Salvelinus Confluentus) and Dolly Varden (S. Malma

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Salvelinus Confluentus) and Dolly Varden (S. Malma Molecular evidence of current and historical introgressive hybridization between bull trout (Salvelinus confluentus) and Dolly Varden (S. malma) by ZOE REDENBACH B.Sc, University of British Columbia, 1997 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE in THE FACULTY OF GRADUATE STUDIES (Department of Zoology) We accept this thesis as conforming to the required standard THE UNIVERSITY OF BRITISH COLUMBIA August 2000 © Zoe Redenbach, 2000 In presenting this thesis in partial fulfilment of the requirements for an advanced degree at the University of British Columbia, I agree that the Library shall make it freely available for reference and study. I further agree that permission for extensive copying of this thesis for scholarly purposes may be granted by the head of my department or by his or her representatives. It is understood that copying or publication of this thesis for financial gain shall not be allowed without my written permission. Department of The University of British Columbia Vancouver, Canada DE-6 (2/88) ABSTRACT Natural hybridization, once thought to be relatively rare, has been widely observed in both plants and animals. Studies of species that hybridize at low rates across wide ranges, however, are still relatively rare. Dolly Varden (Salvelinus malma) and bull trout (S. confluentus) have widely overlapping ranges and have been shown to hybridize at two localities. This thesis is a molecular analysis of Dolly Varden / bull trout hybridization over a range of spatial scales. Large-scale mtDNA phylogeography revealed that Dolly Varden survived the last glaciation in a previously unsuspected refuge south of the ice sheet, which resulted in continuous sympatry of a Dolly Varden refugial population with bull trout over the last 100,000 years. Discordant mitochondrial and nuclear phylogenies revealed historical introgression of bull trout mitochondrial DNA into Dolly Varden. Population samples revealed widespread local sympatry and current hybridization throughout the overlapping range, with hybrids consisting of 0 to 25% of the local samples. A detailed analysis of hybridization within a single watershed in north-central British Columbia revealed that individuals of hybrid origin form 9% of the juvenile population of char (0.5% Fi, 0.5% Fn, and 8% backcross genotypes). Initial interspecific hybridization is unidirectional, Dolly Varden male by bull trout female, likely attributable to a 'sneaking' mating strategy used by smaller Dolly Varden males. The Fi hybrids were fertile and backcrossed with both parental species. The introgression of nuclear and mitochondrial alleles was asymmetrical, with bull trout mtDNA and Growth Hormone 2 introgressing into Dolly Varden at higher levels than both the three other nuclear loci and the reverse direction introgression of Dolly Varden alleles into bull trout, suggesting that the strength of selection can vary across nuclear loci and between species. As Dolly Varden and bull trout appear to be distinct species in sympatry, despite introgressive hybridization, a balance between gene flow and selection must be in place. I suggest that selection acts primarily against the adult hybrid population, as the morphological and behavioural intermediacy of hybrid and backcross individuals as adults would affect their potential reproductive success and their ability to succeed in either of the two alternate life- histories bull trout and Dolly Varden adopt in sympatry (adfluvial vs. stream-resident). ii TABLE OF CONTENTS Abstract ii Table of Contents iii List of Tables v List of Figures vii Acknowledgements viii Chapter 1: General Introduction 1 Chapter 2: Phylogeography of Dolly Varden: evidence for a southern glacial refuge and historical introgression of bull trout mitochondrial DNA 11 Introduction 12 Materials and Methods 16 Results 23 Discussion 37 Chapter 3: Widespread local sympatry and evidence for hybridization between Dolly Varden and bull trout throughout British Columbia 47 Introduction 48 Materials and Methods 50 Results and Discussion 52 Chapter 4: Directional hybridization, bi-directional backcrossing, and the asymmetrical introgression of alleles in a Dolly Varden / bull trout hybrid zone 62 Introduction 63 Materials and Methods 66 Results 78 iii Discussion 97 Chapter 5: General Discussion 115 References 124 Appendix 1: Mitochondrial DNA ND1 sequences 134 Appendix 2: Growth Hormone 2 Intron C sequences.... 136 Appendix 3: Ribosomal DNA ITS-1 sequences 137 Appendix 4: Genotypes by age class and by tributary 138 Appendix 5: Bull trout allele frequencies by age class and by tributary 139 Appendix 6: Hybrid genotypes by age class and by tributary 140 iv LIST OF TABLES Table 1: Salvelinus sample sites for phylogenetic and hybridization analysis .....17 Table 2: Molecular markers ; 20 Table 3: PCR conditions 21 Table 4: Sequence divergence between Salvelinus mtDNA haplotypes, and haplotype and nucleotide diversity within and nucleotide divergence between bull trout and Dolly Varden populations 31 Table 5: Sequence divergence between Salvelinus Growth Hormone 2 intron C sequences and ribosomal DNA first internal transcribed sequences 35 Table 6: Hybridization, species proportions, mtDNA clade by sample site 53 Table 7: Inbreeding deficits for char samples from across B.C. 60 Table 8: Genotypes of juvenile char collected in tributaries to Thutade Lake Watershed 79 Table 9: Visual versus genetic identification of juvenile char 81 Table 10: Bull trout allele frequency and percentage of hybrid origins, by tributary ...82 Table 11: Inbreeding deficits by tributary 84 Table 12: Gametic phase disequilibria by tributary 85 Table 13: Cytonuclear disequilibria by tributary 86 v Table 14: Introgression of nuclear and mitochondrial alleles by tributary 88 Table 15: Static and dynamic cohort analysis 92 vi LIST OF FIGURES Figure 1: Parapatric species distributions of Dolly Varden (5. malma) and bull trout (5. confluentus) 7 Figure 2: Phylogenetic tree of Salvelinus mtDNA sequences 24 Figure 3: Geographic distribution of Dolly Varden and bull trout mtDNA clades 27 Figure 4: Phylogenetic tree of Salvelinus Growth Hormone 2 intron C sequences 33 Figure 5: Phylogenetic tree of Salvelinus ribosomal DNA first internal transcribed sequences .36 Figure 6: Distribution of hybridization amongst sympatric sample sites, and location of Thutade Lake watershed 55 Figure 7: Thutade Lake watershed sample sites and distribution of hybrids 67 Figure 8: Kemess Creek sample sites and distribution of groundwater upwelling (preferred Dolly Varden spawning sites) 69 Figure 9: Introgression of nuclear and mtDNA alleles between Dolly Varden and bull trout 90 Figure 10: Distribution of Dolly Varden, bull trout and hybrid fry and juveniles in Kemess Creek 95 vii ACKNOWLEDGEMENTS My supervisor, Dr. Eric Taylor, guided me through my undergraduate Honour's thesis so skillfully that I knew a Master's degree spent in his lab would be time very well spent. I was right. His door was always open and his enthusiasm unparalleled. His financial and moral support allowed me the unforgettable experience of presenting my research at a European conference. Perhaps most importantly, he always gave thoughtful consideration to my questions and queries. It is thanks to him that my time as a graduate student was so intellectually satisfying. My supervisory committee, Lee Gass, JD McPhail, Eric Taylor, and Mike Whitlock, hashed over my proposal and made many insightful suggestions over the drafts of this thesis. They helped to guide my research and create the final thesis that is before you. My too-short field season was spent in the company of Gordon Haas and John Hagen. Gordon's knowledge of char was an oft-visited source of information. His help in tracking down references and his assistance in a search for char gametes were greatly appreciated. John's study about the ecology of sympatric char provided the ecological framework for my genetics and laid the foundation for my hypothesizing. I spent three years surrounded by a wonderful, supportive lab group, Alon Altman, Dawn Cooper, Janelle Curtis, Jason Ladell, Steve Latham, Derek Louie, Megan McCusker, Jen McLean, Dave O'Brien, Mike Stamford, and Patrick Tamkee. Thanks to them the lab was never lonely and no problem ever went unsolved. I had some fantastic times. Finally, I received tissue samples and molecular markers from various sources. In particular, Dave Bustard sent many samples and shared much knowledge about Thutade Lake watershed. Chris Foote and Brian Urbain at the University of Washington gave me the Alaskan and Kuril Island samples with which I put the last touches on my zoogeographical study. Paul Moran, also from the University of Washington, kindly shared seventeen primer sets developed in his lab. viii Chapter 1: General Introduction 1 Interspecific hybridization is a topic of great interest to both evolutionary and conservation biologists. It is a natural process by which new species can evolve (e.g. Meagher & Dowling 1991; Quattro et al. 1991, 1992; Abbott 1992; DeMarais et al. 1992; Bullini 1994) and by which rare or endangered species can be driven extinct (Arnold 1997). Introgression, the movement of genes across a species barrier, can provide the genetic diversity required to adapt to changing environments, but it can also lead to the dilution or disruption of genomes already well-adapted (Arnold 1997). Studies of the ecological and evolutionary conditions leading to hybridization or reproductive isolation,
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