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PHYLOGENETIC ANALYSIS OF CHROMOSOME NUMBERS AND GENETIC MARKERS by Shing Hei Zhan B.Sc. (Hon.), The University of British Columbia, 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 (Bioinformatics) THE UNIVERSITY OF BRITISH COLUMBIA (Vancouver) August 2020 © Shing Hei Zhan, 2020 The following individuals certify that they have read, and recommend to the Faculty of Graduate and Postdoctoral Studies for acceptance, the dissertation entitled: Evolutionary analysis of chromosome numbers and genetic markers submitted by Shing Hei Zhan in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Bioinformatics Examining Committee: Sarah P. Otto, Professor, Department of Zoology, The University of British Columbia Supervisor Wayne P. Maddison, Professor, Department of Zoology, The University of British Columbia Supervisory Committee Member Darren Irwin, Professor, Department of Zoology, The University of British Columbia University Examiner Alexandre Bouchard-Côté, Associate Professor, Department of Statistics, The University of British Columbia University Examiner Additional Supervisory Committee Members: Sean W. Graham, Professor, Department of Botany, The University of British Columbia Supervisory Committee Member Itay Mayrose, Associate Professor, Department of Molecular Biology and Ecology of Plants, Tel Aviv University Supervisory Committee Member ii Abstract A phylogenetic tree captures the evolutionary relationships among sampled taxa – major taxonomic groups, species, infraspecific taxa, or isolates. Phylogenetic analysis is a central component of evolutionary and ecological studies, as it lends a unifying framework to draw inferences about evolutionary and ecological processes that form biodiversity. Via phylogenetic comparative methods, trait data (for example, morphological or physiological data) and geographical data may be analyzed jointly with a given phylogeny to test specific hypotheses about the evolution and ecology of focal groups of organisms. In this thesis dissertation, I present four studies demonstrating how phylogenetic analysis can yield new evolutionary and ecological insights. In the first two studies, I compare the evolutionary fates of polyploid versus diploid lineages in fish and to test whether polyploidization coincides with speciation events in land plants. Polyploid species arise from whole genome duplication and often exhibit morphological, physiological, and ecological differentiation from their diploid parents. Understanding their evolutionary patterns in the background of diploid species help us to understand why polyploidization is abundant in some organisms (plants) but not in others (fishes). In the other two studies, I explore the biodiversity of freshwater red algae in the wild and aquarium shops, using phylogenetic analyses to reveal potential introductions of these organisms via the global aquarium trade. Furthermore, I identify candidate genetic markers that may be more suitable than commonly used markers to facilitate future studies of phylogenetic community ecology of the red algae. Not only do these studies illustrate the utility of phylogenetic analyses to tackle diverse questions in evolution and ecology, but they also have forwarded the discussion on those four distinct topics. iii Lay Summary A phylogenetic tree represents the evolutionary relationships among organisms. Phylogenetic trees allow biologists to put questions into a larger evolutionary context. In the four studies described herein, I utilized phylogenetic methods to reap insights into the evolution and ecology of different organisms – fishes, plants, and algae. In the first two studies, I compare the evolutionary fates of polyploids (with more than two sets of chromosomes) and their diploid relatives (with two sets of chromosomes) in fishes and plants. Polyploids arise from genome duplication and often possess characteristics distinct from their diploid parents. In the other two studies, I investigate the biodiversity of the red algae in the wild and in aquarium shops and develop a new molecular tool to explore their diversity better. The studies illustrate how phylogenetic analyses can help investigate diverse questions in evolution and ecology. iv Preface The studies presented in this thesis dissertation have either been published or submitted for publication. Below I indicate my contributions and the contributions of my co-authors to each of the studies. A version of Chapter 2 has been published as “Zhan, S. H., Glick, L., Tsigenopoulos, C. S., Otto, S. P., & Mayrose, I. 2014. Comparative analysis reveals that polyploidy does not decelerate diversification in fish. J. Evol. Biol. 27: 391–403”. I assembled the chromosome number and phylogenetic data, and performed the BiSSE analyses. L. Glick performed the ChromEvol analysis on the Cyprinidae data set. C. S. Tsigenopoulos, S. P. Otto, I. Mayrose, and I interpreted the results. S. P. Otto, I. Mayrose, and I jointly wrote the manuscript. A version of Chapter 3 has been published as “Zhan, S. H., Drori, M., Goldberg, E. E., Otto, S. P., & Mayrose, I. 2016. Phylogenetic evidence for cladogenetic polyploidization in land plants. Am. J. Bot. 103: 1252–1258”. I performed the analysis. M. Drori collected the PloiDB data. S. P. Otto performed the mathematical analysis showing the uniformity of the prior distribution of the proportion of cladogenetic shifts. E. E. Goldberg, S.P. Otto, I. Mayrose, and I interpreted the results together. I wrote the manuscript with editing help from S. P. Otto and I. Mayrose. A version of Chapter 4 has been submitted as “Zhan, S. H., Hsieh, T. Y., Yeh, L. W., Kuo, T. C., Suda, S., & S. L. Liu. Hidden introductions of freshwater red algae via the aquarium trade exposed by DNA barcodes.” Also, the version is available on bioRxiv (https://www.biorxiv.org/content/10.1101/2020.06.30.180042v1). At the time that this document was finalized, some of the supplemental materials were being deposited on Dryad Repository (DOI: doi:10.5061/dryad.3n5tb2rf8). S. L. Liu and I conceived the project. S. L. Liu and T. Y. v Hsieh designed the study. S. L. Liu, T. Y. Hsieh, S. Suda, and I performed specimen collection and laboratory experiment. S. L. Liu, L. W., Yeh, and T. C. Kuo analyzed the data. S. L. Liu and I jointly interpreted the results and wrote the manuscript. A version of Chapter 5 has been published as “Zhan, S. H., Shih, C. C., & Liu, S. L. 2020. Reappraising plastid markers of the red algae for phylogenetic community ecology in the genomic era. Ecol. Evol. 10: 1299–1310.” S. L. Liu and I conceived the project. I developed and implemented the methodology and analyzed the data. C. C. Shih and S. L. Liu conducted the experiments. S. L. Liu and I interpreted the results and wrote the manuscript together. vi Table of Contents Abstract ....................................................................................................................................iii Lay Summary ........................................................................................................................... iv Preface ....................................................................................................................................... v Table of Contents .................................................................................................................... vii List of Tables ........................................................................................................................... xii List of Figures ........................................................................................................................ xiii Acknowledgements ................................................................................................................ xiv Dedication............................................................................................................................... xvi Introduction............................................................................................................ 1 Scientific background .................................................................................................. 1 Evolutionary consequences of whole genome duplication ............................................ 2 Invasion biology of freshwater red algae ...................................................................... 7 Community ecology of the red algae ............................................................................ 9 Remarks .................................................................................................................... 11 Comparative analysis reveals that polyploidy does not decelerate diversification in fish ....................................................................................................................................... 13 Overview ................................................................................................................... 13 Introduction ............................................................................................................... 14 Materials and Methods .............................................................................................. 17 2.3.1 Sequence datasets and ploidy level assignments ..................................................... 17 2.3.2 Phylogenetic reconstruction ..................................................................................