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Population Genomics and Sex Determination by Hollie Johnson B Northern Pike of North America: Population Genomics and Sex Determination by Hollie Johnson B.Sc., University of Victoria, 2010 A Thesis Submitted in Partial Fulfillment of the Requirements for the Degree of MASTER OF SCIENCE in the Department of Biology © Hollie Johnson, 2019 University of Victoria All rights reserved. This thesis may not be reproduced in whole or in part, by photocopy or other means, without the permission of the author. Northern Pike of North America: Population Genomics and Sex Determination by Hollie Johnson B.Sc., University of Victoria, 2010 Supervisory Committee Dr. Ben Koop, Supervisor Department of Biology Dr. John Taylor, Co-Supervisor Department of Biology Dr. John Nelson, Departmental Member Department of Biology ii Abstract Northern Pike (Esox lucius) is an economically and ecologically valuable species with a circumpolar distribution across the Northern Hemisphere. Northern Pike have been shown to have low levels of genetic variation despite their great capacity to colonize new environments. Here, high-resolution resequencing data from 47 Northern Pike from across North America was used for SNP discovery and population analysis. Our analysis reveals an extraordinary lack of genetic variation among Northern Pike with observed heterozygosity (Ho) of just 0.0835. Our analyses suggest that two major groups of Northern Pike exist in North America that are separated by the North American Continental Divide. Genetic variation associated with the stratification of these two groups resides across the genome particularly in gene regions with multiple copy number variants and functions related to immunity, tissue permeability, and development. Northern Pike from Alaska and the Yukon River harbour about two times more heterozygosity than Northern Pike east of the Continental Divide with an average of one heterozygous SNP every 6,250 bases. Populations east of the Continental Divide possess a remarkable level of genetic homogenization with an average of just one heterozygous SNP every 16,500 bases. For comparison, an average of one heterozygous SNP per 309 bases was reported in herring (Martinez Barrio et al., 2016), one per 500 in Atlantic cod (Star et al., 2011), and one per 750 bases in Coho and chinook salmon (Koop, 2018). This is at least 5 – 10 fold less variation than is seen in humans (the 1000 Genomes Project Consortium, 2015). We observed a recently described master sex-determining gene, amhby, in three western North American populations but not in populations east of the Continental Divide. We could not resolve any signals indicating a genetic sex determination system was present in populations iii from southern Manitoba or the St. Lawrence River. This may indicate that environmental sex determination is at play in these populations. We found evidence of a possible female- heterozygous, male homozygous ZW-ZZ genetic sex-determination system in New Jersey Northern Pike. With the highest average of 181,268 heterozygous SNPs genome wide and the greatest Ho (0.3228) of all populations, as well as the presence of the sex-determining gene amhby indicate that Northern Pike from our Alaskan population are the oldest in North America. Fewer numbers of heterozygous SNPs (61,073), low Ho (0.0922), and the absence of amhby in Northern Pike east of the Continental Divide suggests that these are relatively young populations and are descended from a small founding population. These results imply that Northern Pike first came to North America through Beringia and colonized its North American range from there, possibly via pro-glacial lake formation and drainage. However, from the data herein it was not possible to trace how re-colonization occurred after the final retreat of glaciers at the end of the last ice age. This thesis provides a genetically high-resolution snapshot of Northern Pike population structure in North America. It demonstrates that organisms with largely homogenous genomes can be incredibly successful and resilient. Finally, it adds to the complex subject of sex determination in fish and provides insight into a sex determination system in transition. iv Table of Contents Supervisory Committee .................................................................................................................. ii Abstract .......................................................................................................................................... iii Supervisory Committee ............................................................................................................... iii Table of Contents ............................................................................................................................ v List of Tables ............................................................................................................................... viii List of Figures ................................................................................................................................ ix List of Acronyms ............................................................................................................................ x Acknowledgements ........................................................................................................................ xi Dedication ..................................................................................................................................... xii Chapter 1 ......................................................................................................................................... 1 Introduction ................................................................................................................................. 1 Thesis Overview ..................................................................................................................... 1 Northern Pike ecology ............................................................................................................ 3 Genetic variation ..................................................................................................................... 4 Variation in Northern Pike ...................................................................................................... 5 Importance of the Northern Pike Reference Genome ........................................................... 10 Phylogenetic position of Northern Pike ................................................................................ 10 Phylogeography .................................................................................................................... 12 Esociformes and relationship to Salmoniformes .................................................................. 13 Sex determination ................................................................................................................. 14 Locating sex determining loci ............................................................................................... 16 Sex determining genes in fish ............................................................................................... 18 Sex determination in Northern Pike ...................................................................................... 22 Benefits of identifying sex determination systems ............................................................... 23 Summary of research questions ............................................................................................ 25 Chapter 2 ....................................................................................................................................... 26 Genetic variation and population genomics .............................................................................. 26 Summary ............................................................................................................................... 26 Introduction ........................................................................................................................... 28 Methods..................................................................................................................................... 30 Samples ................................................................................................................................. 30 DNA extraction and sequencing ........................................................................................... 30 v Read processing and variant calling ..................................................................................... 32 Population analysis ............................................................................................................... 34 Results ....................................................................................................................................... 39 DNA sequence processing and variant discovery ................................................................. 39 Raw SNP counts ................................................................................................................... 39 Phylogeny ............................................................................................................................. 44 PCA ....................................................................................................................................... 46 DAPC and high-loading SNPS ............................................................................................. 47 Genotype
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