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Zhongqi Chen PHYSIOLOGICAL, TRANSCRIPTOMIC AND GENOMIC MECHANISMS OF THERMAL ADAPTATION IN ONCORHYNCHUS MYKISS by Zhongqi Chen B.Sc., Xuzhou Normal University, 2007 M.Sc., Northwest A&F University, 2010 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY in THE FACULTY OF GRADUATE AND POSTDOCTORAL STUDIES (Zoology) THE UNIVERSITY OF BRITISH COLUMBIA (Vancouver) January 2017 © Zhongqi Chen, 2017 Abstract Given the rate and magnitude of the ongoing global warming, there is some urgency to understand the underlying mechanism of thermal adaptation to evaluate and predict the ecological consequences. This thesis used Oncorhynchus mykiss from different thermal regimes to examine thermal adaptation at physiological, transcriptomic and genomic levels. Thermal tolerance was examined in three redband trout (O. mykiss gairdneri) populations from warm desert and cool montane climates (Idaho, USA), as well as in a domesticated rainbow trout (O. mykiss) strain raised in a thermally challenging environment for over 19 generations (Western Australia, Australia). Acclimated to 15°C, the desert redband trout had the highest critical thermal maximum (CTMAX; 29.7°C) and maintained an almost constant absolute aerobic scope (AAS) across a broader range of test temperatures (12-24°C) than seen in other strains, but had the lowest peak AAS, suggesting a tradeoff between thermal performance and tolerance. Western Australian rainbow trout had the highest AAS, even when tested at 21°C, which may be a result of hatchery selection for thermal performance. Although the rate transition temperatures for maximum heart rate (Arrhenius breakpoint and arrhythmia temperature for fH,max) were similar among all populations, fH,max was the highest in the desert redband trout population at all temperatures. Cardiac RNA sequencing revealed different patterns of gene regulation among redband trout populations during acute warming. Many genes had different mRNA abundances between populations due to constitutive and induced expression, and the number of differentially expressed genes among populations was positively correlated to the genetic distance, suggesting intraspecific cellular regulatory strategies in response to acute warming. ii Population and quantitative genetic studies identified potential genomic markers for thermal adaptation. A total of twenty-one loci were putatively under positive thermal selection (“outliers”). In addition, genotypes of some outlier loci had significantly different CTMAX. Genome-wide association study identified twelve loci that were significantly associated with individual CTMAX. Altogether, results in my dissertation demonstrated the capacity of thermal adaptation in O. mykiss populations at multiple organismal levels. This data lays a foundation to improve our understanding on the potential impact of global warming on wild aquatic populations. iii Preface This thesis is a collaborative work by the University of British Columbia, Fisheries and Oceans Canada, Department of Fisheries (Western Australia, Australia) and Columbia River Inter-Tribal Fish Commission (USA). All experiment procedures were approved by the University of British Columbia Committee on Animal Care in accordance with the Canadian Council on Animal Care (A10-0335) and by the University of Idaho (IACUC protocol 2013- 80). Redband trout fry collection from natural streams was approved by Idaho Department of Fish and Game (Permit F-13-06-13). A version of chapter 2 has been published. Chen, Z., Snow, M., Lawrence, C., Church, A., Narum, S., Devlin, R. and Farrell, A. (2015). Selection for upper thermal tolerance in rainbow trout (Oncorhynchus mykiss Walbaum). J. Exp. Biol. 218, 803–812. Anthony Farrell and I conceived and designed the experiments with input from Shawn Narum and Robert Devlin; I performed experiments with assistance from Anthony Church. I analyzed results with input from Tony Farrell. I also drafted the manuscript. Mike Snow and Craig Lawrence organized the fish breeding. Craig Lawrence and Anthony Church performed the breeding and rearing of fish. Mike Snow conduced the hemoglobin and hematocrit analyses. Chapter 3 is based on works conducted in Hagerman Fish Culture Experimental Station in Hagerman, Idaho, USA. I designed the experiments with input from Anthony Farrell, Robert Devlin, and Shawn Narum. I assisted the fish catching from natural streams, which was mainly performed by Shawn Narum, Ben Hecht and Nick Hoffman. I carried out the experiments and most result analyses. Amanda Matala performed the Illumina sequencing. Ben Hecht carried out the bioinformatics analyses and drafted the “Genotyping” iv section in “Materials & Methods”. I wrote the rest manuscript. Anthony Farrell, Robert Devlin and Shawn Narum made key contributions to the subsequent edits. Temperature data loggers were placed and retrieved by Shawn Narum. Chapter 4 is also based on works conducted in Hagerman Fish Culture Experimental Station in Hagerman, Idaho, USA. I designed the experiments with input from Anthony Farrell, Robert Devlin, and Shawn Narum. I performed physiological experiments and prepared RNA sequencing library. Amanda Matala conducted the Illumina sequencing. Shawn Narum conducted the differential gene expression analyses and I analyzed the rest results. I drafted the writing. Anthony Farrell, Robert Devlin, and Shawn Narum provided revisions to this manuscript. v Table of Contents Abstract ................................................................................................................................... ii Preface .................................................................................................................................... iv Table of Contents ................................................................................................................... vi List of Tables ........................................................................................................................ xiii List of Figures ........................................................................................................................ xv List of Abbreviations .......................................................................................................... xvii Acknowledgements ................................................................................................................ xx Chapter 1: Introduction .......................................................................................................... 1 1.1 Characterization of thermal tolerance ....................................................................... 1 1.1.1 Critical temperatures ............................................................................................. 2 1.1.2 Aerobic scope and thermal performance .............................................................. 3 1.2 Cardiac response to temperature and its potential to limit aerobic scope................. 8 1.2.1 Role of heart rate in limiting aerobic scope .......................................................... 9 1.2.2 Cardiac arrhythmia at high temperatures ............................................................ 11 1.2.3 Thermal performance curve for maximum heart rate ......................................... 12 1.3 Cellular response to temperature and its potential to limit thermal tolerance ........ 15 1.3.1 Cellular stress response....................................................................................... 15 1.3.2 Cardiac myocyte responses................................................................................. 16 1.3.3 Using transcriptome analysis to study cellular stress ......................................... 19 1.3.4 Transcriptomic response under different thermal regimes ................................. 20 1.4 Genomic basis of thermal adaptation ..................................................................... 20 1.5 High-throughput sequencing .................................................................................. 23 vi 1.6 Thermal adaptation of Oncorhynchus mykiss ......................................................... 24 1.6.1 Known thermal requirements of O. mykiss......................................................... 25 1.6.2 Adaptation of O. mykiss populations to warm climates ..................................... 26 1.7 Thesis objectives and chapters................................................................................ 28 Chapter 2: Selection for upper thermal tolerance in rainbow trout (Oncorhynchus mykiss) ..................................................................................................................................... 33 2.1 Introduction............................................................................................................. 34 2.2 Materials and methods ............................................................................................ 37 2.2.1 Fish culture and rearing conditions..................................................................... 37 2.2.2 Critical thermal maximum .................................................................................. 38 2.2.3 Routine and maximum metabolic rate ................................................................ 39 2.2.4 Maximum heart rate ............................................................................................ 41 2.2.5 Hemoglobin and hematocrit analyses ................................................................
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