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CHAPTER 2: Are Hypomesus Chishimaensis and H MOLECULAR SYSTEMATICS AND BIOGEOGRAPHY OF THE HOLARCTIC SMELT FAMILY OSMERIDAE (PISCES). by KATRIINA LARISSA ILVES B.Sc., The University of British Columbia, 2000 B.A., The University of British Columbia, 2001 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY in THE FACULTY OF GRADUATE STUDIES (Zoology) THE UNIVERSITY OF BRITISH COLUMBIA December 2007 © Katriina Larissa Ilves, 2007 ABSTRACT Biogeographers have long searched for common processes responsible for driving diversification in the Holarctic region. Although terrestrial flora and fauna have been well studied, much of the marine biogeographic work addresses patterns and processes occurring over a relatively recent timescale. A prerequisite to comparative biogeographic analysis requires well-resolved phylogenies of similarly distributed taxa that diverged over a similar timeframe. The overall aim of my Ph.D. thesis was to address fundamental questions in the systematics and biogeography of a family of Holarctic fish (Osmeridae) and place these results in a broad comparative biogeographic framework. With eight conflicting morphological hypotheses, the northern hemisphere smelts have long been the subjects of systematic disagreement. In addition to the uncertainty in the interrelationships within this family, the relationship of the Osmeridae to several other families remains unclear. Using DNA sequence data from three mitochondrial and three nuclear genes from multiple individuals per species, I reconstructed the phylogenetic relationships among the 6 genera and 15 osmerid species. Phylogenetic reconstruction and divergence dating yielded a well-resolved phylogeny of the osmerid genera and revealed several interesting evolutionary patterns within the family: (1) Hypomesus chishimaensis and H. nipponensis individuals are not reciprocally monophyletic, suggesting that they are conspecific and H. chishimaensis is a recently evolved freshwater ecotype that invaded the Kuril Islands following the last glaciation, (2) ii The trans-Pacific sister relationships in Hypomesus based on lateral line scale counts are not supported, implying that this phenotype evolved in parallel on each side of the North Pacific Ocean, (3) The Plecoglossidae are the Osmeridae sister group, (4) Over half of the characters from previous studies show evidence of parallel evolution; however, 27 traits reflect ancestral relationships, (5) Multiple divergences within the Osmeridae date to both the mid-Miocene cooling period and the Pliocene Bering Seaway opening, suggesting these events were important in the evolution of these fishes, and (6) Divergences in many marine taxa for which dated phylogenies are available are also correlated with these time periods. Future research should target additional Holarctic marine taxa for further comparative analysis. iii TABLE OF CONTENTS Abstract.......................................................................................................................ii Table of Contents.......................................................................................................iv List of Tables ...........................................................................................................viii List of Figures ............................................................................................................ix Acknowledgements....................................................................................................xi Dedication................................................................................................................xiv Co-Authorship Statement..........................................................................................xv CHAPTER 1: General Introduction ............................................................................ 1 1.1 Introduction ........................................................................................................ 1 1.1.1 Brief introduction to systematics and taxonomy ......................................... 1 1.1.2 Brief introduction to historical biogeography............................................... 6 1.1.3 Northern hemisphere smelts: a systematic and biogeographic case study………………………………………………………………………………. ........ 10 1.2 References...................................................................................................... 15 CHAPTER 2: Are Hypomesus chishimaensis and H. nipponensis (Pisces: Osmeridae) Distinct Species? A Molecular Assessment Using Comparative Sequence Data from Five Genes............................................................................. 27 2.1 Introduction ..................................................................................................... 27 2.1.1 Ecotypes and cryptic species ................................................................... 27 2.1.2 Osmeridae systematics background ........................................................ 28 2.2 Materials and Methods.................................................................................... 31 2.2.1 Taxon sampling and molecular analysis................................................... 31 2.2.2 Phylogenetic analysis............................................................................... 33 2.3 Results............................................................................................................ 34 2.3.1 Sequences ................................................................................................ 34 2.3.2 Phylogenetic analyses............................................................................... 35 2.4 Discussion........................................................................................................ 36 2.4.1 Relevance of geologic history of Kuril Islands .......................................... 37 2.4.2 Taxonomic status of Hypomesus chishimaensis ...................................... 37 2.5 References...................................................................................................... 42 iv CHAPTER 3: Evolutionary and Biogeographic Patterns within the Smelt Genus Hypomesus (Pisces: Osmeridae) in the North Pacific Ocean .................................. 48 3.1 Introduction ...................................................................................................... 48 3.1.1 Trans-Pacific distributions ........................................................................ 48 3.1.2 Centres of origin ....................................................................................... 49 3.1.3 Study system............................................................................................ 50 3.1.4 Justification of methods............................................................................ 51 3.1.5 Aims ......................................................................................................... 55 3.2 Materials and Methods.................................................................................... 55 3.2.1 Taxon sampling........................................................................................ 55 3.2.2 DNA sequence data ................................................................................. 56 3.2.3 Phylogenetic analyses.............................................................................. 57 3.2.4 Evaluating biogeographic scenarios......................................................... 59 3.2.5 Comparisons with other North Pacific taxa............................................... 63 3.3 Results............................................................................................................ 64 3.3.1 Sequences ............................................................................................... 64 3.3.2 Hypomesus phylogeny ............................................................................. 64 3.3.3 Biogeographic scenarios .......................................................................... 66 3.3.4 Embiotocidae and Sebastolobus cytb divergence.................................... 68 3.4 Discussion....................................................................................................... 68 3.4.1 Hypomesus phylogeny ............................................................................. 68 3.4.2 Biogeography of Hypomesus ................................................................... 72 3.4.3 Comparative biogeography of the North Pacific ....................................... 75 3.4.4 Conclusions.............................................................................................. 78 3.5 References....................................................................................................... 88 CHAPTER 4: Molecular Systematics of the Osmeridae ....................................... 103 4.1 Introduction ................................................................................................... 103 4.1.1 History of osmerid systematics............................................................... 104 4.1.2 Relationships within the Osmeroidea ..................................................... 105 4.1.3 Relationships within polytypic osmerid genera....................................... 106 4.1.4 Molecular systematics of the Osmeridae................................................ 109 4.2 Materials and Methods.................................................................................. 110 4.2.1 Taxon sampling.....................................................................................
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