANTON Thesis Submitted in partial fulfillment of the requirements for The Degree of Master of Science (Biology) Acadia University Fall Convocation 2008 © by LJILJANA MARIJA STANTON, 2008 I, L. M. Stanton, grant permission to the University Librarian at Acadia University to reproduce, loan, or distrubute copies of my thesis in microform, paper or electronic formats on a non-profit basis. I, however, retain the copyright in my thesis. Signature of Author Date This thesis by Ljiljana Marija Stanton was defended successfully in an oral examination on September 2, 2008. The examining committee for the thesis was: Dr. John Murimboh, Chair Dr. W.R. Hoeh, External Reader Dr. Stephen Mockford, Internal Reader Dr. D.T. Stewart, Supervisor Dr. M. Synder, Head This thesis is accepted in its present form by the Division of Research and Graduate Studies as satisfying the thesis requirements for the degree Master of Science (Biology). TABLE OF CONTENTS List of tables vi List of figures vii Abstract ix Acknowledgements x Chapter 1. Natural history of freshwater mussels: implications for conservation 1 Life history traits of the Family Unionidae 1 Taxonomy and natural history of Pyganodon cataracta and P. fragilis 4 Molecular markers 14 Chapter 2. Population structure and taxonomic status of Pyganodon cataracta and P. fragilis inferred from AFLP and sequence data 18 Introduction 18 Methods 22 Sample collection and DNA isolation 22 Morphology analysis 29 DNA sequencing and data analysis 30 AFLP procedure and data analysis 34 Results 39 Morphological analysis 39 Mitochondrial and nuclear DNA sequencing analysis 42 AFLP analysis 49 Discussion 54 Taxonomic implications 54 (A) Morphology 54 (B) Genetic divergence 56 (C) Population genetic structure 62 Historical biogeography 65 Conservation implications 67 iv Chapter 3. General conclusions and recommendations for future conservation of freshwater mussels 71 Literature cited 76 v List of Tables Table 2.1. Description of sampling localities by province, subdrainage area and site location of both species collected, including sample size for the COI, ITS-1 and AFLP analysis 27 Table 2.2. List of reference specimens and outgroup species used in the COI and ITS-1 analysis, their locality and GenBank accession numbers Table 2.3. Selected primer sequences and primer combinations used in the AFLP analysis. Table 2.4. Genetic distances (Kimura two parameter model) of cytochrome C oxidase I sequences between outgroup species Strophitus undulatus, P. grandis, P. lacustris and P. cataracta and P. fragilis. List of Figures Figure 1.1. Suspected geographic distribution of P. cataracta and P. fragilis in Eastern Canada. 8 Figure 1.2. Illustration of the conchological features of P. cataracta and P. fragilis. 10 Figure 2.1. Map of Pyganodon sampling locations in Atlantic Canada. 26 Figure 2.2. Principle component analysis biplot showing the relationship between P. cataracta and P. fragilis individuals based on common morphological measurements. 40 Figure 2.3. UPGMA dendogram based on common morphological characteristics of the presumptive "P. cataracta" and"P. fragilis" specimens from Nova Scotia and New Brunswick. 41 Figure 2.4. Parsimony network of P. fragilis and P. cataracta mtDNA haplotypes for the COI gene. 43 Figure 2.5. 50% majority rule consensus tree (rooted) produced by a neighbor- joining analysis of the cytochrome c oxidase subunit 1 (COI) sequence data from 128 Pyganodon specimens. 45 Figure 2.6. 50% majority rule consensus tree (unrooted) produced by neighbor joining and maximum parsimony analyses of the cytochrome c oxidase subunit 1 (COI) sequence data from 128 Pyganodon specimens. 46 vn Figure 2.7. 50% majority rule consensus tree (rooted) produced by a maximum parsimony analysis of the cytochrome c oxidase subunit 1 (COI) sequence data from 128 Pyganodon specimens. 47 Figure 2.8. 50% majority rule consensus tree (rooted) produced by a maximum likelihood analysis of the cytochrome c oxidase subunit 1 (COI) sequence data from 128 Pyganodon specimens. 48 Figure 2.9. 50% majority rule consensus tree (rooted) produced by a both neighbor-joining and maximum parsimony analysis of the internal transcribed spacer region (ITS-1) sequence data from 20 Pyganodon specimens. 50 Figure 2.10. Neighbor-joining analysis of 35 Pyganodon specimens based on data from 235 AFLP loci with 100 bootstrap replicates. 51 Figure 2.11. Graphs depicting the methods used for determining value of K or number of groups from the AFLP data set. 52 Figure 2.12. A triangle plot displaying the estimated membership coefficient for each individual into its assigned population (Newfoundland, New Brunswick or Nova Scotia). 53 viii Abstract The freshwater mussels Pyganodon cataracta and Pyganodonfragilis are both found in Atlantic Canada but their taxonomic status and exact geographic distribution is uncertain. Phenotypic plasticity and convergence of shell characteristics has created difficulties in delineating unionids based on morphological traits. Our study will utilize the mitochondrial cytochrome c oxidase (COI) gene, the nuclear internal transcribed spacer region (ITS-1) gene and a multi locus marker, amplified fragment length polymorphisms (AFLPs), in conjunction with morphological data to determine if P.cataracta and P. fragilis are two distinct species, just one species, or a mixed hybridizing population. Mussels collected from Newfoundland, Nova Scotia, New Brunswick and Prince Edward Island displayed low levels of genetic variability and extremely low divergence values for both the COI and ITS-1 sequence data, forming a single monophyletic group. Population genetic structure inferred from 235 AFLP loci, showed a moderate level of geographic structuring based on province, however no genetic differentiation among the putative species was observed. Common morphological characteristics used to distinguish the species in question were found to be unreliable. Our holistic approach of combining morphology, mitochondrial and nuclear data clearly indicates that P. cataracta and P. fragilis are not distinct species and should be regarded as a single species, with P. cataracta having nomenclatural priority. These data also have implications for understanding the historical biogeography of P. cataracta and for conservation strategies for this species in eastern Canada. ix Acknowledgements I can not begin to explain how rewarding and enriching this experience has been for me. I would like to thank, first and foremost, my supervisor Don Stewart who provided me with this opportunity and has guided me along the way, together with all the wonderful people in the Biology Department at Acadia who have allowed me to learn and grow as a biologist. Specifically at Acadia, I would like to thank Rodger Evans for supplying the AFLP reagents, Steve Mockford for all the insightful discussions and Nancy and Wanda for always being so kind and helpful. A special thanks to Aaron Shafer and Mamta Jha in the DTS lab for all your advice and assistance and to my fellow graduate students and friends for our memorable gatherings- I've enjoyed getting to know you all through the past few years. None of this work would have been possible without the hard work and dedication of fellow mussel enthusiasts Randy Hoeh, John Maunder and Don McApline, who collected and donated Pyganodon samples from across Atlantic Canada. Financial support for this research was primarily funded by the New Brunswick Wildlife Trust Fund, in addition to, the Acadia University Research Fund and the National Science and Engineering Research Council of Canada (via Don Stewart). Acadia Graduate Awards and the Dr. Robert Graeme Boutilier Memorial Research Award provided financial assistance for my stipend. x Finally, I would like to thank my family Barret, Renee and especially my Mom for their continued support and enthusiasm for whatever it is I choose to do. To my father for unwittingly instilling in me a love of science, this thesis is dedicated to your lasting memory. Last but certainly not least my wonderful, loving husband you are definitely the best. I cannot thank you enough for supporting me every step of the way, providing advice and encouragement, a listening ear, and a helping hand in collecting mussels - you truly deserve a honourary degree. 'The essential purpose is to decide for oneself what is of genuine value in life. And then to find the courage to take your own thoughts seriously' - Albert Einstein. xi Chapter 1. Natural history of freshwater mussels: Implications for Conservation Life history traits of the Family Unionidae Freshwater mussels (Order Unionoida) are a fascinating yet widely overlooked group of animals whose populations are drastically declining in many areas and are considered among the most endangered groups of organisms in North America (Williams et al, 1993; Lydeard et al, 2004). Freshwater mussels are broadly distributed on all continents except Antarctica but they attain the greatest diversity in North America where over 300 species have been described (Williams et al, 1993; Turgeon et al, 1998, Roe and Hoeh, 2003). Despite their relatively high diversity, the Phylum Mollusca has the greatest number of recorded extinctions of any taxonomic group (Lydeard et al, 2004) and of the freshwater mussels in North America, 70% of species
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